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PREFACE
‘Anatomy is the basis of medical discourse.’ As a general rule, the orientation of diagrams and photographs
(Hippocrates, De locis in homine 2) throughout the book has been standardized to show the left side of the
body, irrespective of whether a lateral or medial view is presented, and
Looking through an almost complete set of the previous editions of transverse sections are viewed from below to facilitate comparison with
Gray’s Anatomy, I am struck by the marked difference in size between clinical images. Clinicopathological examples have been selected where
the first and fortieth editions. That progressive increase in girth has the pathology is either a direct result, or a consequence, of the anatomy,
occurred pari passu with groundbreaking advances in basic science and or where the anatomical features are instrumental in the diagnosis/
clinical medicine over the past 155 years. Anatomy has become a far treatment/management of the condition. Wherever possible, the photo
wider discipline than Henry Gray, Henry van Dyke Carter or any of their micrographs illustrate human histology and embryology; nonhuman
students could have envisaged. Fields such as cell biology, molecular sources are acknowledged in the captions.
genetics, neuroanatomy, embryology and bioinformatics either had not In an ideal world, anatomical terminology would satisfy both anat
emerged or were in their infancy in 1858. Techniques that today inform omists and clinicians. For the avoidance of doubt, the same word
our view of the internal landscape of the body – such as specialized should be agreed and used for each structure that is described, whether
types of light and electron microscopy; imaging modalities, including in the anatomy laboratory or the clinic. In the real world, this goal is
Xrays, magnetic resonance imaging, computed tomography and ultra achieved with varying degrees of success; alternative terms (co)exist and
sonography; the use of ‘soft’ perfusion techniques and frozenthawed, may (and frequently do) confuse or frustrate. Currently, Terminologia
unembalmed cadavers for dissectionbased studies; and the advances Anatomica (TA)1 is the reference source for the terminology for macro
in information technology that enable endoscopic and robotic surgery scopic anatomy; the text of the fortyfirst edition of Gray’s Anatomy is
and facilitate minimally invasive access to structures previously consid almost entirely TAcompliant. However, where terminology is at vari
ered inaccessible – were all unknown. As each development entered ance with, or, more likely, is not included in, the TA, the alternative
mainstream scientific or clinical use, the new perspectives on the body term that is chosen either is cited in the relevant consensus document
it afforded, whether at submicroscopic or macroscopic level, filtered or position paper – e.g. ‘European Position Paper on the Anatomical
into the pages of Gray’s Anatomy: for example, the introduction of Xray Terminology of the Internal Nose and Paranasal Sinuses’2 and the Inter
plates (twentyseventh edition, 1938) and electron micrographs (thirty national Interdisciplinary Consensus Statement on the ‘Nomenclature
second edition, 1958). of the Veins of the Lower Limbs’3 – or enjoys widespread clinical usage:
In the Preface to the first edition, Henry Gray wrote that ‘This Work for example, the use of attitudinally appropriate terms in cardiology
is intended to furnish the Student and Practitioner with an accurate view of (see Chapter 57). The continued use of eponyms is contentious.4 Pro
the Anatomy of the Human Body, and more especially the application of this ponents of their retention argue that some eponyms are entrenched in
science to Practical Surgery.’ We remain true to his intention. An appropri medical language and are (therefore) indispensable, that they facilitate
ate knowledge of clinically relevant, evidencebased anatomy is an communication because their use is so pervasive and that they serve to
essential element in the armamentarium of a practising clinician; remind us of the humanism of medicine. Detractors argue that eponyms
indeed, ‘If anything, the relevance of anatomy in surgery is more impor are inherently inaccurate, nonscientific and often undeserved. In this
tant now than at any other time in the past’ (Tubbs, in Preface Com edition of Gray’s Anatomy, synonyms and eponyms are given in paren
mentary, which accompanies this volume). theses on first usage of a preferred term and not shown thereafter in the
In my Preface to the fortieth edition, I intimated that the book was text; an updated list of eponyms remains available in the ebook for
quite literally in danger of breaking its binding if any more pages were reference purposes.
added. In order to avoid this unfortunate occurrence, the fortyfirst I offer my sincere thanks to the editorial team at Elsevier, initially
edition contains a significant amount of material that is exclusively under the leadership of Madelene Hyde and latterly of Jeremy Bowes,
electronic, in the form of 77,000 words of additional text, 300 artworks for their guidance, professionalism, good humour and unfailing
and tables, 28 videos and 24 specially invited commentaries on topics support. In particular, I thank Poppy Garraway, Humayra Rahman
as diverse as electron microscopy and fluorescence microscopy; the Khan, Wendy Lee, Joanna Souch, Julie Taylor, Jan Ross and Louise Cook,
neurovascular bundles of the prostate; stem cells in regenerative medi for being at the end of a phone or available by email whenever I needed
cine; the anatomy of facial ageing; and technical aspects and applica advice or support.
tions of diagnostic radiology. In keeping with the expectation that I dedicate my work on the fortyfirst edition of Gray’s Anatomy to the
anatomy should be evidencebased, the fortyfirst edition contains memory of my late husband, Guy Standring.
many more references in the ebook than could be included in the
thirtyninth and fortieth printed editions. Susan Standring
Neel Anand, Rolfe Birch, Pat Collins, Alan Crossman, Michael January 2015
Gleeson, Ariana Smith, Jonathan Spratt, Mark Stringer, Shane Tubbs,
Alan Wein and Caroline Wigley brought a wealth of scholarship and
experience as anatomists, cell biologists and clinicians to their roles as
Section Editors. I thank them for their dedication and enthusiastic
support, in selecting and interacting with the authors in their Sections
and for meeting deadlines, despite the everincreasing demands on 1Terminologia Anatomica (1998) is the joint creation of the Federative Committee on
Anatomical Terminology (FCAT) and the Member Associations of the Interna
their time from university and/or hospital managers. Pat Collins,
tional Federation of Associations of Anatomists (IFAA).
Girish Jawaheer, Richard Tunstall and Caroline Wigley worked closely
2Lund VJ, Stammberger H, Fokkens WJ et al 2014 European position paper on the
with many authors to update the text and artworks for organogenesis,
anatomical terminology of the internal nose and paranasal sinuses. Rhinol Suppl
paediatric anatomy, evidencebased surface anatomy and microstruc 24:1–34.
ture, respectively, across Sections 3 to 9. Jonathan Spratt acted as both 3Caggiati A, Bergan JJ, Gloviczki P et al; International Interdisciplinary Consensus
a Section Editor (thorax) and an indefatigable ‘go to’ for sourcing Committee on Venous Anatomical Terminology 2005 Nomenclature of the veins
images throughout the book; in the latter capacity, he has produced of the lower limb: extensions, refinements, and clinical application. J Vasc Surg
a superb collection of additional labelled images, available in the 41:719–24.
ebook (see Bonus imaging collection). Over a hundred highly experi 4Amarnani A, Brodell RT, Mostow EN 2013 Finding the evidence with eponyms. JAMA
Dermatol 149:664–5; Fargen KM, Hoh BL 2014 The debate over eponyms. Clin
enced anatomists and clinicians contributed text, often extensively
Anat 27:1137–40; Lo WB, Ellis H 2010 The circle before Willis: a historical account
revised from the previous edition, and/or artworks, original micro of the intracranial anastomosis. Neurosurgery 66:7–18; Ma L, Chung KC 2012 In
graphs or other images to individual chapters. defense of eponyms. Plast Reconstr Surg 129:896e–8e. ix | 9 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
The continuing relevance of anatomy in
PREFACE
current surgical practice and research
COMMENTARY
R Shane Tubbs
When our anatomy forebears embarked on the uncharted study of the muscle. This distally disconnected medial half of the nerve was then
human body, they did so without reference. Their focus was to chart swung medially to the phrenic nerve, which had been transected proxi-
and map the body simply to learn and describe intricacies never chroni- mally. The two nerves were then sutured together without tension. This
cled before. The anatomical ‘map’ we use today came about thanks to ‘rearranging’ of human anatomy has now been employed clinically with
figures such as da Vinci, Vesalius, Cheselden and, more recently, Henry success. Yang et al (2011) used our study results to treat a 44-year-old
Gray. On the shoulders of these giants, we see farther than our predeces- man with complete spinal cord injury at the C2 level. Clinically, left
sors. In The Metalogicon, published in 1159, John Salisbury recognized diaphragm activity was decreased and the right diaphragm was com-
the profound observation of French philosopher Bernard of Chartres, pletely paralysed. Four weeks after surgery, training of the synchronous
who declared that ‘...we are like dwarfs on the shoulders of giants, so that activities of trapezius and inspiration was conducted. Six months after
we can see more than they, and things at a greater distance, not by virtue of surgery, motion was observed in the previously paralysed right dia-
any sharpness of sight on our part, or any physical distinction, but because phragm. Evaluation of lung function indicated improvements in vital
we are carried high and raised up by their giant size’. So, with the gross capacity and tidal volume. The patient was able to sit in a wheelchair
anatomy of man presumed, by many scholars, to have been described and conduct activities without assisted ventilation 12 months after
and understood long ago, how does the modern anatomist bring rel- surgery. For the surgeon, such manipulation of anatomy requires a
evance to the continued study of morphology? Is there any uncharted comprehensive understanding not only of normal anatomy but also of
territory for the modern anatomist to plot in order to sustain our field what might occur functionally by rewiring such nerves. For example,
of study and for it to continue to be perceived as relevant to an educa- patients undergoing this surgery will initially need to think of moving
tional world, and to medical and dental curricula in which the time their trapezius to activate their diaphragm. With time, this will not be
allotted to anatomical study has significantly waned? Simply put, yes. the case. Similar illustrations of the plasticity of the brain have been
Henry Gray, based on the title of his original text, Anatomy, Descriptive seen in patients undergoing hypoglossal to facial nerve neurotization
and Surgical, knew very well that there was a need to refocus the lenses procedures; these patients at first need to think of moving their tongue
of teaching and research in the anatomical sciences, and to expand and in order for their facial muscles to contract.
explore their surgical relevance. Our gross anatomical map of the Rewiring of nerves has been addressed in other studies. Thus, we
human body must continue to be updated and legends must continue have shown, first in a cadaveric study (Hansasuta et al 2001) and then
to be placed on that map to incorporate modern advances in technol- clinically (Wellons et al 2009), that the medial pectoral nerve can be
ogy. New methods of surgery, such as laparoscopy and endoscopy, as sectioned near its entrance into the deep surface of pectoralis major and
well as the use of the surgical microscope, offer the opportunity to view swung round and sewn into the musculocutaneous nerve (Fig. 1.6.2).
the human form in a different light and in greater surgical detail than If this procedure is successful, axonal regrowth from the medial pectoral
ever before. If anything, the relevance of anatomy in surgery is more nerve into the musculocutaneous nerve (about 1 mm/day) will
important now than at any other time in the past. The modern surgeon re-establish function in the anterior arm muscles; the loss of clinically
must take what is learned macroscopically, in the dissection room, and significant function of the dually innervated pectoralis major is minimal
apply this knowledge to structures seen under magnification and and the functional gain of having the anterior arm muscles work is
through instruments that provide a surgical field that is, at times, just significant (Wellons et al 2009). Being able to bring the hand to the
millimetres in diameter. Therefore, attention to anatomical detail is of mouth and feed oneself is a task that most take for granted. In children
vital importance as references and anatomical landmarks are mini- with birth-related injuries to the upper brachial plexus (i.e. Erb’s palsy),
mized in the surgical theatre of the new millennium. this movement is often the difference between waiting to be fed or
As mentioned before, early anatomists dissected with curiosity about feeding oneself. This method has been used at our institution for over
the unknown and gained knowledge that would become a prerequisite 15 years with an 80% success rate, where success is measured as the
for proper surgical manœuvres. Today, as anatomists, our anatomical patient regaining function of arm flexion.
knowledge should create in us a curiosity about what we can do with Another example of what we have termed ‘reverse translational
the knowledge that we have gained. The ability to apply that knowledge research in anatomy’ (i.e. from the bed to the bench and back) is the
offers an opportunity to be an integral part of the ever-progressing field location of new anatomical diversionary sites (in this case, the medul-
of surgery. For example, today, surgical problems are often the impetus lary cavity of the ilium) that could be used in patients with cerebrospi-
for dissection studies, which can influence the way in which surgery is nal fluid absorption problems (i.e. hydrocephalus) and in whom the
performed and, moreover, can sway the way in which anatomy is taught traditionally used receptacles for absorbing this diverted cerebrospinal
(e.g. redefining a focus in condensed curricula and with decreased work fluid (e.g. peritoneal and pleural cavities, heart) are not options, as a
hours for house officers). Surgically, dissection studies have allowed us consequence of e.g. malabsorption or local infection (Tubbs et al 2015)
to manipulate known human anatomy and to solve, for example, (Fig. 1.6.3). This alternative site has, for the first time, just been used
complex neurological problems. As an illustration of the surgical rele- and with success (unpublished data). Although not proven clinically,
vance of modern-day anatomical studies for neurological pathologies, an earlier study in primates showed that the manubrium of the sternum
we have conducted, in my laboratory, cadaveric feasibility studies that could also be used as a distal receptacle for cerebrospinal fluid collec-
suggested that the phrenic nerve could be reinnervated in high quadri- tion (Tubbs et al 2011). After tubing was tunnelled from the cannulated
plegic patients who are ventilator-dependent (a morbid condition with ventricle, the distal tubing was inserted subcutaneously into the supe-
an associated high mortality rate) by using the intact, adjacent accessory rior aspect of the midline manubrium, where a small hole had been
nerve (i.e. neurotization) (Tubbs et al 2008a) (Fig. 1.6.1). The theory drilled. Up to 50 ml of saline per hour could be infused into the primate
behind this investigation was that the functioning accessory nerve sternum without vital sign changes. This study, and the study using the
would be used to form a new circuit between it and the dysfunctional ilium as a depository, both demonstrate the anatomical continuity
phrenic nerve, and that this would allow recovery of diaphragm func- between the bony medullary cavities and the vascular system. Such
tion. For this technique, a longitudinal incision was made along the positive effects on patient outcomes not only make the study of human
lower half of the posterior border of sternocleidomastoid. Dissection anatomy from a slanted perspective extremely gratifying, but are also
was then performed in order to identify both the accessory nerve at this practical since the results have direct application in the surgical theatre.
level, at its entrance into trapezius, and the phrenic nerve crossing In addition to surgical anatomy playing a role in new uses of the
anterior to scalenus anterior. The medial half of the accessory nerve was normal anatomy, this field can also explore and direct new surgical
then split away from its lateral half and transected at its entrance into approaches where the goals are to make surgery more effective and e1 | 10 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
The conTinuing relevance of anaTomy in currenT surgical pracTice and research
Fig. 1.6.1 A schematic representation of the
anatomically defined technique of using the
accessory nerve for neurotization of the phrenic
nerve with application to patients with high
cervical quadriplegia who are ventilator-
dependent. With nerve regrowth, axons from the
intact and functioning accessory nerve travel into
the phrenic nerve to reinnervate this nerve and
restore diaphragmatic function. In this example,
only one-half of the accessory nerve is used in
order to maintain some function of trapezius.
(Drawn by Mr David Fisher.)
Fig. 1.6.2 The neurotization of the
musculocutaneous nerve with the medial pectoral
nerve (inset). Similar to the example illustrated in
Figure 1.6.1, such a method of nerve repair is
employed in the hope that a patient with an upper
brachial plexus injury and anterior arm muscles
that are dysfunctional can regain function by
regrowth of axons from the intact medial pectoral
nerve into and along the musculocutaneous nerve.
(Drawn by Mr David Fisher.)
minimally invasive, and involve fewer complications. For example, we treatment, resulted in a more limited laminectomy and myelotomy,
have performed feasibility studies looking at a wide range of novel and, in one case, assisted in identifying a residual spinal cord tumour.
approaches that might be used by the surgeon. These include a dorsal It was also useful in the fenestration of a multilevel spinal arachnoid
approach to the carpal tunnel for an entrapped median nerve (Tubbs cyst and in confirming communication of fluid spaces in the setting of
et al 2005a); an anterior approach to the sciatic nerve potentially com- a complex holocord syrinx. Endoscopy aided the visualization of the
pressed by piriformis via the obturator foramen (Tubbs, unpublished spinal cord to ensure the absence of tethering in the case of split spinal
data); an anterior approach to the upper thoracic vertebrae for spine cord malformation. These endoscopic approaches were only possible
fusion procedures (Tubbs et al 2010a); an intra-abdominal laparoscopic by knowing the normal anatomy and how it appears in a confined field
approach to decompress the pudendal nerve (Loukas et al 2008); and of view, as first seen in the anatomy laboratory.
midline endoscopic approaches to the fourth ventricle with application Lastly, the anatomist can add to the relevance of anatomy for the
to decompressing a ‘trapped’ fourth ventricle, as is seen in some cases surgeon with studies that have an impact on the identification or avoid-
of hydrocephalus (Tubbs et al 2004). We have also explored the feasibil- ance of important structures during operative manœuvres (i.e. anatomi-
ity in cadavers of using endoscopy for exploration of pathologies of the cal landmark studies). My group has defined surgical landmarks for
thecal sac (Chern et al 2011). In a series of children with intraspinal anatomical structures such as the superior and inferior gluteal nerves
pathology (arachnoid cyst, spinal cord tumour, holocord syrinx and (Apaydin et al 2013, Apaydin et al 2009); vein of Labbé (Tubbs et al
e2 split cord malformation), intradural spinal endoscopy was a useful 2012); sigmoid sinus (Tubbs et al 2009a); amygdala (Tubbs et al | 11 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
The continuing relevance of anatomy in current surgical practice and research
Fig. 1.6.4 A superior view of the cranium, with the underlying superior
sagittal sinus, cortical veins and lateral lacunae illustrated. This study
explored the relationship between the underlying lateral lacunae and the
overlying coronal and sagittal sutures, and made measurements between
these structures. Neurosurgically, the initial placement of burr-holes
avoids the midline in order to prevent damage to the superior sagittal
sinus. However, the intracranial entrance of the drill often injures more
laterally placed lacunae. Using surface anatomy based on anatomical
landmarks, a neurosurgeon can be more aware of the locations of these
underlying structures while performing craniotomies. Such landmarks
have now been used by neurosurgeons at our institution. (Drawn by Mr
David Fisher.)
(Loukas et al 2006); long thoracic nerve (Tubbs et al 2006b); anterior
interosseous nerve (Tubbs et al 2006c); accessory nerve (Tubbs et al
2005b); lumbar plexus and its branches (Tubbs et al 2005c); trochlear
nerve (Tubbs and Oakes 1998); and frontal sinus (Tubbs et al 2002).
Such studies might assist in decreasing the morbidity and increasing
Fig. 1.6.3 The technique used in a patient with hydrocephalus to divert the efficiency of surgical approaches and certainly illustrate the surgical
cerebrospinal fluid from the cerebral ventricles to the ilium. The enlarged relevance of anatomy. Moreover, this list exemplifies the multitude of
ventricles are cannulated with a catheter connected to a subcutaneous anatomical structures that may be given greater surgical relevance by
valve that drains into tubing tunnelled under the skin and then implanted addressing how they may be more accurately located in the operating
into the medullary cavity of the ilium; here, the cerebrospinal fluid is theatre.
absorbed into the vascular system. The techniques described in Figures
In this day and age, if anatomists are not to lose their footing and
1.6.2 and 1.6.3, based on surgical problems and manipulation of known
simply be considered teachers of an old and outdated discipline, the
anatomy for surgical benefit, were evaluated and studied in the anatomy
onus is on us to renew interest in our field with timely and salient
laboratory, and have now been used clinically. (Drawn by Mr David
studies that gird the loins of a profession that is in danger of becoming
Fisher.)
extinct. It is my opinion, and that of others, that one effective way to
achieve this is to remind the world by demonstrations such as those
listed here that the study of anatomy is as clinically relevant today as it
2010b); buccal branch of the trigeminal nerve (Tubbs et al 2010c); was at its humble beginnings. Considering the adage that anatomy is
radial nerve and posterior interosseous branch (Cox et al 2010, Tubbs the oldest child of Mother Medicine, the fact that surgical problems and
et al 2006a); perineal branch of the posterior femoral cutaneous nerve anatomical studies go hand in hand is obvious – anatomical research
(Tubbs et al 2009b); lateral lacunae (Tubbs et al 2008b) (Fig. 1.6.4); is not a ‘dead’ science! The modern relevance of anatomy to surgical
basal vein of Rosenthal (Tubbs et al 2007); greater occipital nerve practice and research must not be underestimated.
REFERENCES
Apaydin N, Bozkurt M, Loukas M et al 2009 The course of the inferior gluteal Apaydin N, Kendir S, Loukas M et al 2013 Surgical anatomy of the superior
nerve and surgical landmarks for its localization during posterior gluteal nerve and landmarks for its localization during minimally inva-
approaches to hip. Surg Radiol Anat 31:415-18. sive approaches to the hip. Clin Anat 26:614–20. e3 | 12 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
The conTinuing relevance of anaTomy in currenT surgical pracTice and research
Chern JJ, Gordon AS, Naftel RP et al 2011 Intradural spinal endoscopy in Tubbs RS, Miller JH, Cohen-Gadol AA et al 2010b Intraoperative anatomic
children. J Neurosurg Pediatr 8:107–11. landmarks for resection of the amygdala during medial temporal lobe
Cox CL, Riherd D, Tubbs RS et al 2010 Predicting radial nerve location using surgery. Neurosurgery 66:974–7.
palpable landmarks. Clin Anat 23:420–6. Tubbs RS, Miller J, Loukas M et al 2009b Surgical and anatomical landmarks
Hansasuta A, Tubbs RS, Grabb PA 2001 Surgical relationship of the medial for the perineal branch of the posterior femoral cutaneous nerve: impli-
pectoral nerve to the musculocutaneous nerve: a cadaveric study. Neuro- cations in perineal pain syndromes. Laboratory investigation. J Neuro-
surgery 48:203–6. surg 111:332–5.
Loukas M, El-Sedfy A, Tubbs RS et al 2006 Identification of greater occipital Tubbs RS, Oakes WJ 1998 Relationships of the cisternal segment of the
nerve landmarks for the treatment of occipital neuralgia. Folia Morphol trochlear nerve. J Neurosurg 89:1015–19.
(Warsz) 65:337–42. Tubbs RS, Pearson B, Loukas M 2008a Phrenic nerve neurotization utilizing
Loukas M, Louis RG Jr, Tubbs RS et al 2008 Intra-abdominal laparoscopic the spinal accessory nerve: technical note with potential application in
pudendal canal decompression – a feasibility study. Surg Endosc 22: patients with high cervical quadriplegia. Childs Nerv Syst 24:1341–4.
1525–32. Tubbs RS, Salter EG, Custis JW et al 2006b Surgical anatomy of the cervical
Tubbs RS, Bauer D, Chambers MR 2011 A novel method for cerebrospinal and infraclavicular parts of the long thoracic nerve. J Neurosurg 104:
fluid diversion: a cadaveric and animal study. Neurosurgery 68:491–4. 792–5.
Tubbs RS, Custis JW, Salter EG et al 2006c Quantitation of and superficial Tubbs RS, Salter EG, Sheetz J et al 2005a Novel surgical approach to the
surgical landmarks for the anterior interosseous nerve. J Neurosurg carpal tunnel: cadaveric feasibility study. Clin Anat 18:350–6.
104:787–91. Tubbs RS, Salter EG, Wellons JC 3rd et al 2005b Superficial landmarks for
Tubbs RS, Elton S, Salter G et al 2002 Superficial surgical landmarks for the the spinal accessory nerve within the posterior cervical triangle. J Neu-
frontal sinus. J Neurosurg 96:320–2. rosurg Spine 3:375–8.
Tubbs RS, Johnson PC, Loukas M et al 2010c Anatomical landmarks for Tubbs RS, Salter EG, Wellons JC 3rd et al 2005c Anatomical landmarks for
localizing the buccal branch of the trigeminal nerve on the face. Surg the lumbar plexus on the posterior abdominal wall. J Neurosurg Spine
Radiol Anat 3:933–5. 2:335–8.
Tubbs RS, Louis RG Jr, Song YB et al 2012 External landmarks for identifying Tubbs RS, Salter EG, Wellons JC 3rd et al 2006a Superficial surgical land-
the drainage site of the vein of Labbé: application to neurosurgical marks for identifying the posterior interosseous nerve. J Neurosurg
procedures. Br J Neurosurg 26:383–5. 104:796–9.
Tubbs RS, Loukas M, Callahan JD et al 2010a A novel approach to the upper Tubbs RS, Tubbs I, Loukas M et al 2015 Ventriculoiliac shunt: a cadaveric
anterior thoracic spine: a cadaveric feasibility study. J Neurosurg Spine feasibility study. J Neurosurg Pediatr 15:310–12.
13:346–50. Tubbs RS, Wellons JC 3rd, Salter G et al 2004 Fenestration of the superior
Tubbs RS, Loukas M, Louis RG Jr et al 2007 Surgical anatomy and landmarks medullary velum as treatment for a trapped fourth ventricle: a feasibility
for the basal vein of Rosenthal. J Neurosurg 106:900–2. study. Clin Anat 17:82–7.
Tubbs RS, Loukas M, Shoja MM et al 2008b Lateral lakes of Trolard: anatomy, Wellons JC, Tubbs RS, Pugh JA et al 2009 Medial pectoral nerve to muscu-
quantitation, and surgical landmarks. Laboratory investigation. J Neu- locutaneous nerve neurotization for the treatment of persistent birth-
rosurg 108:1005–9. related brachial plexus palsy: an 11-year institutional experience.
J Neurosurg Pediatr 3:348–53.
Tubbs RS, Loukas M, Shoja MM et al 2009a Surface landmarks for the junc-
tion between the transverse and sigmoid sinuses: application of the Yang ML, Li JJ, Zhang SC 2011 Functional restoration of the paralyzed dia-
‘strategic’ burr hole for suboccipital craniotomy. Neurosurgery 65: phragm in high cervical quadriplegia via phrenic nerve neurotization
37–41. utilizing the functional spinal accessory nerve. J Neurosurg Spine 15:
190–4.
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ACKNOWLEDGEMENTS
Within individual figure captions, we have acknowledged all figures kindly loaned from other sources. However, we
would particularly like to thank the following authors who have generously loaned so many figures from other
books published by Elsevier:
Drake RL, Vogl AW, Mitchell A (eds), Gray’s Anatomy for Students, 2nd ed. Elsevier, Churchill Livingstone. Copyright
2010.
Drake RL, Vogl AW, Mitchell A, Tibbitts R, Richardson P (eds), Gray’s Atlas of Anatomy. Elsevier, Churchill
Livingstone. Copyright 2008.
Waschke J, Paulsen F (eds), Sobotta Atlas of Human Anatomy, 15th ed. Elsevier, Urban & Fischer. Copyright 2013.
Acknowledgements for paediatric anatomy content in chapter 45 to Ritchie Marcus, MD and Guirish A. Solanki, MD,
Birmingham Children’s Hospital, UK, and for chapter 81 to Christopher Edward Bache, MBChB, FRCS (Tr & Orth),
Birmingham, UK. The editors would like to thank all contributors and illustrators to the previous editions of Gray’s
Anatomy, including the fortieth and thirty-ninth editions. Much of the illustration in Gray’s Anatomy has as its basis
the work of illustrators and photographers who contributed towards earlier editions, their figures sometimes being
retained almost unchanged, and sometimes being used as the foundation for figures that are new to this edition.
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CONTRIBUTORS TO THE FORTY-FIRST EDITION
The editors would like to acknowledge and offer grateful thanks for the input of all previous editions’ contributors, without whom this new edition
would not have been possible.
Michael A Adams BSc, PhD Brion Benninger MD, MSc Graham J Burton MD, DSc, FMedSci
Professor of Biomechanics Professor, Executive Director Mary Marshall and Arthur Walton Professor
Centre for Comparative and Clinical Anatomy Medical Anatomy Center – Innovation and of the Physiology of Reproduction
University of Bristol, UK Technology Research Centre for Trophoblast Research
McDaniel Surgical, Radiological & Education University of Cambridge
L Max Almond MB, ChB, MRCS, MD Research Lab Cambridge, UK
Senior Registrar in Gastrointestinal Surgery Departments of Medical Anatomical
West Midlands Deanery Sciences & Neuromuscular Medicine Andrew Bush MD, FRCP, FRCPCH, FERS
Birmingham, UK Western University of Health Sciences, Professor of Paediatrics and Head of Section
Lebanon, Oregon (Paediatrics)
Neel Anand MD Faculty Orthopaedics & Surgical Residency Imperial College;
Clinical Professor of Surgery Training Professor of Paediatric Respirology
Director, Spine Trauma, Minimally Invasive Faculty Sports Medicine Fellowship Training National Heart and Lung Institute;
Spine Surgery Samaritan Health Services, Corvallis, Oregon Consultant Paediatric Chest Physician
Spine Center USA Royal Brompton and Harefield NHS
Cedars Sinai Medical Center Foundation Trust
Los Angeles, CA, USA Barry KB Berkovitz BDS, MSc, PhD, FDS, Paediatric Respiratory Medicine
LDSRCS(Eng) London, UK
Nihal Apaydin MD, PhD Emeritus Reader in Dental Anatomy
Associate Professor of Anatomy Anatomy Department Alison Campbell BSc(Hons), MMedSci,
Department of Anatomy and Brain Research King’s College London DipRCPath
Center London, UK; Group Director of Embryology
Ankara University Faculty of Medicine Visiting Professor CARE Fertility
Ankara, Turkey Oman Dental College Nottingham, UK
Oman
Lily A Arya MD, MS Bodo EA Christ MD
Associate Professor of Obstetrics and Leela C Biant BSc(Hons), MBBS, AFRCSEd, Professor and Former Chairman
Gynecology FRCSEd(Tr & Orth), MSres(Lond), MFSTEd Department of Molecular Embryology
Perelman School of Medicine Consultant Trauma and Orthopaedic University of Freiburg
University of Pennsylvania Surgeon Freiburg, Germany
Department of Obstetrics and Gynecology Royal Infirmary of Edinburgh;
Philadelphia, PA, USA Honorary Senior Lecturer Thomas Collin MBBS, FRCS(Plast)
University of Edinburgh Consultant Plastic and Reconstructive Surgeon
Tipu Aziz FMedSci NRS Career Clinician Scientist Fellow University Hospital of North Durham
Professor of Neurosurgery Edinburgh, UK Department of Plastic Surgery
John Radcliffe Hospital Durham, UK
University of Oxford Rolfe Birch MChir, FRCPS(Glasg),
Oxford, UK FRCS(Ed), FRCS(Eng) Patricia Collins BSc, PhD, FHEA
Retired Consultant in Charge Professor of Anatomy
Jonathan BL Bard MA, PhD War Nerve Injury Clinic, Defence Medical Anglo-European College of Chiropractic
Emeritus Professor of Development and Rehabilitation Centre, Surrey; Bournemouth, UK;
Bioinformatics Retired Head, Peripheral Nerve Injury Unit, Editor for Embryology and Development
School of Biomedical Sciences Royal National Orthopaedic Hospital;
University of Edinburgh Professor in Neurological Orthopaedic Anthony T Corcoran MD
Edinburgh, UK Surgery, University College of London Assistant Professor of Urologic Oncology
London, UK and Minimally Invasive Surgery
Eli M Baron MD Department of Urology
Clinical Associate Professor of Neurosurgery Martin A Birchall MD, FRCS, FMedSci SUNY Stony Brook School of Medicine
Spine Surgeon, Cedars Sinai Professor of Laryngology Stony Brook, NY, USA
Department of Neurosurgery Consultant Otolaryngologist, Ear Institute
Cedars Sinai Spine Center, Cedars Sinai University College London and Royal Julie Cox FRCS(Eng), FRCR
Medical Center National Throat Nose and Ear Hospital Consultant Radiologist
Los Angeles, CA, USA University College Hospitals NHS Foundation City Hospitals Sunderland NHS
Trust Foundation Trust Sunderland, UK
Hugh Barr MD(Dist), ChM, FRCS(Eng), London, UK
FRCS(Ed), FHEA, FODI Alan R Crossman BSc, PhD, DSc
Consultant General and Gastrointestinal Sue Black OBE, BSc, PhD, DSc, FRSE, Professor Emeritus
Surgeon FRAI, FRCP, FSB University of Manchester
Oesophagogastric Resection Unit Professor of Anatomy and Forensic Manchester, UK
Gloucestershire Royal Hospital Anthropology
Gloucester, UK Centre for Anatomy and Human Identification
University of Dundee
Scotland, UK
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Contributors to the forty-first edition
Natalie M Cummings BSc(Med Sci), Simon M Gabe MD, MSc, BSc(Hons), Duane E Haines PhD, FAAAS, FAAA
MB ChB, MPhil, MD, MRCP(Ed) MBBS, FRCP Professor, Department of Neurobiology and
Consultant Respiratory Physician Consultant Gastroenterologist and Honorary Anatomy;
University Hospital of North Durham Senior Lecturer; Professor, Department of Neurology
Durham, UK Co-Chair of the Lennard-Jones Intestinal Wake Forest School of Medicine
Failure Unit, St Mark’s Hospital Winston-Salem, NC;
Anthony V D’Antoni MS, DC, PhD Middlesex, UK Professor Emeritus, University of Mississippi
Clinical Professor and Director of Anatomy Medical Center
Department of Pathobiology Andrew JT George MA, PhD, DSc, Jackson, MS, USA
Sophie Davis School of Biomedical Education FRCPath, FSB
City University of New York; Deputy Vice Chancellor (Education and Peter A Helliwell FIBMS, Cert BA, Cert Ed
Adjunct Associate Professor International) Head Biomedical Scientist
Division of Pre-Clinical Sciences and Professor of Immunology Department of Cellular Pathology
Department of Surgery Brunel University Royal Cornwall Hospitals Trust
New York College of Podiatric Medicine London, UK Truro, UK
New York, NY, USA
Serge Ginzburg MD Simon Holmes BDS, MBBS, FDS, RCS,
Paolo De Coppi MD, PhD Assistant Professor of Urologic Oncology FRCS
Professor of Paediatric Surgery; Division of Urology Professor of Craniofacial Traumatology
Head of Stem Cells and Regenerative Fox Chase Cancer Center; Department of Oral and Maxillofacial Surgery
Medicine; Department of Urology Royal London Hospital, Queen Mary
Consultant Paediatric Surgeon Albert Einstein Medical Center University of London
Great Ormond Street Hospital Philadelphia, PA, USA London, UK
UCL Institute of Child Health
London, UK Michael Gleeson MD, FRCS, FRACS Hons, Claire Hopkins MA (Oxon), FRCS
FDS Hons (ORLHNS), DM
John OL DeLancey MD Professor of Skull Base Surgery Consultant Ear, Nose and Throat Surgeon
Norman F Miller Professor of Gynecology University College London Guy’s and St Thomas’ Hospitals;
Department of Obstetrics and Gynecology The National Hospital for Neurology and Reader in ENT
Professor, Department of Urology Neurosurgery King’s College London
University of Michigan Medical School London, UK London, UK
Ann Arbor, MI, USA
Marc Goldstein MD, DSc(Hon), FACS Benjamin M Howe MD
Ronald H Douglas BSc, PhD Matthew P Hardy Distinguished Professor of Assistant Professor of Radiology
Professor of Visual Science Reproductive Medicine and Urology; Mayo Clinic
Division of Optometry and Visual Science Surgeon-in-Chief, Male Reproductive Rochester, MN, USA
School of Health Sciences Medicine and Surgery
City University London Cornell Institute for Reproductive Medicine Daisuke Izawa PhD
London, UK and Department of Urology Assistant Professor, Laboratory of
Weill Cornell Medical Center; Chromosome Dynamics
Barrie T Evans BDS(Hons), MB BCh, Adjunct Senior Scientist, Population Council, Institute of Molecular and Cellular
FRCS(Eng), FRCS(Ed), FDSRCS(Eng), Center for Biomedical Research Biosciences
FFDRCS(Ire) New York, NY, USA University of Tokyo
Consultant Oral and Maxillofacial Surgeon Tokyo, Japan
Southampton University Hospitals; Martin Götz MD, PhD
Honorary Senior Lecturer in Surgery to Professor, Interdisciplinary Endoscopy Eric Jauniaux MD, PhD, FRCOG
Southampton University Medical School; Universitätsklinikum Tübingen Professor in Obstetrics and Fetal Medicine
Civilian Consultant Advisor in Oral and Tübingen, Germany Academic Department of Obstetrics and
Maxillofacial Surgery to the Royal Navy; Gynaecology
Past President, British Association of Oral Anthony Graham BSc, PhD UCL EGA Institute for Women’s Health
and Maxillofacial Surgeons Professor of Developmental Biology University College London
Southampton, UK MRC Centre for Developmental Neurobiology London, UK
King’s College London
Juan C Fernandez-Miranda MD London, UK Girish Jawaheer MD, FRCS(Eng),
Associate Professor of Neurological Surgery; FRCS(Paed)
Associate Director, Center for Cranial Base Leonard P Griffiths MB ChB, MRCP(UK) Consultant Paediatric Surgeon
Surgery; Registrar in Gastroenterology and General Great North Children’s Hospital, Royal
Director, Surgical Neuroanatomy Laboratory Internal Medicine Victoria Infirmary
University of Pittsburgh Medical Center Royal United Hospital Bath; Newcastle upon Tyne NHS Foundation Trust
Pittsburgh, PA, USA Clinical Research Fellow Newcastle upon Tyne, UK;
University of Bath Formerly Specialty Tutor for Paediatric
Jonathan M Fishman BM BCh(Oxon), Bath, UK Surgery
MA(Cantab), MRCS(Eng), DOHNS, PhD Royal College of Surgeons of England
Clinical Lecturer Paul D Griffiths PhD, FRCR, FMedSci London, UK;
University College London Professor of Radiology, Academic Unit of Editor for Paediatric Anatomy
London, UK Radiology
University of Sheffield Marianne Juhler MD, DMSc
Roland A Fleck PhD, FRCPath, FRMS Sheffield, UK Consultant Neurosurgeon
Reader and Director, Centre for Copenhagen University Hospital;
Ultrastructural Imaging Thomas J Guzzo MD, MPH Professor of Neurosurgery
King’s College London Vice-Chief of Urology University Clinic of Neurosurgery
London, UK Assistant Professor of Urology Copenhagen, Denmark
Perelman School of Medicine
David N Furness BSc, PhD University of Pennsylvania Helmut Kettenmann PhD
Professor of Cellular Neuroscience Philadelphia, PA, USA Professor, Charité Universitätsmedizin Berlin
School of Life Sciences Max Delbrück Center for Molecular Medicine
Keele University in the Helmholtz Society
Newcastle-under-Lyme, UK Berlin, Germany
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Contributors to the forty-first edition
Abraham L Kierszenbaum MD, PhD Peter J Lunniss BSc, MS, FRCS Horia Muresian MD, PhD
Medical (Clinical) Professor Emeritus Retired Senior Lecturer Head of Cardiovascular Surgery Department
The Sophie Davis School of Biomedical Academic Surgical Unit, St Bartholomew’s University Hospital of Bucharest
Education and The London Medical College, Queen Bucharest, Romania;
The City University of New York Mary University London; Visiting Professor, St George’s University
New York, NY, USA Retired Honorary Consultant Colorectal School of Medicine
Surgeon Grenada, West Indies
Alexander Kutikov MD, FACS Royal London and Homerton Hospitals
Associate Professor of Urologic Oncology London, UK Robert P Myers MD, MS, FACS
Department of Surgical Oncology Professor Emeritus
Fox Chase Cancer Center, Temple University the late Joseph Mathew MBBS, FMCPath, Department of Urology
Health System FRCPath, CertTLHE, PGCE, CertBusStud, Mayo Clinic
Philadelphia, PA, USA FHEA Rochester, MN, USA
Consultant in Histopathology
Joey E Lai-Cheong BMedSci(Hons), MBBS, Department of Histopathology Donald A Neumann PT, PhD, FAPTA
PhD, MRCP(UK) Royal Cornwall Hospitals Trust Professor of Physical Therapy
Consultant Dermatologist Truro, UK Marquette University
King Edward VII Hospital (Frimley Health Milwaukee, WI, USA
NHS Foundation Trust) John A McGrath MD, FRCP, FMedSci
Windsor, UK Professor of Molecular Dermatology Dylan Myers Owen PhD
St John’s Institute of Dermatology Lecturer in Experimental Biophysics
Simon M Lambert BSc, MBBS, FRCS, King’s College London Department of Physics and Randall Division
FRCS(Ed) (Orth) London, UK of Cell and Molecular Biophysics
Consultant Orthopaedic Surgeon King’s College London
Shoulder and Elbow Service Stephen McHanwell BSc, PhD, FHEA, FLS, London, UK
Royal National Orthopaedic Hospital Trust CBiol FSB, NTF
Stanmore, Middlesex; Professor of Anatomical Sciences Erlick AC Pereira MA(Camb), DM(Oxf),
Honorary Senior Lecturer School of Medical Education and School of FRCS(Eng), FRCS(NeuroSurg), MBPsS,
Institute of Orthopaedics and Dental Sciences SFHEA
Musculoskeletal Science Faculty of Medical Sciences Senior Clinical Fellow in Complex Spinal
University College London Newcastle University Surgery
London, UK Newcastle upon Tyne, UK Guy’s and St Thomas’ Hospitals
National Hospital of Neurology and
John G Lawrenson MSc(Oxon), PhD, Akanksha Mehta MD Neurosurgery
FCOptom Assistant Professor of Urology, London, UK
Professor of Clinical Visual Science Emory University School of Medicine
Division of Optometry and Visual Science Atlanta, GA, USA Nancy Dugal Perrier MD, FACS
City University London Professor, Anderson Cancer Center
London, UK Bryan C Mendelson FRCS(Ed), FRACS, Department of Surgical Oncology
FACS Houston, TX, USA
Nir Lipsman MD, PhD Head of Faculty
Neurosurgery Resident Melbourne Advanced Facial Anatomy Clayton C Petro MD
University of Toronto Course; General Surgery Resident;
Toronto, ON, Canada Private Practitioner, Centre for Facial Plastic Allen Research Scholar
Surgery Department of General Surgery
J Peter A Lodge MD, FRCS Melbourne, VIC, Australia University Hospitals Case Medical Center
Professor of Surgery Cleveland, OH, USA
Hepatobiliary and Transplant Unit Zoltán Molnár MD, DPhil
St James’s University Hospital Professor of Developmental Neuroscience Andy Petroianu MD, PhD
Leeds, UK Department of Physiology, Anatomy and Professor of Surgery
Genetics Department of Surgery
Marios Loukas MD, PhD University of Oxford School of Medicine of the Federal University
Professor, Department of Anatomical Oxford, UK of Minas Gerais
Sciences Belo Horizonte, Minas Gerais, Brazil
Dean of Basic Sciences Antoon FM Moorman MD, PhD
St George’s University Professor of Embryology and Molecular Jonathon Pines PhD, FMedSci
Grenada, West Indies Biology of Cardiovascular Diseases Director of Research in Cell Division
Department of Anatomy, Embryology and University of Cambridge
Andres M Lozano MD, PhD, FRCSC, FRSC, Physiology Cambridge, UK
FCAHS University of Amsterdam, Academic Medical
Professor and Chairman, Center Alexander G Pitman BMedSci, MBBS,
Dan Family Chair in Neurosurgery Amsterdam, The Netherlands MMed(Rad), FRANZCR, FAANMS
University of Toronto Professorial Fellow
Department of Neurosurgery Gillian M Morriss-Kay DSc Department of Anatomy and Neuroscience
Toronto Western Hospital Emeritus Professor of Developmental Anatomy University of Melbourne
Toronto, ON, Canada Department of Physiology, Anatomy and Parkville, VIC, Australia
Genetics
Ellen A Lumpkin PhD University of Oxford Y Raja Rampersaud MD, FRCSC
Associate Professor of Somatosensory Oxford, UK Associate Professor, Division of Orthopaedic
Biology Surgery and Neurosurgery
Columbia University College of Physicians Donald Moss MB, BS, FRACS, FACS Department of Surgery
and Surgeons Consultant Urologist University of Toronto
Departments of Dermatology and of Ballarat, VIC, Australia Toronto, ON, Canada
Physiology and Cellular Biophysics
New York, NY, USA
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Contributors to the forty-first edition
Mettu Srinivas Reddy MS, FRCS, PhD Richard M Sharpe BSc, Msc, PhD, FRSE Susan Standring MBE, DSc, FKC, Hon FAS,
Consultant Surgeon Professor and Group Leader Hon FRCS
Institute of Liver Disease and Transplantation MRC Centre for Reproductive Health Emeritus Professor of Anatomy
Global Health City The Queen’s Medical Research Institute King’s College London
Chennai, India University of Edinburgh London, UK
Edinburgh, UK
Mohamed Rela MS, FRCS, DSc Ido Strauss MD, PhD
Director, Institute of Liver Disease and Mohammadali M Shoja MD Department of Neurosurgery
Transplantation Research Fellow Toronto Western Hospital
Global Health City, Chennai, India; Department of Neurosurgery Toronto, ON, Canada
Professor of Liver Surgery University of Alabama at Birmingham
Institute of Liver Studies, King’s College Birmingham, AL, USA Mark D Stringer BSc, MS, FRCP, FRCS,
Hospital FRCS(Ed), FRACS
London, UK Victoria L Shone PhD, MSc, BSc Professor of Paediatric Surgery
Research Associate in Developmental Christchurch Hospital;
Guilherme C Ribas MD Biology Honorary Professor of Anatomy
Professor of Surgery King’s College London University of Otago
University of São Paulo Medical School; London, UK Dunedin, New Zealand
Neurosurgeon, Hospital Israelita Albert
Einstein Monty Silverdale MD, PhD, FRCP Paul H Sugarbaker MD, FACS, FRCS
São Paulo, Brazil; Consultant Neurologist Medical Director, Center for Gastrointestinal
Visiting Professor of Neurosurgery Salford Royal NHS Foundation Trust; Malignancies;
University of Virginia Honorary Senior Lecturer in Neuroscience Chief, Program in Peritoneal Surface Oncology
Charlottesville, VA, USA University of Manchester MedStar Washington Hospital Center
Manchester, UK Washington, DC, USA
Bruce Richard MBBS, MS, FRCS(Plast)
Consultant Plastic Surgeon Jonathan MW Slack MA, PhD, FMedSci Cheryll Tickle MA, PhD
Birmingham Children’s Hospital Emeritus Professor, University of Bath Emeritus Professor
Birmingham, UK Bath, UK; Department of Biology and Biochemistry
Emeritus Professor, University of Minnesota, University of Bath
Michael J Rosen MD Minneapolis, MN, USA Bath, UK
Professor of Surgery;
Chief, Division of Gastrointestinal and Ariana L Smith MD Kimberly S Topp PT, PhD, FAAA
General Surgery Associate Professor of Urology Professor and Chair, Department of Physical
Case Medical Center Director of Pelvic Medicine and Therapy and Rehabilitation Science
Case Western Reserve University Reconstructive Surgery Professor, Department of Anatomy
University Hospitals of Cleveland Penn Medicine, Perelman School of University of California, San Francisco
Cleveland, OH, USA Medicine San Francisco, CA, USA
University of Pennsylvania Health System
Alistair C Ross MB, FRCS Philadelphia, PA, USA Drew A Torigian MD, MA, FSAR
Consultant Orthopaedic Surgeon Associate Professor of Radiology;
The Bath Clinic Carl H Snyderman MD, MBA Clinical Director, Medical Image Processing
Bath, UK Professor of Otolaryngology and Group
Neurological Surgery Department of Radiology
Stefano Sandrone PhD student Co-Director, UPMC Center for Cranial Base Hospital of the University of Pennsylvania
Neuroscientist, NatBrainLab Surgery Philadelphia, PA, USA
Sackler Institute of Translational University of Pittsburgh Medical Center
Neurodevelopment Pittsburgh, PA, USA David Tosh BSc, PhD
Department of Forensic and Professor of Stem Cell and Regenerative
Neurodevelopmental Sciences Jane C Sowden PhD Biology
Institute of Psychiatry, Psychology and Professor of Developmental Biology and Centre for Regenerative Medicine
Neuroscience Genetics University of Bath
King’s College London UCL Institute of Child Health Bath, UK
London, UK University College London
London, UK R Shane Tubbs MS, PA-C, PhD
Martin Scaal PhD Chief Scientific Officer
Professor of Anatomy and Developmental Robert J Spinner MD Seattle Science Foundation, Seattle, WA,
Biology Chair, Department of Neurologic Surgery USA;
Institute of Anatomy II Burton M Onofrio, MD Professor of Professor of Human Gross and
University of Cologne Neurosurgery; Developmental Anatomy
Cologne, Germany Professor of Orthopedics and Anatomy Department of Anatomical Sciences
Mayo Clinic St. George’s University, Grenada, West
Paul N Schofield MA, DPhil Rochester, MN, USA Indies;
University Reader in Biomedical Informatics Professor
Department of Physiology, Development and Jonathan D Spratt MA(Cantab), FRCS(Eng), Centre of Anatomy and Human Identification
Neuroscience FRCR University of Dundee, Dundee, UK
University of Cambridge Clinical Director of Diagnostic Radiology
Cambridge, UK City Hospitals Sunderland NHS Foundation Richard Tunstall BMedSci, PhD, PGCLTHE
Trust FHEA
Nadav Schwartz MD Sunderland, UK; Head of Clinical Anatomy and Imaging
Assistant Professor, Maternal Fetal Medicine Visiting Professor of Anatomy Warwick Medical School
Department of Obstetrics and Gynecology, Former anatomy examiner for the Royal University of Warwick, UK;
Perelman School of Medicine College of Surgeons of England and Royal University Hospitals Coventry and
University of Pennsylvania College of Radiologists Warwickshire NHS Trust
Philadelphia, PA, USA Editor for Imaging Anatomy Coventry, UK;
Visiting Professor of Anatomy
Vikram Sharma BSc(Hons), MBBS(Lon), Jacob Bertram Springborg MD, PhD St George’s University, Grenada, West Indies
MRCS(Eng), PG(Cert) Consultant Neurosurgeon; Editor for Surface Anatomy
Clinical Research Fellow Associate Professor of Neurosurgery
Nuffield Department of Surgical Sciences University Clinic of Neurosurgery
University of Oxford Copenhagen University Hospital
Oxford, UK Copenhagen, Denmark
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Contributors to the forty-first edition
Andry Vleeming PhD Gary Warburton DDS, MD, FDSRCS, FACS Caroline B Wigley BSc, PhD
Professor of Clinical Anatomy Associate Professor; University of Exeter Medical School
University of New England Program Director and Division Chief Exeter, UK
College of Osteopathic Medicine Oral and Maxillofacial Surgery Editor for Cell and Tissue Microstructure
Biddeford, ME, USA; University of Maryland Dental School
Department of Rehabilitation Sciences and Baltimore, MD, USA Frank H Willard PhD
Physiotherapy Professor of Anatomy
Faculty of Medicine and Health Sciences Jeremy PT Ward BSc, PhD University of New England College of
Ghent University Head of Department of Physiology; Osteopathic Medicine
Ghent, Belgium Professor of Respiratory Cell Physiology Biddeford, Maine, USA
Department of Physiology
Jan Voogd MD King’s College London Chin-Ho Wong MBBS, MRCS(Ed),
Emeritus Professor of Anatomy London, UK MMed(Surg), FAMS(Plast Surg)
Department of Neuroscience Plastic Surgeon, Private Practice
Erasmus Medical Center John C Watkinson MSc, MS, FRCS, DLO Singapore
Rotterdam, The Netherlands Consultant ENT, Head and Neck and Thyroid
Surgeon Stephanie J Woodley PhD, MSc, BPhty
Bart Wagner BSc, CSci, FIBMS, Dip Ult Queen Elizabeth Hospital Senior Lecturer
Path. University of Birmingham NHS Trust Department of Anatomy
Chief Biomedical Scientist Birmingham, UK University of Otago
Electron Microscopy Unit Dunedin, New Zealand
Histopathology Department Alan J Wein MD, PhD(Hon), FACS
Royal Hallamshire Hospital (Sheffield Founders Professor and Chief of Urology
Teaching Hospitals) Director, Urology Residency Program
Sheffield, UK Penn Medicine, Perelman School of
Medicine
University of Pennsylvania Health System
Philadelphia, PA, USA
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HISTORICAL INTRODUCTION
Gray’s Anatomy is now on its way to being 160 years old. The book is a required to operate on real patients, or on soldiers injured at Sebastopol
rarity in textbook publishing in having been in continuous publication or some other battlefield. The book they planned together was a practi-
on both sides of the Atlantic Ocean, since 1858. One and a half centu- cal one, designed to encourage youngsters to study anatomy, help them
ries is an exceptionally long era for a textbook. Of course, the volume pass exams, and assist them as budding surgeons. It was not simply an
now is very different from the one Mr Henry Gray first created with his anatomy textbook, but a guide to dissecting procedure, and to the major
colleague Dr Henry Vandyke Carter, in mid-Victorian London. In this operations.
introductory essay, I shall explain the long history of Gray’s, from those Gray and Carter belonged to a generation of anatomists ready to
Victorian days right up to today. infuse the study of human anatomy with a new, and respectable, scien-
The shortcomings of existing anatomical textbooks probably tificity. Disreputable aspects of the profession’s history, acquired during
impressed themselves on Henry Gray when he was still a student at St the days of body-snatching, were assiduously being forgotten. The
George’s Hospital Medical School, near London’s Hyde Park Corner, in Anatomy Act of 1832 had legalized the requisition of unclaimed bodies
the early 1840s. He began thinking about creating a new anatomy from workhouse and hospital mortuaries, and the study of anatomy
textbook a decade later, while war was being fought in the Crimea. New (now with its own Inspectorate) was rising in respectability in Britain.
legislation was being planned that would establish the General Medical The private anatomy schools that had flourished in the Regency period
Council (1858) to regulate professional education and standards. were closing their doors, and the major teaching hospitals were erecting
Gray was twenty-eight years old, and a teacher himself at St George’s. new, purpose-built dissection rooms (Richardson 2000).
He was very able, hard-working and highly ambitious, already a Fellow The best-known student works when Gray and Carter had qualified
of the Royal Society, and of the Royal College of Surgeons. Although were probably Erasmus Wilson’s Anatomist’s Vade Mecum, and Elements
little is known about his personal life, his was a glittering career so far, of Anatomy by Jones Quain. Both works were small – pocket-sized – but
achieved while he served and taught on the hospital wards and in the Quain came in two thick volumes. Both Quain’s and Wilson’s works
dissecting room (Fig. 1) (Anon 1908). were good books in their way, but their small pages of dense type, and
Gray shared the idea for the new book with a talented colleague on even smaller illustrations, were somewhat daunting, seeming to demand
the teaching staff at St George’s, Henry Vandyke Carter, in November much nose-to-the-grindstone effort from the reader.
1855. Carter was from a family of Scarborough artists, and was himself The planned new textbook’s dimensions and character were serious
a clever artist and microscopist. He had produced fine illustrations for matters. Pocket manuals were commercially successful because they
Gray’s scientific publications before, but could see that this idea was a appealed to students by offering much knowledge in a small compass.
much more complex project. Carter recorded in his diary: But pocket-sized books had button-sized illustrations. Knox’s Manual
of Human Anatomy, for example, was a good book, but was only 6 inches
Little to record. Gray made proposal to assist by drawings in bringing
by 4 (15 × 10 cm) and few of its illustrations occupied more than one-
out a Manual for students: a good idea but did not come to any plan …
third of a page. Gray and Carter must have discussed this matter between
too exacting, for would not be a simple artist (Carter 1855).
themselves, and with Gray’s publisher, JW Parker & Son, before deci-
Neither of these young men was interested in producing a pretty book, sions were taken about the size and girth of the new book, and espe-
or an expensive one. Their purpose was to supply an affordable, accurate cially the size of its illustrations. While Gray and Carter were working
teaching aid for people like their own students, who might soon be on the book, a new edition of Quain’s was published; this time it was
a ‘triple-decker’ – in three volumes – of 1740 pages in all.
The two men were earnestly engaged for the following 18 months
in work for the new book. Gray wrote the text, and Carter created the
illustrations; all the dissections were undertaken jointly. Their working
days were long – all the hours of daylight, eight or nine hours at a
stretch – right through 1856, and well into 1857. We can infer from the
warmth of Gray’s appreciation of Carter in his published acknowledge-
ments that their collaboration was a happy one.
The Author gratefully acknowledges the great services he has derived in
the execution of this work, from the assistance of his friend, Dr. H. V.
Carter, late Demonstrator of Anatomy at St George’s Hospital. All the
drawings from which the engravings were made, were executed by him.
(Gray 1858)
With all the dissections done, and Carter’s inscribed wood-blocks at the
engravers, Gray took six months’ leave from his teaching at St George’s
to work as a personal doctor for a wealthy family. It was probably as
good a way as any to get a well-earned break from the dissecting room
and the dead-house (Nicol 2002).
Carter sat the examination for medical officers in the East India
Company, and sailed for India in the spring of 1858, when the book
Fig. 1 Henry Gray (1827–1861) is shown here in the foreground, seated
was still in its proof stages. Gray had left a trusted colleague, Timothy
by the feet of the cadaver. The photograph was taken by a medical
Holmes, to see it through the press. Holmes’s association with the first
student, Joseph Langhorn. The room is the dissecting room of St
edition would later prove vital to its survival. Gray looked over the final
George’s Hospital Medical School in Kinnerton Street, London. Gray is
shown surrounded by staff and students. When the photo was taken, on galley proofs, just before the book finally went to press.
27 March 1860, Carter had left St George’s, to become Professor of
Anatomy and Physiology at Grant Medical College, in Bombay (nowadays THE FIRST EDITION
Mumbai). The second edition of Gray’s Anatomy was in its proof stages,
to appear in December 1860. Gray died just over a year later, in June The book Gray and Carter had created together, Anatomy, Descriptive
1861, at the height of his powers. and Surgical, appeared at the very end of August 1858, to immediate e5 | 20 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Historical introduction
acclaim. Reviews in The Lancet and the British Medical Journal were
highly complimentary, and students flocked to buy.
It is not difficult to understand why it was a runaway success. Gray’s
Anatomy knocked its competitors into a cocked hat. It was considerably
smaller and more slender than the doorstopper with which modern
readers are familiar. The book held well in the hand, it felt substantial,
and it contained everything required. To contemporaries, it was small
enough to be portable, but large enough for decent illustrations: ‘royal
octavo’ – 91 × 6 inches (24 × 15 cm) – about two-thirds of modern A4
2
size. Its medium-size, single-volume format was far removed from
Quain, yet double the size of Knox’s Manual.
Simply organized and well designed, the book explains itself confi-
dently and well; the clarity and authority of the prose are manifest. But
what made it unique for its day was the outstanding size and quality
of the illustrations. Gray thanked the wood engravers Butterworth and
Heath for the ‘great care and fidelity’ they had displayed in the engrav-
ings, but it was really to Carter that the book owed its extraordinary
success.
The beauty of Carter’s illustrations resides in their diagrammatic
clarity, quite atypical for their time. The images in contemporary
anatomy books were usually ‘proxy-labelled’: dotted with tiny numbers
or letters (often hard to find or read) or bristling with a sheaf of num-
bered arrows, referring to a key situated elsewhere, usually in a footnote,
which was sometimes so lengthy it wrapped round on to the following
page. Proxy labels require the reader’s eye to move to and fro: from the
structure to the proxy label to the legend and back again. There was
plenty of scope for slippage, annoyance and distraction. Carter’s illustra-
tions, by contrast, unify name and structure, enabling the eye to assimi-
late both at a glance. We are so familiar with Carter’s images that it is
hard to appreciate how incredibly modern they must have seemed in
1858. The volume made human anatomy look new, exciting, accessible
and do-able.
The first edition was covered in a brown bookbinder’s cloth embossed
all over in a dotted pattern, and with a double picture-frame border. Its
spine was lettered in gold blocking:
Fig. 2 Henry Vandyke Carter (1831–1897). Carter was appointed
GRAY’S
Honorary Surgeon to Queen Victoria in 1890.
ANATOMY
… with ‘DESCRIPTIVE AND SURGICAL’ in small capitals underneath. sense of calamity. The grand old medical man Sir Benjamin Brodie,
Gray’s Anatomy is how it has been referred to ever since. Carter was given Sergeant-Surgeon to the Queen, and the great supporter of Gray to
credit with Gray on the book’s title page for undertaking all the dissec- whom Anatomy had been dedicated, cried forlornly: ‘Who is there to
tions on which the book was based, and sole credit for all the illustra- take his place?’ (Anon 1908).
tions, though his name appeared in a significantly smaller type, and he But old JW Parker ensured the survival of Gray’s by inviting Timothy
was described as the ‘Late Demonstrator in Anatomy at St George’s Holmes, the doctor who had helped proof-read the first edition, and
Hospital’ rather than being given his full current title, which was Profes- who had filled Gray’s shoes at the medical school, to serve as Editor for
sor of Anatomy and Physiology at Grant Medical College, Bombay. Gray the next edition. Other long-running anatomy works, such as Quain,
was still only a Lecturer at St George’s and he may have been aware that remained in print in a similar way, co-edited by other hands (Quain
his words had been upstaged by the quality of Carter’s anatomical 1856).
images. He need not have worried: Gray is the famous name on the Holmes (1825–1907) was another gifted St George’s man, a scholar-
spine of the book. ship boy who had won an exhibition to Cambridge, where his brilliance
Gray was paid £150 for every thousand copies sold. Carter never was recognized. Holmes was a Fellow of the Royal College of Surgeons
received a royalty payment, just a one-off fee at publication, which may at 28. John Parker junior had commissioned him to edit A System of
have allowed him to purchase the long-wished-for microscope he took Surgery (1860–64), an important essay series by distinguished surgeons
with him to India (Fig. 2). on subjects of their own choosing. Many of Holmes’s authors remain
The first edition print-run of 2000 copies sold out swiftly. A parallel important figures, even today: John Simon, James Paget, Henry Gray,
edition was published in the United States in 1859, and Gray must have Ernest Hart, Jonathan Hutchinson, Brown-Séquard and Joseph Lister.
been deeply gratified to have to revise an enlarged new English edition Holmes had lost an eye in an operative accident, and he had a gruff
in 1859–60, though he was surely saddened and worried by the death manner that terrified students, yet he published a lament for young
of his publisher, John Parker junior, at the young age of 40, while the Parker that reveals him capable of deep feeling (Holmes 1860).
book was going through the press. The second edition came out in the John Parker senior’s heart, however, was no longer in publishing.
December of 1860 and it too sold like hot cakes, as indeed has every His son’s death had closed down the future for him. The business, with
subsequent edition. all its stocks and copyrights, was sold to Messrs Longman. Parker retired
The following summer, in June 1861, at the height of his powers and to the village of Farnham, where he later died.
full of promise, Henry Gray died unexpectedly at the age of only 34. With Holmes as editor, and Longman as publisher, the immediate
Gray had contracted smallpox while nursing his nephew. A new strain future of Gray’s Anatomy was assured. The third edition appeared in
of the disease was more virulent than the one with which Gray had 1864 with relatively few changes, Gray’s estate receiving the balance of
been vaccinated as a child; the disease became confluent, and Gray died his royalty after Holmes was paid £100 for his work.
in a matter of days.
Within months, the whole country would be pitched into mourning THE MISSING OBITUARY
for the death of Prince Albert. The creative era over which he had pre-
sided – especially the decade that had flowered since the Great Exhibi- Why no obituary appeared for Henry Gray in Gray’s Anatomy is curious.
tion of 1851 – would be history. Gray had referred to Holmes as his ‘friend’ in the preface to the first
edition, yet it would also be true to say that they were rivals. Both had
THE BOOK SURVIVES just applied for a vacant post at St George’s, as Assistant Surgeon. Had
Gray lived, it is thought that Holmes may not have been appointed,
Anatomy Descriptive and Surgical could have died too. With Carter in despite his seniority in age (Anon 1908).
India, the death of Gray, so swiftly after that of the younger Parker, Later commentators have suggested, as though from inside knowl-
e6 might have spelled catastrophe. Certainly, at St George’s there was a edge, that Holmes’s ‘proof-reading’ included improving Gray’s writing | 21 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Historical introduction
style. This could be a reflection of Holmes’s own self-regard, but there were not as yet perfected, and in any case could not provide the bold
may be some truth in it. There can be no doubt that, as Editor of seven simplicity of line required for a book like Gray’s, which depended so
subsequent editions of Gray’s Anatomy (third to ninth editions, 1864– heavily on clear illustration and clear lettering. Recognizing the inferior-
1880), Holmes added new material, and had to correct and compress ity of half-tone illustrations by comparison with Carter’s wood-engraved
passages, but it is also possible that, back in 1857, Gray’s original originals, Pick and Howden courageously decided to jettison the
manuscript had been left in a poor state for Holmes to sort out. In other second-rate half-tones altogether. Most of the next edition’s illustrations
works, Gray’s writing style was lucid, but he always seems to have paid were either Carter’s, or old supplementary illustrations inspired by his
a copyist to transcribe his work prior to submission. The original manu- work, or newly commissioned wood engravings or line drawings,
script of Gray’s Anatomy, sadly, has not survived, so it is impossible to intended ‘to harmonize with Carter’s original figures’. They successfully
be sure how much of the finished version had actually been written by emulated Carter’s verve. Having fewer pages and lighter paper, the 1905
Holmes. (sixteenth edition) weighed less than its predecessor, at 4 lb 11 oz/2.1 kg.
It may be that Gray’s glittering career, or perhaps the patronage that Typographically, the new edition was superb.
unquestionably advanced it, created jealousies among his colleagues, Howden took over as sole editor in 1909 (seventeenth edition) and
or that there was something in Gray’s manner that precluded affection, immediately stamped his personality on Gray’s. He excised ‘Surgical’
or that created resentments among clever social inferiors like Carter and from the title, changing it to Anatomy Descriptive and Applied, and
Holmes, especially if they felt their contributions to his brilliant career removed Carter’s name altogether. He also instigated the beginnings of
were not given adequate credit. Whatever the explanation, no reference an editorial board of experts for Gray’s, by adding to the title page ‘Notes
to Gray’s life or death appeared in Gray’s Anatomy itself until the twen- on Applied Anatomy’ by AJ Jex-Blake and W Fedde Fedden, both St
tieth century (Howden et al 1918). George’s men. For the first time, the number of illustrations exceeded
one thousand. Howden was responsible for the significant innovation
A SUCCESSION OF EDITORS of a short historical note on Henry Gray himself, nearly 60 years after
his death, which included a portrait photograph (1918, twentieth
Holmes expanded areas of the book that Gray himself had developed edition).
in the second edition (1860), notably in ‘general’ anatomy (histology)
and ‘development’ (embryology). In Holmes’s time as Editor, the THE NOMENCLATURE CONTROVERSY
volume grew from 788 pages in 1864 to 960 in 1880 (ninth edition),
with the histological section paginated separately in roman numerals Howden’s era, and that of his successor TB Johnston (of Guy’s), was
at the front of the book. Extra illustrations were added, mainly from overshadowed by a cloud of international controversy concerning ana-
other published sources. tomical terminology. European anatomists were endeavouring to stand-
The connections with Gray and Carter, and with St George’s, were ardize anatomical terms, often using Latinate constructions, a move
maintained with the appointment of the next editor, T. Pickering Pick, resisted in Britain and the United States. Gray’s became mired in these
who had been a student at St George’s in Gray’s time. From 1883 (tenth debates for over 20 years. The attempt to be fair to all sides by using
edition) onwards, Pick kept up with current research, rewrote and inte- multiple terms doubtless generated much confusion amongst students,
grated the histology and embryology into the volume, dropped Holmes until a working compromise was at last arrived at in 1955 (thirty-second
from the title page, removed Gray’s preface to the first edition, and edition, 1958).
added bold subheadings, which certainly improved the appearance and Johnston oversaw the second retitling of the book (in 1938, twenty-
accessibility of the text. Pick said he had ‘tried to keep before himself seventh edition): it was now, officially, Gray’s Anatomy, finally ending
the fact that the work is intended for students of anatomy rather than the fiction that it had ever been known as anything else. Gray’s suffered
for the Scientific Anatomist’ (thirteenth edition, 1893). from paper shortages and printing difficulties in World War II, but suc-
Pick also introduced colour printing (in 1887, eleventh edition) and cessive editions nevertheless continued to grow in size and weight,
experimented with the addition of illustrations using the new printing while illustrations were replaced and added as the text was revised.
method of half-tone dots: for colour (which worked) and for new black- Between Howden’s first sole effort (1909, seventeenth edition) and
and-white illustrations (which did not). Half-tone shades of grey com- Johnston’s last edition (1958, thirty-second edition), Gray’s expanded
pared poorly with Carter’s wood engravings, still sharp and clear by by over 300 pages – from 1296 to 1604 pages, and almost 300 addi-
comparison. tional illustrations brought the total to over 1300. Johnston also intro-
What Henry Vandyke Carter made of these changes is a rich topic duced X-ray plates (1938) and, in 1958 (thirty-second edition), electron
for speculation. He returned to England in 1888, having retired from micrographs by AS Fitton-Jackson, one of the first occasions on which
the Indian Medical Service, full of honours – Deputy Surgeon General, a woman was credited with a contribution to Gray’s. Johnston felt com-
and in 1890, he was made Honorary Surgeon to Queen Victoria. Carter pelled to mention that she was ‘a blood relative of Henry Gray himself’,
had continued researching throughout his clinical medical career in perhaps by way of mitigation.
India, and became one of India’s foremost bacteriologists/tropical
disease specialists before there was really a name for either discipline. AFTER WORLD WAR II
Carter made some important discoveries, including the fungal cause of
mycetoma, which he described and named. He was also a key figure in The editions of Gray’s issued in the decades immediately following the
confirming scientifically in India some major international discoveries, Second World War give the impression of intellectual stagnation. Steady
such as Hansen’s discovery of the cause of leprosy, Koch’s discovery of expansion continued in an almost formulaic fashion, with the insertion
the organism causing tuberculosis, and Laveran’s discovery of the organ- of additional detail. The central historical importance of innovation in
ism that causes malaria. Carter married late in life, and his wife was left the success of Gray’s seems to have been lost sight of by its publishers
with two young children when he died in Scarborough in 1897, aged and editors – Johnston (1930–1958, twenty-fourth to thirty-second
65. Like Gray, he received no obituary in the book. editions), J Whillis (co-editor with Johnston, 1938–1954), DV Davies
When Pick was joined on the title page by Robert Howden (a profes- (1958–1967, thirty-second to thirty-fourth editions) and F Davies
sional anatomist from the University of Durham) in 1901 (fifteenth (co-editor with DV Davies 1958–1962, thirty-second to thirty-third
edition), the volume was still easily recognizable as the book Gray and editions). Gray’s had become so pre-eminent that perhaps complacency
Carter had created. Although many of Carter’s illustrations had been crept in, or editors were too daunted or too busy to confront the
revised or replaced, many others still remained. Sadly, though, an entire ‘massive undertaking’ of a root and branch revision (Tansey 1995). The
section (embryology) was again separately paginated, as its revision had unexpected deaths of three major figures associated with Gray’s in this
taken longer than anticipated. Gray’s had grown, seemingly inexorably, era, James Whillis, Francis Davies and David Vaughan Davies – each of
and was now quite thick and heavy: 1244 pages, weighing 5 lb whom had been ready to take the editorial reins – may have contributed
8 oz/2.5 kg. Both co-editors, and perhaps also its publisher, were dis- to retarding the process. The work became somewhat dull.
satisfied with it.
KEY EDITION: 1973
KEY EDITION: 1905
DV Davies had recognized the need for modernization, but his unex-
Serious decisions were taken well in advance of the next edition, which pected death left the work to other hands. Two Professors of Anatomy
turned out to be Pick’s last with Howden. Published 50 years after Gray at Guy’s, Roger Warwick and Peter Williams, the latter of whom had
had first suggested the idea to Carter, the 1905 (sixteenth) edition was been involved as an indexer for Gray’s for several years, regarded it as
a landmark one. an honour to fulfill Davies’s intentions.
The period 1880–1930 was a difficult time for anatomical illustra- Their thirty-fifth edition of 1973 was a significant departure from
tion, because the new techniques of photo-lithography and half-tone tradition. Over 780 pages (of 1471) were newly written, almost a third e7 | 22 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Historical introduction
of the illustrations were newly commissioned, and the illustration cap- had developed a distinct character of its own in the interval), and sold
tions were freshly written throughout. With a complete re-typesetting extremely well there (Williams and Warwick 1973).
of the text in larger double-column pages, a new index and the innova- The influence of the Warwick and Williams edition was forceful and
tion of a bibliography, this edition of Gray’s looked and felt quite unlike long-lasting, and set a new pattern for the following quarter-century.
its 1967 (thirty-fourth edition) predecessor, and much more like its As has transpired several times before, wittingly or unwittingly, a new
modern incarnation. editor was being prepared for the future: Dr Susan Standring (of
This 1973 edition departed from earlier volumes in other significant Guy’s), who created the new bibliography for the 1973 edition of
ways. The editors made explicit their intention to try to counter the Gray’s, went on to serve on the editorial board, and has served as
impetus towards specialization and compartmentalization in twentieth- Editor-in-Chief for the last two editions before this one (2005–2008,
century medicine, by embracing and attempting to reintegrate the com- thirty-ninth and fortieth editions). Both editions are important for dif-
plexity of the available knowledge. Warwick and Williams openly ferent reasons.
renounced the pose of omniscience adopted by many textbooks, believ- For the thirty-ninth edition, the entire content of Gray’s was reorgan-
ing it important to accept and mention areas of ignorance or uncer- ized, from systematic to regional anatomy. This great sea-change was
tainty. They shared with the reader the difficulty of keeping abreast in not just organizational but historic, because, since its outset, Gray’s had
the sea of research, and accepted with a refreshing humility the impos- prioritized bodily systems, with subsidiary emphasis on how the
sibility of fulfilling their own ambitious programme. systems interweave in the regions of the body. Professor Standring
Warwick and Williams’s 1973 edition had much in common with explained that this regional change of emphasis had long been asked
Gray and Carter’s first edition. It was bold and innovative – respectful for by readers and users of Gray’s, and that new imaging techniques in
of its heritage, while also striking out into new territory. It was visually our era have raised the clinical importance of local anatomy (Standring
attractive and visually informative. It embodied a sense of a treasury of 2005). The change was facilitated by an enormous collective effort on
information laid out for the reader (Williams and Warwick 1973). It the part of the editorial team and the illustrators. The subsequent and
was published simultaneously in the United States (the American Gray’s current editions consolidate that momentous change. (See Table 1.)
Table 1 Gray’s Anatomy Editions
Edition Date Author/Editor(s) Publisher Title
1st 1858 Henry Gray JW Parker & Son Anatomy Descriptive and Surgical
The drawings by Henry Vandyke Carter. The dissections jointly by
the author and Dr Carter
2nd 1860 Henry Gray JW Parker & Son
3rd 1864 T Holmes Longman
4th 1866 T Holmes Longman
5th 1869 T Holmes Longman
6th 1872 T Holmes Longman
7th 1875 T Holmes Longman
8th 1877 T Holmes Longman
9th 1880 T Holmes Longman
10th 1883 TP Pick Longman
11th 1887 TP Pick Longman
12th 1890 TP Pick Longman
13th 1893 TP Pick Longman
Gray’s preface removed
14th 1897 TP Pick Longman
15th 1901 TP Pick & R Howden Longman
16th 1905 TP Pick & R Howden Longman
17th 1909 Robert Howden Longman Anatomy Descriptive and Applied
Notes on applied anatomy by AJ Jex-Blake & W Fedde Fedden
18th 1913 Robert Howden & Blake & Fedden Longman
19th 1916 Robert Howden & Blake & Fedden Longman
20th 1918 Robert Howden & Blake & Fedden Longman
First edition ever to feature a photograph and obituary of Henry Gray
21st 1920 Robert Howden Longman
Notes on applied anatomy by AJ Jex-Blake & John Clay
22nd 1923 Robert Howden Longman
Notes on applied anatomy by John Clay & John D Lickley
23rd 1926 Robert Howden Longman
24th 1930 TB Johnston Longman
25th 1932 TB Johnston Longman
26th 1935 TB Johnston Longman
27th 1938 TB Johnston & J Whillis Longman Gray’s Anatomy
28th 1942 TB Johnston & J Whillis Longman
29th 1946 TB Johnston & J Whillis Longman
30th 1949 TB Johnston & J Whillis Longman
31st 1954 TB Johnston & J Whillis Longman
32nd 1958 TB Johnston & DV Davies & F Davies Longman
33rd 1962 DV Davies & F Davies Longman
34th 1967 DV Davies & RE Coupland Longman
35th 1973 Peter L Williams & Roger Warwick Longman
With a separate volume: Functional Neuroanatomy of Man – being the
neurology section of Gray’s Anatomy. 35th edition, 1975
36th 1980 Roger Warwick & Peter L Williams Churchill Livingstone
37th 1989 Peter L Williams Churchill Livingstone
38th 1995 Peter L Williams & Editorial Board Churchill Livingstone
39th 2005 Susan Standring & Editorial Board Elsevier The Anatomical Basis of Clinical Practice
40th 2008 Susan Standring & Editorial Board Elsevier The Anatomical Basis of Clinical Practice
41st 2015 Susan Standring & Editorial Board Elsevier The Anatomical Basis of Clinical Practice
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Historical introduction
THE DOCTORS’ BIBLE Howden R, Jex-Blake AJ, Fedde Fedden W (eds) 1918 Gray’s Anatomy, 20th
ed. London: Longman.
Neither Gray nor Carter, the young men who – by their committed hard
Lewis H Sinclair 1925 Arrowsmith. New York: Harcourt Brace; p. 4.
work between 1856 and 1858 – created the original Gray’s Anatomy,
Nicol KE 2002 Henry Gray of St George’s Hospital: a Chronology. London:
would have conceived that so many years after their deaths their book
published by the author.
would not only be a household name, but also be regarded as a work
of such pre-eminent importance that a novelist half a world away would Quain J 1856 Elements of Anatomy. Ed. by Sharpey W, Ellis GV. London:
rank it as cardinal – alongside the Bible and Shakespeare – to a doctor’s Walton & Maberly.
education (Sinclair Lewis 1925, Richardson 2008). From this forty-first Richardson R 2000 Death, Dissection and the Destitute. Chicago: Chicago
edition of Gray’s Anatomy, we can look back to appraise the long-term University Press; pp. 193–249, 287, 357.
value of their efforts. We can discern how the book they created tri-
Richardson R 2008 The Making of Mr Gray’s Anatomy. Oxford: Oxford
umphed over its competitors, and has survived pre-eminent. Gray’s is a University Press.
remarkable publishing phenomenon. Although the volume now looks
Standring S (ed.) 2005 Preface. In: Gray’s Anatomy, 39th ed. Elsevier:
quite different to the original, and contains so much more, its kinship
London.
with the Gray’s Anatomy of 1858 is easily demonstrable by direct descent,
every edition updated by Henry Gray’s successor. Works are rare indeed Tansey EM 1995 A brief history of Gray’s Anatomy. In: Gray’s Anatomy, 38th
that have had such a long history of continuous publication on both ed. London: Churchill Livingstone.
sides of the Atlantic, and such a useful one. Williams PL, Warwick R (eds.) 1973 Preface. In: Gray’s Anatomy, 35th ed.
London: Churchill Livingstone.
Ruth Richardson, MA, DPhil, FRHistS
Senior Visiting Research Fellow, Centre for Life-Writing Research, ACKNOWLEDGEMENTS
King’s College London;
Affiliated Scholar in the History and Philosophy of Science, For their assistance while I was undertaking the research for this essay,
University of Cambridge, UK I should like to thank the Librarians and Archivists and Staff at the
British Library, Society of Apothecaries, London School of Hygiene and
Tropical Medicine, Royal College of Surgeons, Royal Society of Medi-
REFERENCES
cine, St Bride Printing Library, St George’s Hospital Tooting, Scarbor-
Anon 1908 Henry Gray. St George’s Hospital Gazette 16:49–54. ough City Museum and Art Gallery, University of Reading, Wellcome
Institute Library, Westminster City Archives and Windsor Castle; and
Carter HV 1855 Diary. Wellcome Western Manuscript 5818; 25 Nov.
the following individuals: Anne Bayliss, Gordon Bell, David Buchanan,
Gray H 1858 Preface. In: Anatomy: Descriptive and Surgical. London: JW Dee Cook, Arthur Credland, Chris Hamlin, Victoria Killick, Louise King,
Parker & Son. Keith Nicol, Sarah Potts, Mark Smalley, and Nallini Thevakarrunai.
Holmes T (ed.) 1860 I: Preface. In: A System of Surgery. London: JW Parker Above all, my thanks to Brian Hurwitz, who has read and advised on
& Son. the evolving text.
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ANATOMICAL NOMENCLATURE
Anatomy is the study of the structure of the body. Conventionally, it is with the median plane; although often employed, ‘parasagittal’ is there-
divided into topographical (macroscopic or gross) anatomy (which fore redundant and should not be used. The coronal (frontal) plane is
may be further divided into regional anatomy, surface anatomy, neuro- orthogonal to the median plane and divides the body into anterior
anatomy, endoscopic and imaging anatomy); developmental anatomy (front) and posterior (back). The horizontal (transverse) plane is
(embryogenesis and subsequent organogenesis); and the anatomy of orthogonal to both median and sagittal planes. Radiologists refer to
microscopic and submicroscopic structure (histology). transverse planes as (trans)axial; convention dictates that axial anatomy
Anatomical language is one of the fundamental languages of medi- is viewed as though looking from the feet towards the head.
cine. The unambiguous description of thousands of structures is impos- Structures nearer the head are superior, cranial or (sometimes)
sible without an extensive and often highly specialized vocabulary. cephalic (cephalad), whereas structures closer to the feet are inferior;
Ideally, these terms, which are often derived from Latin or Greek, caudal is most often used in embryology to refer to the hind end of the
should be used to the exclusion of any other, and eponyms should be embryo. Medial and lateral indicate closeness to the median plane,
avoided. In reality, this does not always happen. Many terms are ver- medial being closer than lateral; in the anatomical position, the little
nacularized and, around the world, synonyms and eponyms still finger is medial to the thumb, and the great toe is medial to the little
abound in the literature, in medical undergraduate classrooms and in toe. Specialized terms may also be used to indicate medial and lateral.
clinics. The Terminologia Anatomica,1 drawn up by the Federative Com- Thus, in the upper limb, ulnar and radial are used to mean medial and
mittee on Anatomical Terminology (FCAT) in 1998, continues to serve lateral, respectively; in the lower limb, tibial and fibular (peroneal) are
as our reference source for the terminology for macroscopic anatomy, used to mean medial and lateral, respectively. Terms may be based on
and the text of the forty-first edition of Gray’s Anatomy is almost entirely embryological relationships; the border of the upper limb that includes
TA-compliant. However, where terminology is at variance with, or, more the thumb, and the border of the lower limb that includes the great toe
likely, is not included in, the TA, the alternative term used either is cited are the pre-axial borders, whilst the opposite borders are the post-axial
in the relevant consensus document or position paper, or enjoys wide- borders. Various degrees of obliquity are acknowledged using com-
spread clinical usage. Synonyms and eponyms are given in parentheses pound terms, e.g. posterolateral.
on first usage of a preferred term and not shown thereafter in the text; When referring to structures in the trunk and upper limb, we have
an updated list of eponyms and short biographical details of the clini- freely used the synonyms anterior, ventral, flexor, palmar and volar, and
cians and anatomists whose names are used in this way is available in posterior, dorsal and extensor. We recognize that these synonyms are
the e-book for reference purposes (see Preface, p. ix, for further discus- not always satisfactory, e.g. the extensor aspect of the leg is anterior with
sion of the use of eponyms). respect to the knee and ankle joints, and superior in the foot and digits;
the plantar (flexor) aspect of the foot is inferior. Dorsal (dorsum) and
PLANES, DIRECTIONS AND ventral are terms used particularly by embryologists and neuroanato-
RELATIONSHIPS mists; they therefore feature most often in Sections 2 and 3.
Distal and proximal are used particularly to describe structures in
To avoid ambiguity, all anatomical descriptions assume that the body the limbs, taking the datum point as the attachment of the limb to the
is in the conventional ‘anatomical position’, i.e. standing erect and trunk (sometimes referred to as the root), such that a proximal structure
facing forwards, upper limbs by the side with the palms facing forwards, is closer to the attachment of the limb than a distal structure. However,
and lower limbs together with the toes facing forwards (Fig. 1). Descrip- proximal and distal are also used in describing branching structures,
tions are based on four imaginary planes – median, sagittal, coronal e.g. bronchi, vessels and nerves. External (outer) and internal (inner)
and horizontal – applied to a body in the anatomical position. The refer to the distance from the centre of an organ or cavity, e.g. the layers
median plane passes longitudinally through the body and divides it of the body wall, or the cortex and medulla of the kidney. Superficial
into right and left halves. The sagittal plane is any vertical plane parallel and deep are used to describe the relationships between adjacent struc-
tures. Ipsilateral refers to the same side (of the body, organ or structure),
bilateral to both sides, and contralateral to the opposite side.
Teeth are described using specific terms that indicate their relation-
1Terminologia Anatomica (1998) is the joint creation of the Federative Committee on
Anatomical Terminology (FCAT) and the Member Associations of the Interna- ship to their neighbours and to their position within the dental arch;
tional Federation of Associations of Anatomists (IFAA). these terms are described on page 517.
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AnAtomicAl nomenclAture
SUPERIOR ASPECT
Coronal plane
Anterior or ventral
Posterior or dorsal
Median or sagittal plane
Inferior or caudal
Superior or cranial
Transverse or horizontal plane Lateral
Medial
POSTERIOR ASPECT
RIGHT LATERAL ASPECT
Lateral (external) rotation
Medial (internal) rotation
Proximally
Distally
Proximally
LEFT LATERAL ASPECT
ANTERIOR ASPECT Supination
Pronation
Distally
Lateral (external) rotation
Medial (internal) rotation
Eversion
Inversion
INFERIOR ASPECT
Fig. 1 The terminology widely used in descriptive anatomy. Abbreviations shown on arrows: AD, adduction; AB, abduction; FLEX, flexion (of the thigh at
the hip joint); EXT, extension (of the leg at the knee joint).
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Medical.
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Young B, O’Dowd G, Woodford P 2013 Wheater’s Functional Histology:
Edinburgh: Elsevier, Churchill Livingstone.
A Text and Colour Atlas, 6th ed. Edinburgh: Elsevier, Churchill
Livingstone.
CLINICAL EXAMINATION
IMAGING AND RADIOLOGY/RADIOLOGICAL
O’Brien M 2010 Aids to the Examination of the Peripheral Nervous
ANATOMY System, 5th ed. London: Elsevier, WB Saunders.
Lumley JSP 2008 Surface Anatomy: The Anatomical Basis of Clinical
Butler P, Mitchell AWM, Healy JC 2011 Applied Radiological Anatomy,
Examination, 4th ed. Edinburgh: Elsevier, Churchill Livingstone.
2nd ed. New York: Cambridge University Press.
Ellis H, Logan BM, Dixon AK 2007 Human Sectional Anatomy: Pocket
xviii Atlas of Body Sections, CT and MRI Images, 3rd ed. CRC Press. | 27 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
4
1
NOITCES
CHAPTER
1
Basic structure and function of cells
Epithelial cells rarely operate independently of each other and com-
CELL STRUCTURE
monly form aggregates by adhesion, often assisted by specialized inter-
cellular junctions. They may also communicate with each other either
GENERAL CHARACTERISTICS OF CELLS by generating and detecting molecular signals that diffuse across inter-
cellular spaces, or more rapidly by generating interactions between
The shapes of mammalian cells vary widely depending on their interac- membrane-bound signalling molecules. Cohesive groups of cells con-
tions with each other, their extracellular environment and internal stitute tissues, and more complex assemblies of tissues form functional
structures. Their surfaces are often highly folded when absorptive or systems or organs.
transport functions take place across their boundaries. Cell size is Most cells are between 5 and 50 µm in diameter: e.g. resting lym-
limited by rates of diffusion, either that of material entering or leaving phocytes are 6 µm across, red blood cells 7.5 µm and columnar epithe-
cells, or that of diffusion within them. Movement of macromolecules lial cells 20 µm tall and 10 µm wide (all measurements are approximate).
can be much accelerated and also directed by processes of active trans- Some cells are much larger than this: e.g. megakaryocytes of the bone
port across the plasma membrane and by transport mechanisms within marrow and osteoclasts of the remodelling bone are more than 200 µm
the cell. According to the location of absorptive or transport functions, in diameter. Neurones and skeletal muscle cells have relatively extended
apical microvilli (Fig. 1.1) or basolateral infoldings create a large shapes, some of the former being over 1 m in length.
surface area for transport or diffusion.
Motility is a characteristic of most cells, in the form of movements
of cytoplasm or specific organelles from one part of the cell to another. CELLULAR ORGANIZATION
It also includes: the extension of parts of the cell surface such as pseu-
dopodia, lamellipodia, filopodia and microvilli; locomotion of entire Each cell is contained within its limiting plasma membrane, which
cells, as in the amoeboid migration of tissue macrophages; the beating encloses the cytoplasm. All cells, except mature red blood cells, also
of flagella or cilia to move the cell (e.g. in spermatozoa) or fluids overly- contain a nucleus that is surrounded by a nuclear membrane or enve-
ing it (e.g. in respiratory epithelium); cell division; and muscle contrac- lope (see Fig. 1.1; Fig. 1.2). The nucleus includes: the genome of the
tion. Cell movements are also involved in the uptake of materials from cell contained within the chromosomes; the nucleolus; and other sub-
their environment (endocytosis, phagocytosis) and the passage of large nuclear structures. The cytoplasm contains cytomembranes and several
molecular complexes out of cells (exocytosis, secretion). membrane-bound structures, called organelles, which form separate
Surface projections
(cilia, microvilli)
Surface invagination
Actin filaments
Vesicle Mitochondrion
Cell junctions
Plasma membrane
Desmosome Peroxisomes
Cytosol
Nuclear pore
Intermediate
filaments Nuclear envelope
Smooth endoplasmic Nucleus
reticulum
Nucleolus
Ribosome
Rough endoplasmic
reticulum
Microtubules
Golgi apparatus Centriole pair
Lysosomes
Cell surface folds
Fig . 1 .1 The main structural components and internal organization of a generalized cell . | 31 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
5
1
RETPaHC
CC MMVV AAPPMM
AAJJCC
Receptor
Transmembrane protein
pore complex
of proteins
Carbohydrate
residues
External
(extracellular)
surface
MM
MM
CCyy
LLPPMM
Internal
(intracellular)
surface
NN Lipid bilayer
appearance
in electron
microscope
Intrinsic
membrane
protein Extrinsic Transmembrane
protein
protein Transport Non-polar tail
or diffusion of phospholipid
channel Cytoskeletal
Polar end of
element
EENN phospholipid
Fig . 1 .3 The molecular organization of the plasma membrane, according
to the fluid mosaic model of membrane structure . Intrinsic or integral
membrane proteins include diffusion or transport channel complexes,
receptor proteins and adhesion molecules . These may span the thickness
of the membrane (transmembrane proteins) and can have both
extracellular and cytoplasmic domains . Transmembrane proteins have
hydrophobic zones, which cross the phospholipid bilayer and allow the
Fig . 1 .2 The structural organization and some principal organelles of a
protein to ‘float’ in the plane of the membrane . Some proteins are
typical cell . This example is a ciliated columnar epithelial cell from human
restricted in their freedom of movement where their cytoplasmic domains
nasal mucosa . The central cell, which occupies most of the field of
are tethered to the cytoskeleton .
view, is closely apposed to its neighbours along their lateral plasma
membranes . Within the apical junctional complex, these membranes form
a tightly sealed zone (tight junction) that isolates underlying tissues from,
charides and polysaccharides are bound either to proteins (glycopro-
in this instance, the nasal cavity . Abbreviations: AJC, apical junctional
teins) or to lipids (glycolipids), and project mainly into the extracellular
complex; APM, apical plasma membrane; C, cilia; Cy, cytoplasm; EN,
domain (Fig. 1.3).
euchromatic nucleus; LPM, lateral plasma membrane; M, mitochondria;
In the electron microscope, membranes fixed and contrasted by
MV, microvilli; N, nucleolus . (Courtesy of Dr Bart Wagner, Histopathology
heavy metals such as osmium tetroxide appear in section as two densely
Department, Sheffield Teaching Hospitals, UK .)
stained layers separated by an electron-translucent zone – the classic
unit membrane. The total thickness of each layer is about 7.5 nm. The
and distinct compartments within the cytoplasm. Cytomembranes
overall thickness of the plasma membrane is typically 15 nm. Freeze-
include the rough and smooth endoplasmic reticulum and Golgi appa-
fracture cleavage planes usually pass along the hydrophobic portion of
ratus, as well as vesicles derived from them. Organelles include lyso-
the bilayer, where the hydrophobic tails of phospholipids meet, and
somes, peroxisomes and mitochondria. The nucleus and mitochondria
split the bilayer into two leaflets. Each cleaved leaflet has a surface and
are enclosed by a double-membrane system; lysosomes and peroxi-
a face. The surface of each leaflet faces either the extracellular surface
somes have a single bounding membrane. There are also non-
(ES) or the intracellular or protoplasmic (cytoplasmic) surface (PS). The
membranous structures, called inclusions, which lie free in the cytosolic
extracellular face (EF) and protoplasmic face (PF) of each leaflet are
compartment. They include lipid droplets, glycogen aggregates and pig-
artificially produced during membrane splitting. This technique has
ments (e.g. lipofuscin). In addition, ribosomes and several filamentous
also demonstrated intramembranous particles embedded in the lipid
protein networks, known collectively as the cytoskeleton, are found in
bilayer; in most cases, these represent large transmembrane protein
the cytosol. The cytoskeleton determines general cell shape and sup-
molecules or complexes of proteins. Intramembranous particles are
ports specialized extensions of the cell surface (microvilli, cilia, flag-
distributed asymmetrically between the two half-layers, usually adher-
ella). It is involved in the assembly of specific structures (e.g. centrioles)
ing more to one half of the bilayer than to the other. In plasma mem-
and controls cargo transport in the cytoplasm. The cytosol contains
branes, the intracellular leaflet carries most particles, seen on its face
many soluble proteins, ions and metabolites.
(the PF). Where they have been identified, clusters of particles usually
represent channels for the transmembrane passage of ions or molecules
Plasma membrane
between adjacent cells (gap junctions).
Biophysical measurements show the lipid bilayer to be highly fluid,
Cells are enclosed by a distinct plasma membrane, which shares fea- allowing diffusion in the plane of the membrane. Thus proteins are able
tures with the cytomembrane system that compartmentalizes the cyto- to move freely in such planes unless anchored from within the cell.
plasm and surrounds the nucleus. All membranes are composed of Membranes in general, and the plasma membrane in particular, form
lipids (mainly phospholipids, cholesterol and glycolipids) and pro- boundaries selectively limiting diffusion and creating physiologically
teins, in approximately equal ratios. Plasma membrane lipids form a distinct compartments. Lipid bilayers are impermeable to hydrophilic
lipid bilayer, a layer two molecules thick. The hydrophobic ends of each solutes and ions, and so membranes actively control the passage of ions
lipid molecule face the interior of the membrane and the hydrophilic and small organic molecules such as nutrients, through the activity of
ends face outwards. Most proteins are embedded within, or float in, the membrane transport proteins. However, lipid-soluble substances can
lipid bilayer as a fluid mosaic. Some proteins, because of extensive pass directly through the membrane so that, for example, steroid hor-
hydrophobic regions of their polypeptide chains, span the entire width mones enter the cytoplasm freely. Their receptor proteins are either
of the membrane (transmembrane proteins), whereas others are only cytosolic or nuclear, rather than being located on the cell surface.
superficially attached to the bilayer by lipid groups. Both are integral Plasma membranes are able to generate electrochemical gradients
(intrinsic) membrane proteins, as distinct from peripheral (extrinsic) and potential differences by selective ion transport, and actively take up
membrane proteins, which are membrane-bound only through their or export small molecules by energy-dependent processes. They also
association with other proteins. Carbohydrates in the form of oligosac- provide surfaces for the attachment of enzymes, sites for the receptors | 32 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
5.e1
1
RETPaHC
Combinations of biochemical, biophysical and biological tech-
niques have revealed that lipids are not homogenously distributed in
membranes, but that some are organized into microdomains in the
bilayer, called ‘detergent-resistant membranes’ or lipid ‘rafts’, rich in
sphingomyelin and cholesterol. The ability of select subsets of proteins
to partition into different lipid microdomains has profound effects on
their function, e.g. in T-cell receptor and cell–cell signalling. The highly
organized environment of the domains provides a signalling, trafficking
and membrane fusion environment. | 33 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
6
1
NOITCES
of external signals, including hormones and other ligands, and sites for abundant proteins; SER is abundant in steroid-producing cells and
the recognition and attachment of other cells. Internally, plasma mem- muscle cells. A variant of the endoplasmic reticulum in muscle cells is
branes can act as points of attachment for intracellular structures, in the sarcoplasmic reticulum, involved in calcium storage and release for
particular those concerned with cell motility and other cytoskeletal muscle contraction. For further reading on the endoplasmic reticulum,
functions. Cell membranes are synthesized by the rough endoplasmic see Bravo et al (2013).
reticulum in conjunction with the Golgi apparatus.
Smooth endoplasmic reticulum
Cell coat (glycocalyx)
The smooth endoplasmic reticulum (see Fig. 1.4) is associated with
The external surface of a plasma membrane differs structurally from carbohydrate metabolism and many other metabolic processes, includ-
internal membranes in that it possesses an external, fuzzy, carbohydrate- ing detoxification and synthesis of lipids, cholesterol and steroids. The
rich coat, the glycocalyx. The cell coat forms an integral part of the membranes of the smooth endoplasmic reticulum serve as surfaces for
plasma membrane, projecting as a diffusely filamentous layer 2–20 nm the attachment of many enzyme systems, e.g. the enzyme cytochrome
or more from the lipoprotein surface. The cell coat is composed of the P450, which is involved in important detoxification mechanisms and
carbohydrate portions of glycoproteins and glycolipids embedded in is thus accessible to its substrates, which are generally lipophilic. The
the plasma membrane (see Fig. 1.3). membranes also cooperate with the rough endoplasmic reticulum
The precise composition of the glycocalyx varies with cell type; many and the Golgi apparatus to synthesize new membranes; the protein,
tissue- and cell type-specific antigens are located in the coat, including carbohydrate and lipid components are added in different structural
the major histocompatibility complex of the immune system and, in compartments. The smooth endoplasmic reticulum in hepatocytes con-
the case of erythrocytes, blood group antigens. Therefore, the glycocalyx tains the enzyme glucose-6-phosphatase, which converts glucose-6-
plays a significant role in organ transplant compatibility. The glycocalyx phosphate to glucose, a step in gluconeogenesis.
found on apical microvilli of enterocytes, the cells forming the lining
epithelium of the intestine, consists of enzymes involved in the diges- Rough endoplasmic reticulum
tive process. Intestinal microvilli are cylindrical projections (1–2 µm The rough endoplasmic reticulum is a site of protein synthesis; its
long and about 0.1 µm in diameter) forming a closely packed layer cytosolic surface is studded with ribosomes (Fig. 1.5E). Ribosomes only
called the brush border that increases the absorptive function of bind to the endoplasmic reticulum when proteins targeted for secretion
enterocytes. begin to be synthesized. Most proteins pass through its membranes and
accumulate within its cisternae, although some integral membrane pro-
Cytoplasm teins, e.g. plasma membrane receptors, are inserted into the rough
endoplasmic reticulum membrane, where they remain. After passage
Compartments and functional organization from the rough endoplasmic reticulum, proteins remain in membrane-
bound cytoplasmic organelles such as lysosomes, become incorporated
The cytoplasm consists of the cytosol, a gel-like material enclosed by
into new plasma membrane, or are secreted by the cell. Some carbohy-
the cell or plasma membrane. The cytosol is made up of colloidal pro-
drates are also synthesized by enzymes within the cavities of the rough
teins such as enzymes, carbohydrates and small protein molecules,
endoplasmic reticulum and may be attached to newly formed protein
together with ribosomes and ribonucleic acids. The cytoplasm contains
(glycosylation). Vesicles are budded off from the rough endoplasmic
two cytomembrane systems, the endoplasmic reticulum and Golgi
reticulum for transport to the Golgi as part of the protein-targeting
apparatus, as well as membrane-bound organelles (lysosomes, peroxi-
mechanism of the cell.
somes and mitochondria), membrane-free inclusions (lipid droplets,
glycogen and pigments) and the cytoskeleton. The nuclear contents, Ribosomes, polyribosomes
the nucleoplasm, are separated from the cytoplasm by the nuclear
and protein synthesis
envelope.
Ribosomes are macromolecular machines that catalyse the synthesis of
Endoplasmic reticulum proteins from amino acids; synthesis and assembly into subunits takes
The endoplasmic reticulum is a system of interconnecting membrane- place in the nucleolus and includes the association of ribosomal RNA
lined channels within the cytoplasm (Fig. 1.4). These channels take (rRNA) with ribosomal proteins translocated from their site of synthesis
various forms, including cisternae (flattened sacs), tubules and vesicles. in the cytoplasm. The individual subunits are then transported into the
The membranes divide the cytoplasm into two major compartments. cytoplasm, where they remain separate from each other when not
The intramembranous compartment, or cisternal space, is where secre- actively synthesizing proteins. Ribosomes are granules approximately
tory products are stored or transported to the Golgi complex and cell 25 nm in diameter, composed of rRNA molecules and proteins assem-
exterior. The cisternal space is continuous with the perinuclear space. bled into two unequal subunits. The subunits can be separated by their
Structurally, the channel system can be divided into rough or granu- sedimentation coefficients (S) in an ultracentrifuge into larger 60S and
lar endoplasmic reticulum (RER), which has ribosomes attached to its smaller 40S components. These are associated with 73 different pro-
outer, cytosolic surface, and smooth or agranular endoplasmic reticu- teins (40 in the large subunit and 33 in the small), which have structural
lum (SER), which lacks ribosomes. The functions of the endoplasmic and enzymatic functions. Three small, highly convoluted rRNA strands
reticulum vary greatly and include: the synthesis, folding and transport (28S, 5.8S and 5S) make up the large subunit, and one strand (18S) is
of proteins; synthesis and transport of phospholipids and steroids; and in the small subunit.
storage of calcium within the cisternal space and regulated release into A typical cell contains millions of ribosomes. They may form groups
the cytoplasm. In general, RER is well developed in cells that produce (polyribosomes or polysomes) attached to messenger RNA (mRNA),
which they translate during protein synthesis for use outside the system
of membrane compartments, e.g. enzymes of the cytosol and cytoskel-
etal proteins. Some of the cytosolic products include proteins that can
be inserted directly into (or through) membranes of selected organelles,
such as mitochondria and peroxisomes. Ribosomes may be attached to
the membranes of the rough endoplasmic reticulum (see Fig. 1.5E).
In a mature polyribosome, all the attachment sites of the mRNA are
occupied as ribosomes move along it, synthesizing protein according
to its nucleotide sequence. Consequently, the number and spacing of
ribosomes in a polyribosome indicate the length of the mRNA mole-
cule and hence the size of the protein being made. The two subunits
have separate roles in protein synthesis. The 40S subunit is the site of
attachment and translation of mRNA. The 60S subunit is responsible
for the release of the new protein and, where appropriate, attachment
to the endoplasmic reticulum via an intermediate docking protein that
directs the newly synthesized protein through the membrane into the
cisternal space.
Golgi apparatus (Golgi complex)
Fig . 1 .4 Smooth endoplasmic reticulum with associated vesicles . The The Golgi apparatus is a distinct cytomembrane system located near the
dense particles are glycogen granules . (Courtesy of Rose Watson, Cancer nucleus and the centrosome. It is particularly prominent in secretory
Research UK .) cells and can be visualized when stained with silver or other metallic | 34 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
6.e1
1
RETPaHC
The glycocalyx plays a significant role in maintenance of the integrity
of tissues and in a wide range of dynamic cellular processes, e.g. serving
as a vascular permeability barrier and transducing fluid shear stress to
the endothelial cell cytoskeleton (Weinbaum et al 2007). Disruption of
the glycocalyx on the endothelial surface of large blood vessels precedes
inflammation, a conditioning factor of atheromatosis (e.g. deposits of
cholesterol in the vascular wall leading to partial or complete obstruc-
tion of the vascular lumen).
Protein synthesis on ribosomes may be suppressed by a class of RNA
molecules known as small interfering RNA (siRNA) or silencing RNA.
These molecules are typically 20–25 nucleotides in length and bind (as
a complex with proteins) to specific mRNA molecules via their comple-
mentary sequence. This triggers the enzymatic destruction of the mRNA
or prevents the movement of ribosomes along it. Synthesis of the
encoded protein is thus prevented. Their normal function may have
antiviral or other protective effects; there is also potential for developing
artificial siRNAs as a therapeutic tool for silencing disease-related genes. | 35 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
7
1
RETPaHC
A B
N
GG
V
GG M
C Phagocytic pathway Secretory pathway Membrane recycling Receptor-mediated endocytosis
Clathrin-coated pit
Early endosome
Late endosome
Lysosomal
fusion
Secondary lysosome
Residual body
Vesicle shuttling
between cisternae trans-Golgi network
Golgi cisternae
cis-Golgi network
Rough endoplasmic
reticulum
D E
G
R
Fig . 1 .5 The Golgi apparatus and functionally related organelles . A, Golgi apparatus (G) adjacent to the nucleus (N) (V, vesicle) . B, A large residual body
(tertiary lysosome) in a cardiac muscle cell (M, mitochondrion) . C, The functional relationships between the Golgi apparatus and associated cellular
structures . D, A three-dimensional reconstruction of the Golgi apparatus in a pancreatic β cell showing stacks of Golgi cisternae from the cis-face (pink)
and cis-medial cisternae (red, green) to the trans-Golgi network (blue, yellow, orange–red); immature proinsulin granules (condensing vesicles) are
shown in pale blue and mature (crystalline) insulin granules in dark blue . The flat colour areas represent cut faces of cisternae and vesicles . E, Rough
endoplasmic reticulum (R), associated with the Golgi apparatus (G) . (D, Courtesy of Dr Brad Marsh, Institute for Molecular Bioscience, University of
Queensland, Brisbane . A,B,E From human tissue, courtesy of Dr Bart Wagner, Histopathology Department, Sheffield Teaching Hospitals, UK .) | 36 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
8
1
NOITCES
salts. Traffic between the endoplasmic reticulum and the Golgi appara- Endocytic (internalization) pathway
tus is bidirectional and takes place via carrier vesicles derived from the
The endocytic pathway begins at the plasma membrane and ends in
donor site that bud, tether and fuse with the target site.
lysosomes involved in the degradation of the endocytic cargo through
Golgins are long coiled-coil proteins attached to the cytoplasmic
the enzymatic activity of lysosomal hydrolases. Endocytic cargo is
surface of cisternal membranes, forming a fibrillar matrix surrounding
internalized from the plasma membrane to early endosomes and
the Golgi apparatus to stabilize it; they have a role in vesicle trafficking
then to late endosomes. Late endosomes transport their cargo to lyso-
(for further reading on golgins, see Munro 2011). The Golgi apparatus
somes, where the cargo material is degraded following fusion and
has several functions: it links anterograde and retrograde protein and
mixing of contents of endosomes and lysosomes. Early endosomes
lipid flow in the secretory pathway; it is the site where protein and lipid
derive from endocytic vesicles (clathrin-coated vesicles and caveolae).
glycosylation occurs; and it provides membrane platforms to which
Once internalized, endocytic vesicles shed their coat of adaptin and
signalling and sorting proteins bind.
clathrin, and fuse to form an early endosome, where the receptor
Ultrastructurally, the Golgi apparatus (Fig. 1.5A) displays a contin-
molecules release their bound ligands. Membrane and receptors from
uous ribbon-like structure consisting of a stack of several flattened
the early endosomes can be recycled to the cell surface as exocytic
membranous cisternae, together with clusters of vesicles surrounding
vesicles.
its surfaces. Cisternae differ in enzymatic content and activity. Small
Clathrin-dependent endocytosis occurs at specialized patches of
transport vesicles from the rough endoplasmic reticulum are received
plasma membrane called coated pits; this mechanism is also used to
at one face of the Golgi stack, the convex cis-face (entry or forming
internalize ligands bound to surface receptor molecules and is also
surface). Here, they deliver their contents to the first cisterna in the
termed receptor-mediated endocytosis. Caveolae (little caves) are struc-
series by membrane fusion. From the edges of this cisterna, the protein
turally distinct pinocytotic vesicles most widely used by endothelial and
is transported to the next cisterna by vesicular budding and then
smooth muscle cells, when they are involved in transcytosis, signal
fusion, and this process is repeated across medial cisternae until the
transduction and possibly other functions. In addition to late endo-
final cisterna at the concave trans-face (exit or condensing surface) is
somes, lysosomes can also fuse with phagosomes, autophagosomes
reached. Here, larger vesicles are formed for delivery to other parts of
and plasma membrane patches for membrane repair. Lysosomal hydro-
the cell.
lases process or degrade exogenous materials (phagocytosis or hetero-
The cis-Golgi and trans-Golgi membranous networks form an inte-
phagy) as well as endogenous material (autophagy). Phagocytosis
gral part of the Golgi apparatus. The cis-Golgi network is a region of
consists of the cellular uptake of invading pathogens, apoptotic cells
complex membranous channels interposed between the rough endo-
and other foreign material by specialized cells. Lysosomes are numerous
plasmic reticulum and the Golgi cis-face, which receives and transmits
in actively phagocytic cells, e.g. macrophages and neutrophil granulo-
vesicles in both directions. Its function is to select appropriate proteins
cytes, in which lysosomes are responsible for destroying phagocytosed
synthesized on the rough endoplasmic reticulum for delivery by vesicles
particles, e.g. bacteria. In these cells, the phagosome, a vesicle poten-
to the Golgi stack, while inappropriate proteins are shuttled back to the
tially containing a pathogenic microorganism, may fuse with several
rough endoplasmic reticulum.
lysosomes.
The trans-Golgi network, at the other side of the Golgi stack, is also
Autophagy involves the degradation and recycling within an
a region of interconnected membrane channels engaged in protein
autophagosome of cytoplasmic components that are no longer needed,
sorting. Here, modified proteins processed in the Golgi cisternae are
including organelles. The assembly of the autophagosome involves
packaged selectively into vesicles and dispatched to different parts of
several proteins, including autophagy-related (Atg) proteins, as well as
the cell. The packaging depends on the detection, by the trans-Golgi
Hsc70 chaperone, that translocate the substrate into the lysosome (Boya
network, of particular amino-acid signal sequences, leading to their
et al 2013). Autophagosomes sequester cytoplasmic components and
enclosure in membranes of appropriate composition that will further
then fuse with lysosomes without the participation of a late endosome.
modify their contents, e.g. by extracting water to concentrate them
The 26S proteasome (see below) is also involved in cellular degradation
(vesicles entering the exocytosis pathway) or by pumping in protons to
but autophagy refers specifically to a lysosomal degradation–recycling
acidify their contents (lysosomes destined for the intracellular sorting
pathway. Autophagosomes are seen in response to starvation and cell
pathway).
growth.
Within the Golgi stack proper, proteins undergo a series of sequen-
Late endosomes receive lysosomal enzymes from primary lysosomes
tial chemical modifications by Golgi resident enzymes synthesized
derived from the Golgi apparatus after late endosome–lysosome mem-
in the rough endoplasmic reticulum. These include: glycosylation
brane tethering and fusion followed by diffusion of lysosomal contents
(changes in glycosyl groups, e.g. removal of mannose, addition of
into the endosomal lumen. The pH inside the fused hybrid organelle,
N-acetylglucosamine and sialic acid); sulphation (addition of sulphate
now a secondary lysosome, is low (about 5.0) and this activates lyso-
groups to glycosaminoglycans); and phosphorylation (addition of
somal acid hydrolases to degrade the endosomal contents. The products
phosphate groups). Some modifications serve as signals to direct pro-
of hydrolysis either are passed through the membrane into the cytosol,
teins and lipids to their final destination within cells, including lyso-
or may be retained in the secondary lysosome. Secondary lysosomes
somes and plasma membrane. Lipids formed in the endoplasmic
may grow considerably in size by vesicle fusion to form multivesicular
reticulum are also routed for incorporation into vesicles.
bodies, and the enzyme concentration may increase greatly to form
large lysosomes (Fig. 1.5B).
Exocytic (secretory) pathway
Secreted proteins, lipids, glycoproteins, small molecules such as amines
Lysosomes
and other cellular products destined for export from the cell are trans-
ported to the plasma membrane in small vesicles released from the Lysosomes are membrane-bound organelles 80–800 nm in diameter,
trans-face of the Golgi apparatus. This pathway either is constitutive, in often with complex inclusions of material undergoing hydrolysis (sec-
which transport and secretion occur more or less continuously, as with ondary lysosomes). Two classes of proteins participate in lysosomal
immunoglobulins produced by plasma cells, or it is regulated by exter- function: soluble acid hydrolases and integral lysosomal membrane
nal signals, as in the control of salivary secretion by autonomic neural proteins. Each of the 50 known acid hydrolases (including proteases,
stimulation. In regulated secretion, the secretory product is stored tem- lipases, carbohydrases, esterases and nucleases) degrades a specific sub-
porarily in membrane-bound secretory granules or vesicles. Exocytosis strate. There are about 25 lysosomal membrane proteins participating
is achieved by fusion of the secretory vesicular membrane with the in the acidification of the lysosomal lumen, protein import from the
plasma membrane and release of the vesicle contents into the extracel- cytosol, membrane fusion and transport of degradation products to the
lular domain. In polarized cells, e.g. most epithelia, exocytosis occurs cytoplasm. Material that has been hydrolysed within secondary lyso-
at the apical plasma membrane. Glandular epithelial cells secrete into somes may be completely degraded to soluble products, e.g. amino
a duct lumen, as in the pancreas, or on to a free surface, such as the acids, which are recycled through metabolic pathways. However, degra-
lining of the stomach. In hepatocytes, bile is secreted across a very small dation is usually incomplete and some debris remains. A debris-laden
area of plasma membrane forming the wall of the bile canaliculus. This vesicle is called a residual body or tertiary lysosome (see Fig. 1.5B), and
region is defined as the apical plasma membrane and is the site of may be passed to the cell surface, where it is ejected by exocytosis;
exocrine secretion, whereas secretion of hepatocyte plasma proteins alternatively, it may persist inside the cell as an inert residual body.
into the blood stream is targeted to the basolateral surfaces facing the Considerable numbers of residual bodies can accumulate in long-lived
sinusoids. Packaging of different secretory products into appropriate cells, often fusing to form larger dense vacuoles with complex lamellar
vesicles takes place in the trans-Golgi network. Delivery of secretory inclusions. As their contents are often darkly pigmented, this may
vesicles to their correct plasma membrane domains is achieved by change the colour of the tissue; e.g. in neurones, the end-product of
sorting sequences in the cytoplasmic tails of vesicular membrane lysosomal digestion, lipofuscin (neuromelanin or senility pigment),
proteins. gives ageing brains a brownish-yellow colouration. Lysosomal enzymes | 37 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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Carrier vesicles in transit from the endoplasmic reticulum to the
Golgi apparatus (anterograde transport) are coated by coat protein
complex II (COPII), whereas COPI-containing vesicles function in the
retrograde transport route from the Golgi apparatus (reviewed in Spang
(2013)).
The membranes contain specific signal proteins that may allocate
them to microtubule-based transport pathways and allow them to dock
with appropriate targets elsewhere in the cell, e.g. the plasma mem-
brane in the case of secretory vesicles. Vesicle formation and budding
at the trans-Golgi network involves the addition of clathrin on their
external surface, to form coated pits.
Specialized cells of the immune system, called antigen-presenting
cells, degrade protein molecules, called antigens, transported by the
endocytic pathway for lysosomal breakdown, and expose their frag-
ments to the cell exterior to elicit an immune response mediated ini-
tially by helper T cells. | 38 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
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RETPaHC
may also be secreted – often as part of a process to alter the extracellular A
matrix, as in osteoclast-mediated erosion during bone resorption. For
further reading on lysosome biogenesis, see Saftig and Klumperman
(2009).
lysosomal dysfunction
Lysosomal storage diseases (LSDs) are a consequence of lysosomal
dysfunction. Approximately 60 different types of LSD have been identi-
fied on the basis of the type of material accumulated in cells (such as
mucopolysaccharides, sphingolipids, glycoproteins, glycogen and lipo-
fuscins). LSDs are characterized by severe neurodegeneration, mental
decline, and cognitive and behavioural abnormalities. Autophagy
impairment caused by defective lysosome–autophagosome coupling
triggers a pathogenic cascade by the accumulation of substrates that
contribute to neurodegenerative disorders including Parkinson’s dis-
ease, Alzheimer’s disease, Huntington’s disease and several tau-opathies.
Many lysosomal storage diseases are known, e.g. Tay–Sachs disease
(GM2 gangliosidosis), in which a faulty β-hexosaminidase A leads to
the accumulation of the glycosphingolipid GM2 ganglioside in neu-
rones, causing death during childhood. In Danon disease, a vacuolar
skeletal myopathy and cardiomyopathy with neurodegeneration in
hemizygous males, lysosomes fail to fuse with autophagosomes because
of a mutation of the lysosomal membrane protein LAMP-2 (lysosomal B
associated membrane protein-2).
26S proteasome
Outer membrane
A protein can be degraded by different mechanisms, depending on
the cell type and different pathological conditions. Furthermore, the
same substrate can engage different proteolytic pathways (Park and Inner membrane
Cuervo 2013). Three major protein degradation mechanisms operate
in eukaryotic cells to dispose of non-functional cellular proteins: Cristae (folds)
the autophagosome–lysosomal pathway (see above); the apoptotic
procaspase–caspase pathway (see below); and the ubiquitinated Elementary
particles
protein–26S proteasome pathway. The 26S proteasome is a multicata-
lytic protease found in the cytosol and the nucleus that degrades intra-
cellular proteins conjugated to a polyubiquitin chain by an enzymatic
cascade. The 26S proteasome consists of several subunits arranged into
two 19S polar caps, where protein recognition and adenosine 5′-
triphosphate (ATP)-dependent target processing occur, flanking a 20S
central barrel-shaped structure with an inner proteolytic chamber
(Tomko and Hochstrasser 2013). The 26S proteasome participates in
the removal of misfolded or abnormally assembled proteins, the deg-
radation of cyclins involved in the control of the cell cycle, the process-
ing and degradation of transcription regulators, cellular-mediated Fig . 1 .6 A, Mitochondria in human cardiac muscle . The folded cristae
immune responses, and cell cycle arrest and apoptosis. (arrows) project into the matrix from the inner mitochondrial membrane .
B, The location of the elementary particles that couple oxidation and
Peroxisomes
phosphorylation reactions . (A, Courtesy of Dr Bart Wagner,
Peroxisomes are small (0.2–1 µm in diameter) membrane-bound Histopathology Department, Sheffield Teaching Hospitals, UK .)
organelles present in most mammalian cells. They contain more than
50 enzymes responsible for multiple catabolic and synthetic biochemi-
cal pathways, in particular the β-oxidation of very-long-chain fatty Mitochondria
acids (>C22) and the metabolism of hydrogen peroxide (hence the In the electron microscope, mitochondria usually appear as round or
name peroxisome). Peroxisomes derive from the endoplasmic reticu- elliptical bodies 0.5–2.0 µm long (Fig. 1.6), consisting of an outer
lum through the transfer of proteins from the endoplasmic reticulum mitochondrial membrane; an inner mitochrondrial membrane, sepa-
to peroxisomes by vesicles that bud from specialized sites of the endo- rated from the outer membrane by an intermembrane space; cristae,
plasmic reticulum and by a lipid non-vesicular pathway. All matrix infoldings of the inner membrane that harbour ATP synthase to gener-
proteins and some peroxisomal membrane proteins are synthesized by ate ATP; and the mitochondrial matrix, a space enclosed by the inner
cytosolic ribosomes and contain a peroxisome targeting signal that membrane and numerous cristae. The permeability of the two mito-
enables them to be imported by proteins called peroxins (Braverman chondrial membranes differs considerably: the outer membrane is
et al 2013, Theodoulou et al 2013). Mature peroxisomes divide by freely permeable to many substances because of the presence of large
small daughter peroxisomes pinching off from a large parental non-specific channels formed by proteins (porins), whereas the inner
peroxisome. membrane is permeable to only a narrow range of molecules. The pres-
Peroxisomes often contain crystalline inclusions composed mainly ence of cardiolipin, a phospholipid, in the inner membrane may con-
of high concentrations of the enzyme urate oxidase. Oxidases use tribute to this relative impermeability.
molecular oxygen to oxidize specific organic substrates (such as L-amino Mitochondria are the principal source of chemical energy in most
acids, D-amino acids, urate, xanthine and very-long-chain fatty acids) cells. Mitochondria are the site of the citric acid (Krebs’) cycle and the
and produce hydrogen peroxide that is detoxified (degraded) by per- electron transport (cytochrome) pathway by which complex organic
oxisomal catalase. Peroxisomes are particularly numerous in hepato- molecules are finally oxidized to carbon dioxide and water. This process
cytes. Peroxisomes are important in the oxidative detoxification of provides the energy to drive the production of ATP from adenosine
various substances taken into or produced within cells, including diphosphate (ADP) and inorganic phosphate (oxidative phosphoryla-
ethanol. Peroxin mutation is a characteristic feature of Zellweger syn- tion). The various enzymes of the citric acid cycle are located in the
drome (craniofacial dysmorphism and malformations of brain, liver, mitochondrial matrix, whereas those of the cytochrome system and
eye and kidney; cerebrohepatorenal syndrome). Neonatal leukodystro- oxidative phosphorylation are localized chiefly in the inner mitochon-
phy is an X-linked peroxisomal disease affecting mostly males, caused drial membrane.
by deficiency in β-oxidation of very-long-chain fatty acids. The build-up The intermembrane space houses cytochrome c, a molecule involved
of very-long-chain fatty acids in the nervous system and suprarenal in activation of apoptosis.
glands determines progressive deterioration of brain function and The number of mitochondria in a particular cell reflects its general
suprarenal insufficiency (Addison’s disease). For further reading, see energy requirements; e.g. in hepatocytes there may be as many as 2000,
Braverman et al (2013). whereas in resting lymphocytes there are usually very few. Mature | 39 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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The transcription factor EB (TFEB) is responsible for regulating lyso-
somal biogenesis and function, lysosome-to-nucleus signalling and
lipid catabolism (for further reading, see Settembre et al (2013)). If any
of the actions of lysosomal hydrolases, of the lysosome acidification
mechanism or of lysosomal membrane proteins fails, the degradation
and recycling of extracellular substrates delivered to lysosomes by the
late endosome and the degradation and recycling of intracellular sub-
strates by autophagy lead to progressive lysosomal dysfunction in
several tissues and organs.
Experimentally, TFEB activation can reduce the accumulation of
the pathogenic protein in a cellular model of Huntington’s disease (a
neurodegenerative genetic disorder that affects muscle coordination)
and improves the Parkinson’s disease phenotype in a murine model.
Cristae are abundant in mitochondria seen in cardiac muscle
cells and in steroid-producing cells (in the suprarenal cortex, corpus
luteum and Leydig cells). The protein steroidogenic acute regulatory
protein (StAR) regulates the synthesis of steroids by transporting
cholesterol across the outer mitochondrial membrane. A mutation
in the gene encoding StAR causes defective suprarenal and gonadal
steroidogenesis. | 40 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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erythrocytes lack mitochondria altogether. Cells with few mitochondria ent and its electronic charge, and the potential difference across the
generally rely largely on glycolysis for their energy supplies. These membrane. These factors combine to produce an electrochemical gradi-
include some very active cells, e.g. fast twitch skeletal muscle fibres, ent, which governs ion flux. Channel proteins are utilized most effec-
which are able to work rapidly but for only a limited duration. Mito- tively by the excitable plasma membranes of nerve cells, where the
chondria appear in the light microscope as long, thin structures in the resting membrane potential can change transiently from about −80 mV
cytoplasm of most cells, particularly those with a high metabolic rate, (negative inside the cell) to +40 mV (positive inside the cell) when
e.g. secretory cells in exocrine glands. In living cells, mitochondria stimulated by a neurotransmitter (as a result of the opening and sub-
constantly change shape and intracellular position; they multiply by sequent closure of channels selectively permeable to sodium and
growth and fission, and may undergo fusion. potassium).
The mitochondrial matrix is an aqueous environment. It contains a Carrier proteins bind their specific solutes, such as amino acids, and
variety of enzymes, and strands of mitochondrial DNA with the capacity transport them across the membrane through a series of conforma-
for transcription and translation of a unique set of mitochondrial genes tional changes. This latter process is slower than ion transport through
(mitochondrial mRNAs and transfer RNAs, mitochondrial ribosomes membrane channels. Transport by carrier proteins can occur either pas-
with rRNAs). The DNA forms a closed loop, about 5 µm across; several sively by simple diffusion, or actively against the electrochemical gradi-
identical copies are present in each mitochondrion. The ratio between ent of the solute. Active transport must therefore be coupled to a source
its bases differs from that of nuclear DNA, and the RNA sequences also of energy, such as ATP generation, or energy released by the coordinate
differ in the precise genetic code used in protein synthesis. At least 13 movement of an ion down its electrochemical gradient. Linked trans-
respiratory chain enzymes of the matrix and inner membrane are port can be in the same direction as the solute, in which case the carrier
encoded by the small number of genes along the mitochondrial DNA. protein is described as a symporter, or in the opposite direction, when
The great majority of mitochondrial proteins are encoded by nuclear the carrier acts as an antiporter.
genes and made in the cytosol, then inserted through special channels
in the mitochondrial membranes to reach their destinations. Their Translocation of proteins across
membrane lipids are synthesized in the endoplasmic reticulum. intracellular membranes
It has been shown that mitochondria are of maternal origin because Proteins are generally synthesized on ribosomes in the cytosol or on
the mitochondria of spermatozoa are not generally incorporated the rough endoplasmic reticulum. A few are made on mitochondrial
into the ovum at fertilization. Thus mitochondria (and mitochondrial ribosomes. Once synthesized, many proteins remain in the cytosol,
genetic variations and mutations) are passed only through the where they carry out their functions. Others, such as integral membrane
female line. proteins or proteins for secretion, are translocated across intracellular
Mitochondria are distributed within a cell according to regional membranes for post-translational modification and targeting to their
energy requirements, e.g. near the bases of cilia in ciliated epithelia, in destinations. This is achieved by the signal sequence, an addressing
the basal domain of the cells of proximal convoluted tubules in the system contained within the protein sequence of amino acids, which is
renal cortex (where considerable active transport occurs) and around recognized by receptors or translocators in the appropriate membrane.
the proximal segment, called middle piece, of the flagellum in sperma- Proteins are thus sorted by their signal sequence (or set of sequences
tozoa. They may be involved with tissue-specific metabolic reactions, that become spatially grouped as a signal patch when the protein folds
e.g. various urea-forming enzymes are found in liver cell mitochondria. into its tertiary configuration), so that they are recognized by and enter
Moreover, a number of genetic diseases of mitochondria affect particu- the correct intracellular membrane compartment.
lar tissues exclusively, e.g. mitochondrial myopathies (skeletal muscle)
and mitochondrial neuropathies (nervous tissue). For further informa-
Cell signalling
tion on mitochondrial genetics and disorders, see Chinnery and Hudson
(2013).
Cellular systems in the body communicate with each other to coordi-
Cytosolic inclusions nate and integrate their functions. This occurs through a variety of
The aqueous cytosol surrounds the membranous organelles described processes known collectively as cell signalling, in which a signalling
above. It also contains various non-membranous inclusions, including molecule produced by one cell is detected by another, almost always by
free ribosomes, components of the cytoskeleton, and other inclusions, means of a specific receptor protein molecule. The recipient cell trans-
such as storage granules (e.g. glycogen), pigments (such as lipofuscin duces the signal, which it most often detects at the plasma membrane,
granules, remnants of the lipid oxidative mechanism seen in the supra- into intracellular chemical messages that change cell behaviour.
renal cortex) and lipid droplets. The signal may act over a long distance, e.g. endocrine signalling
through the release of hormones into the blood stream, or neuronal
lipid droplets synaptic signalling via electrical impulse transmission along axons
Lipid droplets are spherical bodies of various sizes found within many and subsequent release of chemical transmitters of the signal at syn-
cells, but are especially prominent in the adipocytes (fat cells) of apses or neuromuscular junctions. A specialized variation of endocrine
adipose connective tissue. They do not belong to the Golgi-related vacu- signalling (neurocrine or neuroendocrine signalling) occurs when neu-
olar system of the cell. They are not membrane-bound, but are droplets rones or paraneurones (e.g. chromaffin cells of the suprarenal medulla)
of lipid suspended in the cytosol and surrounded by perilipin proteins, secrete a hormone into interstitial fluid and the blood stream.
which regulate lipid storage and lipolysis. See Smith and Ordovás Alternatively, signalling may occur at short range through a paracrine
(2012) for further reading on obesity and perilipins. In cells specialized mechanism, in which cells of one type release molecules into the inter-
for lipid storage, the vacuoles reach 80 µm or more in diameter. They stitial fluid of the local environment, to be detected by nearby cells of
function as stores of chemical energy, thermal insulators and mechani- a different type that express the specific receptor protein. Neurocrine
cal shock absorbers in adipocytes. In many cells, they may represent cell signalling uses chemical messengers found also in the central
end-products of other metabolic pathways, e.g. in steroid-synthesizing nervous system, which may act in a paracrine manner via interstitial
cells, where they are a prominent feature of the cytoplasm. They may fluid or reach more distant target tissues via the blood stream. Cells
also be secreted, as in the alveolar epithelium of the lactating breast. may generate and respond to the same signal. This is autocrine signal-
ling, a phenomenon that reinforces the coordinated activities of a group
Transport across cell membranes of like cells, which respond together to a high concentration of a local
Lipid bilayers are increasingly impermeable to molecules as they signalling molecule. The most extreme form of short-distance signalling
increase in size or hydrophobicity. Transport mechanisms are therefore is contact-dependent (juxtacrine) signalling, where one cell responds to
required to carry essential polar molecules, including ions, nutrients, transmembrane proteins of an adjacent cell that bind to surface recep-
nucleotides and metabolites of various kinds, across the plasma mem- tors in the responding cell membrane. Contact-dependent signalling
brane and into or out of membrane-bound intracellular compartments. also includes cellular responses to integrins on the cell surface binding
Transport is facilitated by a variety of membrane transport proteins, to elements of the extracellular matrix. Juxtacrine signalling is impor-
each with specificity for a particular class of molecule, e.g. sugars. Trans- tant during development and in immune responses. These different
port proteins fall mainly into two major classes: channel proteins and types of intercellular signalling mechanism are illustrated in Figure 1.7.
carrier proteins. For further reading on cell signalling pathways, see Kierszenbaum and
Channel proteins form aqueous pores in the membrane, which open Tres (2012).
and close under the regulation of intracellular signals, e.g. G-proteins,
Signalling molecules and their receptors
to allow the flux of solutes (usually inorganic ions) of specific size and
charge. Transport through ion channels is always passive, and ion flow The majority of signalling molecules (ligands) are hydrophilic and so
through an open channel depends only on the ion concentration gradi- cannot cross the plasma membrane of a recipient cell to effect changes | 41 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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Mitochondrial ribosomes are smaller and quite distinct from those
of the rest of the cell in that they (and mitochondrial nucleic acids)
resemble those of bacteria. This similarity underpins the theory that
mitochondrial ancestors were oxygen-utilizing bacteria that existed in
a symbiotic relationship with eukaryotic cells unable to metabolize the
oxygen produced by early plants. As mitochondria are formed only
from previously existing ones, it follows that all mitochondria in the
body are descended from those in the cytoplasm of the fertilized ovum. | 42 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
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RETPaHC
A Endocrine B Paracrine
Short-range signalling
molecule
Endocrine cell A
Endocrine cell B Receptor Y Sig cn ea ll lling
Receptor X
Target
cells
Target cell B
Different
Target cell A
Blood stream hormones
C Autocrine D Synaptic
Neurone
Synapse
Membrane receptor Axon
Hormone or Cell body Neurotransmitter Target cell
growth factor
E Neurocrine F Contact-dependent
Neuroendocrine Neuropeptide
Stimulus cell or amine Signalling cell Target cell
Blood vessel
Membrane-bound
Distant target cell signal molecule
Fig . 1 .7 The different modes of cell–cell signalling .
inside the cell unless they first bind to a plasma membrane receptor among signalling molecules in having no specific receptor protein; it
protein. Ligands are mainly proteins (usually glycoproteins), polypep- acts directly on intracellular enzymes of the response pathway.
tides or highly charged biogenic amines. They include: classic peptide
hormones of the endocrine system; cytokines, which are mainly of Receptor proteins
haemopoietic cell origin and involved in inflammatory responses and There are some 20 different families of receptor proteins, each with
tissue remodelling (e.g. the interferons, interleukins, tumour necrosis several isoforms responding to different ligands. The great majority of
factor, leukaemia inhibitory factor); and polypeptide growth factors these receptors are transmembrane proteins. Members of each family
(e.g. the epidermal growth factor superfamily, nerve growth factor, share structural features that indicate either shared ligand-binding char-
platelet-derived growth factor, the fibroblast growth factor family, trans- acteristics in the extracellular domain or shared signal transduction
forming growth factor beta and the insulin-like growth factors). properties in the cytoplasmic domain, or both. There is little relation-
Polypeptide growth factors are multifunctional molecules with more ship either between the nature of a ligand and the family of receptor
widespread actions and cellular sources than their names suggest. They proteins to which it binds and activates, or the signal transduction
and their receptors are commonly mutated or aberrantly expressed in strategies by which an intracellular response is achieved. The same
certain cancers. The cancer-causing gene variant is termed a transform- ligand may activate fundamentally different types of receptor in differ-
ing oncogene and the normal (wild-type) version of the gene is a cel- ent cell types.
lular oncogene or proto-oncogene. The activated receptor acts as a Cell surface receptor proteins are generally grouped according to
transducer to generate intracellular signals, which are either small dif- their linkage to one of three intracellular systems: ion channel-linked
fusible second messengers (e.g. calcium, cyclic adenosine monophos- receptors; G-protein coupled receptors; and receptors that link to
phate or the plasma membrane lipid-soluble diacylglycerol), or larger enzyme systems. Other receptors do not fit neatly into any of these
protein complexes that amplify and relay the signal to target control categories. All the known G-protein coupled receptors belong to a
systems. structural group of proteins that pass through the membrane seven
Some signals are hydrophobic and able to cross the plasma mem- times in a series of serpentine loops. These receptors are thus known as
brane freely. Classic examples are the steroid hormones, thyroid hor- seven-pass transmembrane receptors or, because the transmembrane
mones, retinoids and vitamin D. Steroids, for instance, enter cells regions are formed from α-helical domains, as seven-helix receptors.
non-selectively, but elicit a specific response only in those target cells The best known of this large group of phylogenetically ancient receptors
that express specific cytoplasmic or nuclear receptors. Light stimuli also are the odorant-binding proteins of the olfactory system; the light-
cross the plasma membranes of photoreceptor cells and interact intra- sensitive receptor protein, rhodopsin; and many of the receptors for
cellularly, at least in rod cells, with membrane-bound photosensitive clinically useful drugs. A comprehensive list of receptor proteins, their
receptor proteins. Hydrophobic ligands are transported in the blood activating ligands and examples of the resultant biological function is
stream or interstitial fluids, generally bound to carrier proteins, and they given in Pollard and Earnshaw (2008).
often have a longer half-life and longer-lasting effects on their targets
than do water-soluble ligands. Intracellular signalling
A separate group of signalling molecules able to cross the plasma A wide variety of small molecules carry signals within cells, conveying
membrane freely is typified by the gas, nitric oxide. The principal target the signal from its source (e.g. activated plasma membrane receptor) to
of short-range nitric oxide signalling is smooth muscle, which relaxes its target (e.g. the nucleus). These second messengers convey signals as
in response. Nitric oxide is released from vascular endothelium as a fluctuations in local concentration, according to rates of synthesis and
result of the action of autonomic nerves that supply the vessel wall degradation by specific enzymes (e.g. cyclases involved in cyclic nucle-
causing local relaxation of smooth muscle and dilation of vessels. This otide (cAMP, cGMP) synthesis), or, in the case of calcium, according to
mechanism is responsible for penile erection. Nitric oxide is unusual the activities of calcium channels and pumps. Other, lipidic, second | 43 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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NOITCES
messengers such as phosphatidylinositol, derive from membranes and are microfilaments (7 nm thick), microtubules (25 nm thick) and inter-
may act within the membrane to generate downstream effects. For mediate filaments (10 nm thick). Other important components are
further consideration of the complexity of intracellular signalling path- proteins that bind to the principal filamentous types to assemble or
ways, see Pollard and Earnshaw (2008). disassemble them, regulate their stability or generate movement. These
include actin-binding proteins such as myosin, which in some cells can
Cytoskeleton assemble into thick filaments, and microtubule-associated proteins.
Pathologies involving cytoskeletal abnormalities include ciliopathies
(resulting from the abnormal assembly and function of centrioles, basal
The cytoskeleton is a three-dimensional network of filamentous intra-
bodies and cilia); neurodegenerative diseases (a consequence of defec-
cellular proteins of different shapes, sizes and composition distributed
tive anterograde transport of neurotransmitters along microtubules in
throughout the cytoplasm. It provides mechanical support, maintains
axons); and sterility (determined by defective or absent microtubule-
cell shape and rigidity, and enables cells to adopt highly asymmetric or
associated dynein in axonemes, e.g. Kartagener’s syndrome).
irregular profiles. It plays an important part in establishing structural
polarity and different functional domains within a cell. It also provides
Actin filaments (microfilaments)
mechanical support for permanent projections from the cell surface (see
below), including persistent microvilli and cilia, and transient proc- Actin filaments are flexible filaments, 7 nm thick (Fig. 1.8). Within
esses, such as the thin finger-like protrusions called filopodia (0.1– most cell types, actin constitutes the most abundant protein and in
0.3 µm) and lamellipodia (0.1–0.2 µm). Filopodia consist of parallel some motile cells its concentration may exceed 200 µM (10 mg protein
bundles of actin filaments and have a role in cell migration, wound per ml cytoplasm). The filaments are formed by the ATP-dependent
healing and neurite growth. The protrusive thin and broad lamellipo- polymerization of actin monomer (with a molecular mass of 43 kDa)
dia, found at the leading edge of a motile cell, contain a branched into a characteristic string of beads in which the subunits are arranged
network of actin filaments. in a linear tight helix with a distance of 13 subunits between turns
The cytoskeleton restricts specific structures to particular cellular (Dominguez 2010). The polymerized filamentous form is termed
locations. For example, the Golgi apparatus is near the nucleus and F-actin (fibrillar actin) and the unpolymerized monomeric form is
endoplasmic reticulum, and mitochondria are near sites of energy known as G-actin (globular actin). Each monomer has an asymmetric
requirement. In addition, the cytoskeleton provides tracks for intracel- structure. When monomers polymerize, they confer a defined polarity
lular transport (e.g. shuttling vesicles and macromolecules, called on the filament: the plus or barbed end favours monomer addition,
cargoes, among cytoplasmic sites), the movement of chromosomes and the minus or pointed end favours monomer dissociation.
during cell division (mitosis and meiosis) or movement of the entire Treadmilling designates the simultaneous polymerization of an
cell during embryonic morphogenesis or the chemotactic extravascular actin filament at one end and depolymerization at the other end to
migration of leukocytes during homing. Examples of highly developed maintain its constant length.
and specialized functions of the cytoskeleton include the contraction See Bray (2001) for further reading.
of the sarcomere in striated muscle cells and the bending of the axoneme
of cilia and flagella. actin-binding proteins
The catalogue of cytoskeletal structural proteins is extensive and still A wide variety of actin-binding proteins are capable of modulating the
increasing. The major filamentous structures found in non-muscle cells form of actin within the cell. These interactions are fundamental to the
Monomer Tubulin dimer Tetramer Fig . 1 .8 Structural and molecular
features of cytoskeletal components .
G-actin–ATP β-tubulin GTP A, The actin filament (F-actin) is a
7 nm thick polymer chain of
α-tubulin GTP
ATP-bound G-actin monomers .
F-actin consists of a barbed (plus)
GTP
end, the initiation site of F-actin,
and a pointed (minus) end, the
Plus end dissociation site of F-actin . F-actin
can be severed and capped at the
Barbed end barbed end by gelsolin . B, The
microtubule is a 25 nm diameter
polymer of GTP-bound α-tubulin and
Unit length filament
GTP-bound β-tubulin dimers . The
dimer assembles at the plus end and
depolymerizes at the minus end . A
linear chain of α-tubulin/β-tubulin
dimers is called a protofilament . In
the end-on (top view), a microtubule
displays 13 concentrically arranged
7 nm thick 25 nm in diameter tubulin subunits . C, Tetrameric
complexes of intermediate filament
subunits associate laterally to form a
unit length filament consisting of
Intermediate filament
eight tetramers . Additional unit length
filaments anneal longitudinally and
generate a mature 10 nm thick
intermediate filament .
Severed actin filament Minus end
Gelsolin
Capped barbed end Protofilament
10 nm thick
Pointed end
Top view:
13 concentric tubulins
A Actin filament B Microtubule C Intermediate filament | 44 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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Septins are emerging as a novel cytoskeletal member because of their
filamentous organization and association with actin filaments and
microtubules. They are guanosine triphosphate (GTP)-binding proteins
that form hetero-oligomeric complexes (see Mostowy and Cossart
(2012) for additional information).
This polarity can be visualized in negatively stained images by allow-
ing F-actin to react with fragments containing the active head region of
myosin. Myosins bind to filamentous actin at an angle to give the
appearance of a series of arrowheads pointing towards the minus end
of the filament, with the barbs pointing towards the plus end.
It involves the addition of ATP-bound G-actin monomers at the
barbed end (fast-growing plus end) and removal of ADP-bound G-actin
at the pointed end (slow-growing minus end). Actin filaments grow or
shrink by addition or loss of G-actin monomer at both ends. Essentially,
actin polymerization in vitro proceeds in three steps: nucleation (aggre-
gation of G-actin monomers into a 3–4-monomer aggregate), elonga-
tion (addition of G-actin monomers to the aggregate) and a dynamic
steady state (treadmilling). Specific toxins (e.g. cytochalasins, phalloi-
dins and lantrunculins) bind to actin and affect its polymerization.
Cytochalasin D blocks the addition of new G-actin monomers to the
barbed end of F-actin; phalloidin binds to the interface between G-actin
monomers in F-actin, thus preventing depolymerization; and lantrun-
culin binds to G-actin monomers, blocking their addition to an actin
filament. | 45 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
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Fig . 1 .9 The membrane at both ends), maintain a degree of active rigidity. Filamin
cytoskeleton . A, An interconnects adjacent actin filaments to produce loose filamentous
immunofluorescence gel-like networks composed of randomly orientated F-actin.
micrograph of α-actin F-actin can branch. The assembly of branched filamentous actin
microfilaments (green) in networks involves a complex of seven actin-related proteins 2/3
human airway smooth (Arp2/3) that is structurally similar to the barbed end of actin.
muscle cells in culture . See Rotty et al (2013) for further reading.
The actin-binding
Branched actin generated by the Arp2/3 protein complex localizes
protein, vinculin (red), is
at the leading edge of migrating cells, lamellipodia and phagosomes
localized at the ends of
(required for the capture by endocytosis and phagocytosis of particles
actin filament bundles;
and foreign pathogens by immune cells). Formin can elongate pre-
nuclei are blue . B, An
existing actin filaments by removing capping proteins at the barbed
immunofluorescence
end.
micrograph of keratin
intermediate filaments Other classes of actin-binding protein link the actin cytoskeleton to
(green) in human the plasma membrane either directly or indirectly through a variety of
keratinocytes in culture . membrane-associated proteins. The latter may also create links via
A
Desmosome junctions transmembrane proteins to the extracellular matrix. Best known of
are labelled with these is the family of spectrin-like molecules, which can bind to actin
antibody against and also to each other and to various membrane-associated proteins to
desmoplakin (red) . create supportive networks beneath the plasma membrane. Tetrameres
Nuclei are stained blue of spectrin α and β chains line the intracellular side of the plasma
(Hoechst) . C, An membrane of erythrocytes and maintain their integrity by their associa-
electron micrograph of tion with short actin filaments at either end of the tetramer.
human nerve showing Class V myosins are unconventional motor proteins transporting
microtubules (small, cargoes (such as vesicles and organelles) along actin filaments.
hollow structures in
Class I myosins are involved in membrane dynamics and actin organi-
cross-section, long
zation at the cell cortex, thus affecting cell migration, endocytosis,
arrow) in a transverse
pinocytosis and phagocytosis. Tropomyosin, an important regulatory
section of an
protein of muscle fibres, is also present in non-muscle cells, where
unmyelinated axon (A),
its function may be primarily to stabilize actin filaments against
engulfed by a Schwann
depolymerization.
cell (S) . Neuronal
intermediate filaments
Myosins, the motor proteins
(neurofilaments) are the
B solid, electron-dense The myosin family of microfilaments is often classified within a distinct
profiles, also in category of motor proteins. Myosin proteins have a globular head
transverse section (short region consisting of a heavy and a light chain. The heavy chain bears
arrow) . (A, Courtesy of an α-helical tail of varying length. The head has an ATPase activity and
Dr T Nguyen, Professor can bind to and move along actin filaments – the basis for myosin
J Ward, Dr SJ Hirst, function as a motor protein. The best-known class is myosin II, which
King’s College London . occurs in muscle and in many non-muscle cells. Its molecules have two
AA B, Courtesy of Prof . heads and two tails, intertwined to form a long rod. The rods can bind
Dr WW Franke, German to each other to form long, thick filaments, as seen in striated and
Cancer Research smooth muscle fibres and myoepithelial cells. Myosin II molecules can
Centre, Heidelberg . also assemble into smaller groups, especially dimers, which can cross-
C, Courtesy of Dr Bart
link individual actin microfilaments in stress fibres and other F-actin
Wagner, Histopathology
SS arrays. The ATP-dependent sliding of myosin on actin forms the basis
Department, Sheffield
for muscle contraction and the extension of microfilament bundles, as
Teaching Hospitals, UK .)
seen in cellular motility or in the contraction of the ring of actin and
myosin around the cleavage furrow of dividing cells. There are a number
of known subtypes of myosin II; they assemble in different ways and
have different dynamic properties. In skeletal muscle the myosin mol-
ecules form bipolar filaments 15 nm thick. Because these filaments have
C
a symmetric antiparallel arrangement of subunits, the midpoint is bare
of head regions. In smooth muscle the molecules form thicker, flattened
bundles and are orientated in random directions on either face of the
bundle. These arrangements have important consequences for the con-
organization of cytoplasm and to cell shape. The actin cytoskeleton is tractile force characteristics of the different types of muscle cell.
organized as closely packed parallel arrays of actin filaments forming Related molecules include the myosin I subfamily of single-headed
bundles or cables, or loosely packed criss-crossed actin filaments molecules with tails of varying length. Functions of myosin I include
forming networks (Fig. 1.9A). Actin-binding proteins hold together the movements of membranes in endocytosis, filopodial formation in
bundles and networks of actin filaments. Actin-binding proteins can neuronal growth cones, actin–actin sliding and attachment of actin to
be grouped into G-actin (monomer) binding proteins and F-actin membranes as seen in microvilli. As indicated above, molecular motors
(polymer) capping, cross-linking and severing proteins. Actin-binding of the myosin V family are implicated in the movements of cargoes on
proteins may have more than one function. actin filaments. So, for example, myosin Va transports vesicles along
Capping proteins bind to the ends of the actin filament either F-actin tracks in a similar manner to kinesin and cytoplasmic dynein-
to stabilize an actin filament or to promote its disassembly (see related cargo transport along microtubules. Each class of motor protein
Fig. 1.8). has different properties, but during cargo trafficking they often function
Cross-linking or bundling proteins tie actin filaments together in together in a coordinated fashion. (See Hammer 3rd and Sellers (2012)
longitudinal arrays to form bundles, cables or core structures. The for further reading on class V myosins.)
bundles may be closely packed in microvilli and filopodia, where paral-
lel filaments are tied tightly together to form stiff bundles orientated in Other thin filaments
the same direction. Cross-linking proteins of the microvillus actin A heterogeneous group of filamentous structures with diameters of
bundle core include fimbrin and villin. 2–4 nm occurs in various cells. The two most widely studied forms, titin
Other actin-bundling proteins form rather looser bundles of fila- and nebulin, constitute around 13% of the total protein of skeletal
ments that run antiparallel to each other with respect to their plus and muscle. They are amongst the largest known molecules and have
minus ends. They include myosin II, which can form cross-links with subunit weights of around 106; native molecules are about 1 µm in
ATP-dependent motor activity, and cause adjacent actin filaments to length. Their repetitive bead-like structure gives them elastic properties
slide on each other in the striated muscle sarcomere, and either change that are important for the effective functioning of muscle, and possibly
the shape of cells or (if the actin bundles are anchored into the cell for other cells. | 46 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
13.e1
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Profilin and thymosin β4 are G-actin binding proteins. Profilin binds In the presence of activated nucleation promotion factors, such as
to G-actin bound to ATP; it inhibits addition of G-actin to the slow- Wiskott–Aldrich syndrome protein (WASP) and WASP family verprolin-
growing (pointed) end of F-actin but enables the fast-growing (barbed) homologous protein (WAVE, also known as SCAR), the Arp2/3 protein
end to grow faster and then dissociates from the actin filament. In addi- complex binds to the side of an existing actin filament (mother fila-
tion, profilin participates in the conversion of ADP back to the ATP–G- ment) and initiates the formation of a branching actin daughter fila-
actin bound form. Thymosin β4 binds to the ATP–G-actin bound form, ment at a 70° angle relative to the mother filament utilizing G-actin
preventing polymerization by sequestering ATP–G-actin into a reserve delivered to the Arp2/3 complex site.
pool. Spectrin-related molecules are present in many other cells. For
Members of the F-actin capping protein family are heterodimers instance, fodrin is found in neurones and dystrophin occurs in muscle
consisting of an α subunit (CPα) and a β subunit (CPβ) that cap the cells, linking the contractile apparatus with the extracellular matrix via
barbed end of actin filaments within all eukaryotic cells. Gelsolin has integral membrane proteins. Proteins such as ankyrin (which also binds
a dual role: it severs F-actin and caps the newly formed barbed end, actin directly), vinculin, talin, zyxin and paxillin connect actin-binding
blocking further filament elongation. proteins to integral plasma membrane proteins such as integrins
Fascin is an additional cross-linking protein. Villin is also a severing (directly or indirectly), and thence to focal adhesions (consisting of a
protein, causing the disassembly of actin filaments and the collapse of bundle of actin filaments attached to a portion of a plasma membrane
the microvillus. linked to the extracellular matrix). | 47 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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NOITCES
Microtubules Fig . 1 .10 A duplicated
pair of centrioles in a
Microtubules are polymers of tubulin with the form of hollow, rela-
human carcinoma
tively rigid cylinders, approximately 25 nm in diameter and of varying
specimen . Each
length (up to 70 µm in spermatozoan flagella). They are present in most
TT centriole pair consists
cell types, being particularly abundant in neurones, leukocytes and
of a mother and
blood platelets. Microtubules are the predominant constituents of the
daughter, orientated
mitotic spindles of dividing cells and also form part of the axoneme of
approximately at right
cilia, flagella and centrioles. angles to each other so
Microtubules consist of tubulin dimers and microtubule-associated that one is sectioned
proteins. There are two major classes of tubulin: α- and β-tubulins. transversely (T) and the
Before microtubule assembly, tubulins are associated as dimers with a other longitudinally (L) .
combined molecular mass of 100 kDa (50 kDa each). Each protein The transversely
subunit is approximately 5 nm across and is arranged along the long sectioned centrioles
axis in straight rows of alternating α- and β-tubulins, forming protofila- are seen as rings of
ments (see Fig. 1.8). Typically, 13 protofilaments (the number can vary L microtubule triplets
between 11 and 16) associate in a ring to form the wall of a hollow (arrow) . (Courtesy of
cylindrical microtubule. Each longitudinal row is slightly out of align- Dr Bart Wagner,
ment with its neighbour, so that a spiral pattern of alternating α and β Histopathology
subunits appears when the microtubule is viewed from the side. There Department, Sheffield
Teaching Hospitals,
is a dynamic equilibrium between the dimers and assembled microtu-
UK .)
bules: dimeric asymmetry creates polarity (α-tubulins are all orientated
towards the minus end, β-tubulins towards the plus end). Tubulin is
added preferentially to the plus end; the minus end is relatively slow-
growing. Microtubules frequently grow and shrink at a rapid and con-
stant rate, a phenomenon known as dynamic instability, in which
growing tubules can undergo a ‘catastrophe’, abruptly shifting from net
growth to rapid shrinkage. The primary determinant of whether micro-
tubules grow or shrink is the rate of GTP hydrolysis. Tubulins are GTP-
binding proteins; microtubule growth is accompanied by hydrolysis of microtubules for considerable distances, thus enabling selective target-
GTP, which may regulate the dynamic behaviour of the tubules. Micro- ing of materials within the cell. Such movements occur in both direc-
tubule growth is initiated at specific sites, the microtubule-organizing tions along microtubules. Kinesin-dependent motion is usually towards
centres, of which the best known are centrosomes (from which most the plus ends of microtubules, e.g. from the cell body towards the axon
cellular microtubules polymerize) and the centriole-derived basal terminals in neurones, and away from the centrosome in other cells.
bodies (from which cilia grow). Microtubule-organizing centres include Conversely, dynein-related movements are in the opposite direction, i.e.
a specialized tubulin isoform known as γ-tubulin that is essential for to the minus ends of microtubules. Dyneins also form the arms of
the nucleation of microtubule growth. peripheral microtubules in cilia and flagella, where they make dynamic
Various drugs (e.g. colcemid, vinblastine, griseofulvin, nocodazole) cross-bridges to adjacent microtubule pairs. When these tethered
cause microtubule depolymerization by binding the soluble tubulin dyneins try to move, the resulting shearing forces cause the axonemal
dimers and so shifting the equilibrium towards the unpolymerized array of microtubules to bend, generating ciliary and flagellar beating
state. Microtubule disassembly causes a wide variety of effects, including movements. Kinesins form a large and diverse family of related
the inhibition of cell division by disruption of the mitotic spindle. microtubule-stimulated ATPases. Some kinesins are motors that move
Conversely, the drug paclitaxel (taxol) is a microtubule depolymeriza- cargo and others cause microtubule disassembly, whilst still others
tion inhibitor because it stabilizes microtubules and promotes abnor- cross-link mitotic spindle microtubules to push the two centriolar poles
mal microtubule assembly. Although this can cause a peripheral apart during mitotic prophase. See Bray (2001) for further reading.
neuropathy, paclitaxel is widely used as an effective chemotherapeutic
Centrioles, centrosomes and basal bodies
agent in the treatment of breast and ovarian cancer.
Centrioles are microtubular cylinders 0.2 µm in diameter and 0.4 µm
long (Fig. 1.10). They are formed by a ring of nine microtubule triplets
microtubule-associated proteins linked by a number of other proteins. At least two centrioles occur in
Various proteins that can bind to assembled tubulins may be concerned all animal cells that are capable of mitotic division (eggs, which undergo
with structural properties or associated with motility. One important meiosis instead of mitosis, lack centrioles). See Gönczy (2012) for
class of microtubule-associated proteins (MAPs) consists of proteins further reading on the structure and assembly of the centriole. They
that associate with the plus ends of microtubules. They regulate the usually lie close together, at right angles or, most usually, at an oblique
dynamic instability of microtubules as well as interactions with other angle to each other (an arrangement often termed a diplosome), within
cellular substructures. Structural MAPs form cross-bridges between adja- the centrosome, a densely filamentous region of cytoplasm at the centre
cent microtubules or between microtubules and other structures such of the cell. The centrosome is the major microtubule-organizing centre
as intermediate filaments, mitochondria and the plasma membrane. of most cells; it is the site at which new microtubules are formed and
Microtubule-associated proteins found in neurones include: MAPs 1A the mitotic spindle is generated during cell division. Centriole biogen-
and 1B, which are present in neuronal dendrites and axons; MAPs 2A esis is a complex process. At the beginning of the S phase (DNA replica-
and 2B, found chiefly in dendrites; and tau, found only in axons. MAP tion phase) of the cell cycle (see below), a new daughter centriole forms
4 is the major microtubule-associated protein in many other cell types. at right angles to each separated maternal centriole. Each mother–
Structural microtubule-associated proteins are implicated in microtu- daughter pair forms one pole of the next mitotic spindle, and the
bule formation, maintenance and disassembly, and are therefore of daughter centriole becomes fully mature only as the progeny cells are
considerable significance in cell morphogenesis, mitotic division, and about to enter the next mitosis. Because centrosomes are microtubule-
the maintenance and modulation of cell shape. Transport-associated organizing centres, they lie at the centre of a network of microtubules,
microtubule-associated proteins are found in situations in which move- all of which have their minus ends proximal to the centrosome.
ment occurs over the surfaces of microtubules, e.g. cargo transport, The microtubule-organizing centre contains complexes of γ-tubulin
bending of cilia and flagella, and some movements of mitotic spindles. that nucleate microtubule polymerization at the minus ends of micro-
They include a large family of motor proteins, the best known of which tubules. Basal bodies are microtubule-organizing centres that are closely
are the dyneins and kinesins. Another protein, dynamin, is involved in related to centrioles, and are believed to be derived from them. They
endocytosis. The kinetochore proteins assemble at the chromosomal are located at the bases of cilia and flagella, which they anchor to the
centromere during mitosis and meiosis. They attach (and thus fasten cell surface. The outer microtubule doublets of the axoneme of cilia and
chromosomes) to spindle microtubules; some of the kinetochore pro- flagella originate from two of the microtubules in each triplet of the
teins are responsible for chromosomal movements in mitotic and basal body.
meiotic anaphase.
All of these microtubule-associated proteins bind to microtubules microtubule-based transport of cargoes
and either actively slide along their surfaces or promote microtubule The transport of cargoes along microtubules via the motor proteins
assembly or disassembly. Kinesins and dyneins can simultaneously kinesin and cytoplasmic dynein respectively is the means by which
attach to membranes such as transport vesicles and convey them along neurotransmitters are delivered along axons to neuronal synapses | 48 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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The association of membrane vesicles with dynein motors means
that certain cytomembranes (including the Golgi apparatus) concen-
trate near the centrosome. This is convenient because the microtubules
provide a means of targeting Golgi vesicular products to different parts
of the cell. | 49 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
15
1
RETPaHC
(anterograde axonal transport) and membrane-bound vesicles are sion. Of the different classes of intermediate filaments, keratin (cyto-
returned for recycling to the neuronal soma (retrograde axonal trans- keratin) proteins are found in epithelia, where keratin filaments are
port) (p. 45). In addition to anterograde and retrograde motor proteins, always composed of equal ratios of type I (acidic) and type II (basic to
the assembly and maintenance of all cilia and flagella involve the par- neutral) keratins to form heteropolymers. About 20 types of each of the
ticipation of non-membrane-bound macromolecular protein com- acidic and basic/neutral keratin proteins are known. For further reading
plexes called intraflagellar transport (IFT) particles. IFT particles localize on keratins in normal and diseased epithelia, see Pan et al (2012).
along the polarized microtubules of the axoneme, beneath the ciliary Within the epidermis, expression of keratin heteropolymers changes as
and flagellar membrane. IFT particles consist of two protein subcom- keratinocytes mature during their transition from basal to superficial
plexes: IFT-A (with a role in returning cargoes from the tip of the layers. Genetic abnormalities of keratins are known to affect the
axoneme to the cell body) and IFT-B (with a role in delivering cargoes mechanical stability of epithelia. For example, the disease epidermolysis
from the cell body to the tip of the axoneme). For further reading, see bullosa simplex is caused by lysis of epidermal basal cells and blistering
Scholey (2008) and Hao and Scholey (2009). of the skin after mechanical trauma. Defects in genes encoding keratins
During ciliogenesis, IFT requires the anterograde kinesin-2 motor 5 and 14 produce cytoskeletal instability leading to cellular fragility in
and the retrograde IFT-dynein motor to transport IFT particles–cargo the basal cells of the epidermis. When keratins 1 and 10 are affected,
complexes in opposite directions along the microtubules, from the cells in the spinous (prickle) cell layer of the epidermis lyse, and this
basal body to the tip of the ciliary axoneme and back again (intraciliary produces the intraepidermal blistering of epidermolytic hyperkeratosis.
transport). IFT is not just restricted to microtubules of cilia and flagella. See Porter and Lane (2003) for further reading.
During spermatid development, IFT particles–motor protein–cargo Type III intermediate filament proteins, including vimentin, desmin,
complexes appear to utilize microtubules of the manchette, a transient glial fibrillary acidic protein and peripherin, form homopolymer inter-
microtubule-containing structure, to deliver tubulin dimers and other mediate filaments. Vimentin is expressed in mesenchyme-derived cells
proteins by intramanchette transport during the development of the of connective tissue and some ectodermal cells during early develop-
spermatid tail (Kierszenbaum et al 2011). IFT also occurs along the ment; desmins in muscle cells; glial fibrillary acidic protein in glial
modified cilium of photoreceptor cells of the retina. Mutations in IFT cells; and peripherin in peripheral axons. Type IV intermediate fila-
proteins lead to the absence of cilia and are lethal during embryogen- ments include neurofilaments, nestin, syncoilin and α-internexin. Neu-
esis. Ciliopathies, many related to the defective sensory and/or mechan- rofilaments are a major cytoskeletal element in neurones, particularly
ical function of cilia, include retinal degeneration, polycystic kidney in axons (see Fig. 1.9C), where they are the dominant protein. Neuro-
disease, Bardet–Biedl syndrome, Jeune asphyxiating thoracic dystrophy, filaments (NF) are heteropolymers of low (NF–L), medium (NF–M)
respiratory disease and defective determination of the left–right axis. and high (NF–H) molecular weight (the NF–L form is always present
The seven-protein complex designated BBSome (for Bardet–Biedl syn- in combination with either NF–M or NF–H forms). Abnormal accumu-
drome, an obesity/retinopathy ciliopathy) is a component of the basal lations of neurofilaments (neurofibrillary tangles) are characteristic
body and participates in the formation of the primary cilium by regulat- features of a number of neuropathological conditions. Nestin resem-
ing the export and/or import of ciliary proteins. The transport of the bles a neurofilament protein, which forms intermediate filaments in
BBSome up and down and round about in cilia occurs in association neurectodermal stem cells in particular. The type V intermediate fila-
with anterograde IFT-B and retrograde IFT-A particles. For further ment group includes the nuclear lamins A, lamin B1 and lamin B2
reading on the BBSome, see Jin and Nachury (2009). For further reading lining the inner surface of the nuclear envelope of all nucleated cells.
on ciliogenesis, see Baldari and Rosenbaum (2010). Lamin C is a splice variant of lamin A. Lamins provide a mechanical
framework for the nucleus and act as attachment sites for a number of
Intermediate filaments
proteins that organize chromatin at the periphery of the nucleus. They
Intermediate filaments are about 10 nm thick and are formed by a are unusual in that they form an irregular anastomosing network of
heterogeneous group of filamentous proteins. In contrast to actin fila- filaments rather than linear bundles. See Burke and Stewart (2013) for
ments and microtubules, which are assembled from globular proteins further reading.
with nucleotide-binding and hydrolysing activity, intermediate fila-
ments consist of filamentous monomers lacking enzymatic activity.
Nucleus
Intermediate filament proteins assemble to form linear filaments in a
three-step process. First, a pair of intermediate filament protein sub-
units, each consisting of a central α-helical rod domain of about 310 The nucleus (see Figs 1.1–1.2) is generally the largest intracellular struc-
amino acids flanked by head and tail non-α-helical domains of varia- ture and is usually spherical or ellipsoid in shape, with a diameter of
ble size, form a parallel dimer through their central α-helical rod 3–10 µm. Conventional histological stains, such as haematoxylin or
domains coiled around each other. The variability of intermediate fila- toluidine blue, detect the acidic components (phosphate groups) of
ment protein subunits resides in the length and amino-acid sequence deoxyribonucleic acid (DNA) and ribonucleic acid (RNA) in cells and
of the head and tail domains, thought to be involved in regulating the tissue sections. DNA and RNA molecules are said to be basophilic
interaction of intermediate filaments with other proteins. Second, a because of the binding affinity of their negatively charged phosphate
tetrameric unit is formed by two antiparallel half-staggered coiled groups to basic dyes such as haematoxylin. A specific stain for DNA is
dimers. Third, eight tetramers associate laterally to form a 16 nm thick the Feulgen reaction.
unit length filament (ULF). Individual ULFs join end to end to form
Nuclear envelope
short filaments that continue growing longitudinally by annealing to
other ULFs and existing filaments. Filament elongation is followed by The nucleus is surrounded by the nuclear envelope, which consists of
internal compaction leading to the 30 nm thick intermediate filament an inner nuclear membrane (INM) and an outer nuclear membrane
(see Fig. 1.8). The tight association of dimers, tetramers and ULFs pro- (ONM), separated by a 40–50 nm perinuclear space that is spanned by
vides intermediate filaments with high tensile strength and resistance nuclear pore complexes (NPCs). The perinuclear space is continuous
to stretching, compression, twisting and bending forces. In contrast to with the lumen of the endoplasmic reticulum. The ONM has multiple
actin filaments and microtubules, intermediate filaments are non- connections with the endoplasmic reticulum, with which it shares its
polar (because of the antiparallel alignment of the initial tetramers) membrane protein components. The INM contains its own specific
and do not bind nucleot ides (as in G-actin and tubulin dimers), and integral membrane proteins (lamin B receptor and emerin, both pro-
ULFs anneal end to end to each other (in contrast to the polarized viding binding sites for chromatin bridging proteins). A mutation in
F-actin and microtubules, with one end, the plus end, growing faster the gene encoding emerin causes X-linked Emery–Dreifuss muscular
than the other end, the minus end). See Herrmann et al (2007) for dystrophy (EDMD), characterized by skeletal muscle wasting and
further reading. cardiomyopathy.
Intermediate filaments are found in different cell types and are often The nuclear lamina, a 15–20 nm thick, protein-dense meshwork, is
present in large numbers, either to provide structural strength where it associated with the inner face of the INM. The major components of
is needed (see Fig. 1.9B,C) or to provide scaffolding for the attachment the nuclear lamina are lamins, the type V intermediate filament proteins
of other structures. Intermediate filaments form extensive cytoplasmic consisting of A-type and B-type classes.
networks extending from cage-like perinuclear arrangements to the cell The nuclear lamina reinforces the nuclear membrane mechanically,
surface. Intermediate filaments of different molecular classes are char- determines the shape of the nucleus and provides a binding site for a
acteristic of particular tissues or states of maturity and are therefore range of proteins that anchor chromatin to the cytoskeleton. Nuclear
important indicators of the origins of cells or degrees of differentiation, lamin A, with over 350 mutations, is the most mutated protein linked
as well as being of considerable value in histopathology. to human disease. These are referred to as laminopathies, characterized
Intermediate filament proteins have been classified into five distinct by nuclear structural abnormalities that cause structurally weakened
types on the basis of their primary structure and tissue-specific expres- nuclei, leading to mechanical damage. Lamin A mutations cause a | 50 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
15.e1
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A-type lamins include lamin A (interacting with emerin), lamin C,
lamin C2 and lamin AΔ10 encoded by a single gene (LMNA). Lamin A
and lamin C are the major A-type lamins expressed in somatic cells,
whereas lamin C2 is expressed in testis. B-type lamins include lamin
B1 and lamin B2 (expressed in somatic cells), and testis-specific lamin
B3. Lamin B1 is encoded by the LMNB1 gene; lamin B2 is encoded by
the LMNB2 gene. | 51 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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NOITCES
surprisingly wide range of diseases, from progeria to various dystro- permeable to small molecules, ions and proteins up to about 17 kDa.
phies, including an autosomal dominant form of EDMD. A truncated See Raices and D’Angelo (2012) for further reading on nuclear pore
farnesylated form of lamin A, referred to as progerin, leads to defects complex composition. Most proteins that enter the nucleus do so as
in cell proliferation and DNA damage of mesenchymal stem cells and complexes with specific transport receptor proteins known as import-
vascular smooth muscle cells. Affected patients display cardiovascular ins. Importins shuttle back and forth between the nucleus and cyto-
disease and die at an early age. Mice lacking lamin B1 and lamin B2 plasm. Binding of the cargo to the importin requires a short sequence
survive until birth; however, neuronal development is compromised of amino acids known as a nuclear localization sequence (NLS), and
when lamin B1 or lamin B2 is absent. Overexpression of lamin B1 is can either be direct or take place via an adapter protein. Interactions of
associated with autosomal dominant leukodystrophy characterized by the importin with components of the nuclear pore move it, together
gradual demyelination in the central nervous system. See Worman with its cargo, through the pore by an energy-independent process.
(2012) and Burke and Stewart (2013) for additional reading on lamins A complementary cycle functions in export of proteins and RNA mol-
and laminopathies. ecules from the nucleus to the cytoplasm using transport receptors
Condensed chromatin (heterochromatin) tends to aggregate near known as exportins.
the nuclear envelope during interphase. At the end of mitotic and A small GTPase called Ras-related nuclear protein (Ran) regulates the
meiotic prophase (see below), the lamin filaments disassemble by import and export of proteins across the nuclear envelope.
phosphorylation, causing the nuclear membranes to vesiculate and For further reading on the Ran pathway and exportins/importins, see
disperse into the endoplasmic reticulum. During the final stages of Clarke and Zhang (2008) and Raices and D’Angelo (2012).
mitosis (telophase), proteins of the nuclear periphery, including lamins,
Chromatin
associate with the surface of the chromosomes, providing docking sites
for membrane vesicles. Fusion of these vesicles reconstitutes the nuclear DNA is organized within the nucleus in a DNA–protein complex known
envelope, including the nuclear lamina, following lamin dephosphor- as chromatin. The protein constituents of chromatin are the histones
ylation. See Simon and Wilson (2011) for further reading on the and the non-histone proteins. Non-histone proteins are an extremely
nucleoskeleton. heterogeneous group that includes structural proteins, DNA and RNA
The transport of molecules between the nucleus and the cytoplasm polymerases, and gene regulatory proteins. Histones are the most abun-
occurs via specialized nuclear pore structures that perforate the nuclear dant group of proteins in chromatin, primarily responsible for the
membrane (Fig. 1.11A). They act as highly selective directional molecu- packaging of chromosomal DNA into its primary level of organization,
lar filters, permitting proteins such as histones and gene regulatory the nucleosome. There are four core histone proteins – H2A, H2B, H3
proteins (which are synthesized in the cytoplasm but function in the and H4 – which combine in equal ratios to form a compact octameric
nucleus) to enter the nucleus, and molecules that are synthesized in the nucleosome core. A fifth histone, H1, is involved in further compaction
nucleus but destined for the cytoplasm (e.g. ribosomal subunits, trans- of the chromatin. The DNA molecule (one per chromosome) winds
fer RNAs and messenger RNAs) to leave the nucleus. twice around each nucleosome core, taking up 165 nucleotide pairs.
Ultrastructurally, nuclear pores appear as disc-like structures with an This packaging organizes the DNA into a chromatin fibre 11 nm in
outer diameter of 130 nm and an inner pore with an effective diameter diameter, and imparts to this form of chromatin the electron micro-
for free diffusion of 9 nm (Fig. 1.11B). The nuclear envelope of an scopic appearance of beads on a string, in which each bead is separated
active cell contains up to 4000 such pores. The nuclear pore complex by a variable length of DNA, typically about 35 nucleotide pairs long.
has an octagonal symmetry and is formed by an assembly of more than The nucleosome core region and one of the linker regions constitute
50 proteins, the nucleoporins. The inner and outer nuclear membranes the nucleosome proper, which is typically about 200 nucleotide pairs
fuse around the pore complex (see Fig. 1.11A). Nuclear pores are freely in length. However, chromatin rarely exists in this simple form and is
usually packaged further into a 30 nm thick fibre, involving a single H1
histone per nucleosome, which interacts with both DNA and protein
to impose a higher order of nucleosome packing. Usually, 30 nm thick
N
fibres are further coiled or folded into larger domains. Individual
domains are believed to decondense and extend during active transcrip-
tion. In a typical interphase nucleus, euchromatin (nuclear regions that
appear pale in appropriately stained tissue sections, or relatively
electron-lucent in electron micrographs; see Fig. 1.2) is likely to consist
A mainly of 30 nm fibres and loops, and contains the transcriptionally
C
active genes. Transcriptionally active cells, such as most neurones, have
nuclei that are predominantly euchromatic. See Luger et al (2012) for
further reading on the nucleosome and chromatin structure.
Heterochromatin (nuclear regions that appear dark in appropriately
stained tissue sections or electron-dense in electron micrographs) is
characteristically located mainly around the periphery of the nucleus,
except over the nuclear pores (see Fig. 1.11A), and adjacent to the
nucleolus (see Fig. 1.2). It is a relatively compacted form of chromatin
in which the histone proteins carry a specific set of post-translational
modifications, including methylation at characteristic residues. This
facilitates the binding of specific heterochromatin-associated proteins.
Heterochromatin includes non-coding regions of DNA, such as centro-
meric regions, which are known as constitutive heterochromatin. DNA
becomes transcriptionally inactive in some cells as they differentiate
during development or cell maturation, and contributes to heterochro-
matin; it is known as facultative heterochromatin. The inactive X chro-
mosome in females is an example of facultative heterochromatin and
can be identified in the light microscope as the deeply staining Barr
B
body often located near the nuclear periphery or a drumstick extension
of a nuclear lobe of a mature multilobed neutrophil leukocyte.
Fig . 1 .11 A, The nuclear envelope with nuclear pores (arrows) in
In transcriptionally inactive cells, chromatin is predominantly in the
transverse section, showing the continuity between the inner and outer
condensed, heterochromatic state, and may comprise as much as 90%
phospholipid layers of the envelope on either side of the pore . The fine
of the total. Examples of such cells are mature neutrophil leukocytes
‘membrane’ appearing to span the pore is formed by proteins of the pore
(in which the condensed chromatin is present in a multilobular, densely
complex . Note that the chromatin is less condensed in the region of
staining nucleus) and the highly condensed nuclei of orthochromatic
nuclear pores . Abbreviations: N, nucleus; C, cytoplasm . B, Nuclear pores
erythroblasts (late-stage erythrocyte precursors). In most mature cells,
seen ‘en face’ as spherical structures (arrows) in a tangential section
through the nuclear envelope . The appearance of the envelope varies in a mixture of the two occurs, indicating that only a proportion of the
electron density as the plane of section passes through different regions DNA is being transcribed. A particular instance of this is seen in the B
of the curved double membrane, which is interrupted at intervals by pores lymphocyte-derived plasma cell, in which much of the chromatin is in
through the envelope (see also Fig . 1 .1) . The surrounding cytoplasm with the condensed condition and is arranged in regular masses around the
ribosomes is less electron-dense . Human tissues . (Courtesy of Dr Bart perimeter of the nucleus, producing the so-called ‘clock-face’ nucleus
Wagner, Histopathology Department, Sheffield Teaching Hospitals, UK .) (see Figs 4.6, 4.12). Although this cell is actively transcribing, much of | 52 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell structure
17
1
RETPaHC
its protein synthesis is of a single immunoglobulin type, and conse- easily seen during metaphase, although prophase chromosomes can be
quently much of its genome is in an inactive state. used for more detailed analyses.
During mitosis, the chromatin is further reorganized and condensed Lymphocytes separated from blood samples, or cells taken from
to form the much-shortened chromosomes characteristic of metaphase. other tissues, are used as a source of chromosomes. Diagnosis of fetal
This shortening is achieved through further levels of close packing of chromosome patterns is generally carried out on samples of amniotic
the chromatin. The condensed chromosomes are stabilized by protein fluid containing fetal cells aspirated from the uterus by amniocentesis,
complexes known as condensins. Progressive folding of the chromo- or on a small piece of chorionic villus tissue removed from the placenta.
somal DNA by interactions with specific proteins can reduce 5 cm of Whatever their origin, the cells are cultured in vitro and stimulated to
chromosomal DNA by 10,000-fold, to a length of 5 µm in the mitotic divide by treatment with agents that stimulate cell division. Mitosis is
chromosome. interrupted at metaphase with spindle inhibitors. The chromosomes are
dispersed by first causing the cells to swell in a hypotonic solution, then
Chromosomes and telomeres
the cells are gently fixed and mechanically ruptured on a slide to spread
The nuclear DNA of eukaryotic cells is organized into linear units called the chromosomes. They are subsequently stained in various ways to
chromosomes. The DNA in a normal human diploid cell contains allow the identification of individual chromosomes by size, shape and
6 × 109 nucleotide pairs organized in the form of 46 chromosomes (44 distribution of stain (Fig. 1.12). General techniques show the obvious
autosomes and 2 sex chromosomes). The largest human chromosome landmarks, e.g. lengths of arms and positions of constrictions. Banding
(number 1) contains 2.5 × 108 nucleotide pairs, and the smallest (the Y techniques demonstrate differential staining patterns, characteristic for
chromosome) 5 × 107 nucleotide pairs. each chromosome type. Fluorescence staining with quinacrine mustard
Each chromosomal DNA molecule contains a number of specialized and related compounds produces Q bands, and Giemsa staining (after
nucleotide sequences that are associated with its maintenance. One is treatment that partially denatures the chromatin) gives G bands (Fig.
the centromeric DNA region. During mitosis, a disc-shaped structure 1.12A). Other less widely used methods include: reverse Giemsa stain-
composed of a complex array of proteins, the kinetochore, forms as a ing, in which the light and dark areas are reversed (R bands); the stain-
substructure at the centromeric region of DNA to which kinetochore ing of constitutive heterochromatin with silver salts (C-banding); and
microtubules of the spindle attach. Another region, the telomere, T-banding to stain the ends (telomeres) of chromosomes. Collectively,
defines the end of each chromosomal DNA molecule. Telomeres consist these methods permit the classification of chromosomes into num-
of hundreds of repeats of the nucleotide sequence (TTAGGG) n. The very bered autosomal pairs in order of decreasing size, from 1 to 22, plus
ends of the chromosomes cannot be replicated by the same DNA the sex chromosomes.
polymerase as the rest of the chromosome, and are maintained by a A summary of the major classes of chromosome is given in
specific enzyme called telomerase, which contains an RNA subunit Table 1.1.
acting as the template for lengthening the TTAGGG repeats. See Methodological advances in banding techniques improved the re-
Nandakumar and Cech (2013) for further reading on the recruitment cognition of abnormal chromosome patterns. The use of in situ hybridi-
of telomerase to telomeres. Thus telomerase is a specialized type of zation with fluorescent DNA probes specific for each chromosome (Fig.
polymerase known as a reverse transcriptase that turns sequences in 1.12B) permits the identification of even very small abnormalities.
RNA back into DNA. The number of tandem repeats of the telomeric
Nucleolus
DNA sequence varies. The telomere appears to shorten with successive
cell divisions because telomerase activity reduces or is absent in dif- Nucleoli are a prominent feature of an interphase nucleus (see Fig. 1.2).
ferentiated cells with a finite lifespan. In mammals, telomerase is active They are the site of most of the synthesis of ribosomal RNA (rRNA) and
in the germ-cell lineage and in stem cells, but its expression in somatic assembly of ribosome subunits. Nucleoli organize at the end of mitosis
cells may lead to or prompt cancer. A lack of telomere maintenance
determines the shrinking of telomeres in proliferating cells to the point
when cells stop dividing, a condition known as replicative senescence. Table 1.1 Summary of the major classes of chromosome
See Sahin and DePinho (2012) for further reading on telomeres and
Group Features
progressive DNA damage.
The role of the telomere in ageing and cell senescence is further 1–3 (A) Large metacentric chromosomes
discussed at the end of this chapter. 4–5 (B) Large submetacentric chromosomes
6–12 + X (C) Metacentrics of medium size
Karyotypes: classification of human chromosomes
13–15 (D) Medium-sized acrocentrics with satellites
A number of genetic abnormalities can be directly related to the chro- 16–18 (E) Shorter metacentrics (16) or submetacentrics (17,18)
mosomal pattern. The characterization or karyotyping of chromosome
19–20 (F) Shortest metacentrics
number and structure is therefore of considerable diagnostic impor-
21–22 + Y (G) Short acrocentrics; 21, 22 with satellites, Y without
tance. The identifying features of individual chromosomes are most
1 2 3 4 5
1 2 3 4 5
6 7 8 9 10 11 12 6 7 8 9 10 11 12
13 14 15 16 17 18 13 14 15 16 17 18
A 19 20 21 22 X Y B 19 20 21 22 X Y
Fig . 1 .12 Chromosomes from normal males, arranged as karyotypes . A, G-banded preparation . B, Preparation stained by multiplex fluorescence in situ
hybridization to identify each chromosome . (Courtesy of Dr Denise Sheer, Cancer Research UK .) | 53 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
17.e1
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Telomerase has been associated with ageing and cell senescence
because a gradual loss of telomeres may lead to tissue atrophy, stem
cell depletion and deficient tissue repair or regeneration. Mutations
causing loss of function of telomerase or the RNA-containing template
have been associated with dyskeratosis congenita (characterized by
abnormal skin pigmentation, nail dystrophy and mucosal leukoplasia),
aplastic anaemia and pulmonary fibrosis. | 54 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
18
1
NOITCES
and consist of repeated clusters of ribosomal DNA (rDNA) genes and Cdk1
processing molecules responsible for producing ribosome subunits. The
initial step of the assembly of a ribosome subunit starts with the tran- G2 Cyclin A
scription of rDNA genes by RNA polymerase I. The rDNA genes,
arranged in tandem repeats called nucleolar organizing regions (NORs), Cdk1
are located on acrocentric chromosomes. There are five pairs of acro- Mitosis
centric chromosomes in humans. The initial 47S rRNA precursor tran- Cyclin B
script is cleaved to form the mature 28S, 18S and 5.8S rRNAs, assembled
Checkpoint 2
with the 5S rRNA (synthesized by RNA polymerase III outside the
nucleolus) and coupled to small nucleolar ribonucleoproteins and
other non-ribosomal proteins to form 60S (containing 28S rRNA, 5.8S
rRNA and 5S rRNA) and 40S (containing 18S rRNA) preribosome sub-
units. These are then exported to the cytoplasm across nuclear pores as S
mature ribosome subunits. About 726 human nucleolar proteins have
Checkpoint 1 Cyclin D
been identified by protein purification and mass spectrometry. For
further reading on nucleolar functions, see Boisvert et al (2007).
Cdk2 Cdk4
Ribosomal biogenesis occurs in distinct subregions of the nucleolus, G1
visualized by electron microscopy. The three nucleolar subregions are Cyclin A
fibrillar centres (FCs), dense fibrillar components (DFCs) and granular
components (GCs). Transcription of the rDNA repeats takes place at
the FC-DFC boundary; pools of RNA polymerase I reside in the FC
Cyclin E
region; processing of transcripts and coupling to small nucleolar ribo-
nucleoproteins take place in DFC; and the assembly of ribosome sub- Cdk2
units is completed in the GC region. Fig . 1 .13 The cell cycle consists of an interphase (G phase, S phase and
1
The nucleolus is disassembled when cells enter mitosis and tran- G phase) followed by mitosis . The cyclin D/Cdk4 complex assembles at
2
scription becomes inactive. It reforms after nuclear envelope reorganiza- the beginning of G; the cyclin E/Cdk2 complex assembles near the end
1
tion in telophase, in a process associated with the onset of transcription of G as the cell is preparing to cross checkpoint 1 to start DNA synthesis
1
in nucleolar organizing centres on each specific chromosome, and (during S phase) . The cyclin A/Cdk2 complex assembles as DNA
becomes functional during the G phase of the cell cycle. An adequate synthesis starts . Completion of G is indicated by the assembled cyclin A/
1 2
pool of ribosome subunits during cell growth and cell division requires Cdk1 complex . A cell crosses checkpoint 2 to initiate mitosis when the
steady nucleolar activity to support protein synthesis. Several DNA cyclin B/Cdk1 complex assembles . The cyclin B/Cdk1 complex is
helicases, a conserved group of enzymes that unwind DNA, accumulate degraded by the 26S proteasome and an assembled cyclin D/Cdk4 marks
in the nucleolus under specific conditions such as Bloom’s syndrome the start of the G 1 phase of a new cell cycle . For details, see text .
(an autosomal recessive disorder characterized by growth deficiency, (Modified with permission from Kierszenbaum AL, Tres LL . Histology and
Cell Biology: An Introduction to Pathology . 3rd ed, Philadelphia: Elsevier,
immunodeficiency and a predisposition to cancer) and Werner’s syn-
Saunders; 2011 .)
drome (an autosomal recessive condition characterized by the early
appearance of various age-related diseases).
certain tumour suppressor genes (e.g. the gene mutated in retinoblas-
toma, Rb) block the cycle in G. DNA synthesis (replication of the
CELL DIVISION AND THE CELL CYCLE 1
genome) occurs during S phase, at the end of which the DNA content
of the cell has doubled. During G, the cell prepares for division; this
2
During prenatal development, most cells undergo repeated division period ends with the onset of chromosome condensation and break-
(see Video 1.1) as the body grows in size and complexity. As cells down of the nuclear envelope. The times taken for S, G and M are
2
mature, they differentiate structurally and functionally. Some cells, such similar for most cell types, and occupy 6–8, 2–4 and 1–2 hours respec-
as neurones, lose the ability to divide. Others may persist throughout tively. In contrast, the duration of G shows considerable variation,
1
the lifetime of the individual as replication-competent stem cells, e.g. sometimes ranging from less than 2 hours in rapidly dividing cells to
cells in the haemopoietic tissue of bone marrow. Many stem cells divide more than 100 hours, within the same tissue.
infrequently, but give rise to daughter cells that undergo repeated cycles The passage of a cell through the cell cycle is controlled by proteins
of mitotic division as transit (or transient) amplifying cells. Their divi- in the cytoplasm: cyclins and cyclin-dependent kinases (Cdks; Fig
sions may occur in rapid succession, as in cell lineages with a short 1.13). Cyclins include G cyclins (D cyclins), S-phase cyclins (cyclins E
1
lifespan and similarly fast turnover and replacement time. Transit and A) and mitotic cyclins (B cyclins). Cdks, protein kinases, which are
amplifying cells are all destined to differentiate and ultimately to die activated by binding of a cyclin subunit, include G Cdk (Cdk4), an
1
and be replaced, unlike the population of parental stem cells, which S-phase Cdk (Cdk2) and an M-phase Cdk (Cdk1). Cell cycle progres-
self-renews. sion is driven in part by changes in the activity of Cdks. Each cell cycle
Patterns and rates of cell division within tissues vary considerably. stage is characterized by the activity of one or more Cdk–cyclin pairs.
In many epithelia, such as the crypts between intestinal villi, the replace- Transitions between cell cycle stages are triggered by highly specific
ment of damaged or ageing cells by division of stem cells can be rapid. proteolysis by the 26S proteasome of the cyclins and other key
Rates of cell division may also vary according to demand, as occurs in components.
the healing of wounded skin, in which cell proliferation increases to a To give one example, the transition from G to mitosis is driven by
2
peak and then returns to the normal replacement level. The rate of cell activation of Cdk1 by its partners, the A- and B-type cyclins; the char-
division is tightly coupled to the demand for growth and replacement. acteristic changes in cellular structure that occur as cells enter mitosis
Where this coupling is faulty, tissues either fail to grow or replace their are largely driven by phosphorylation of proteins by active Cdk1-cyclin
cells, or they can overgrow, producing neoplasms. A and Cdk1-cyclin B. Cells exit from mitosis when an E3 ubiquitin
The cell cycle is an ordered sequence of events, culminating in cell ligase, the anaphase promoting complex, also called cyclosome
growth and division to produce two daughter cells. It generally lasts a (APC/C), marks the cyclins for destruction. In addition, APC/C prompts
minimum of 12 hours, but in most adult tissues can be considerably the degradation of the mitotic cyclin B and the destruction of cohesins,
longer, and is divided into four distinct phases, which are known as G thus allowing sister chromatids to separate.
1
(for gap 1), S (for DNA synthesis), G (for gap 2) and M (for mitosis). There are important checkpoints in the cell cycle (see Fig. 1.13).
2
The combination of G, S and G phases is known as interphase. M is Checkpoint 1 requires G cyclins to bind to their corresponding Cdks
1 2 1
the mitotic phase, which is further divided into four phases (see below). to signal the cell to prepare for DNA synthesis. S-phase promoting
G is the period when cells respond to growth factors directing the cell factor (SPF; cyclin A bound to Cdk2) enters the nucleus to stimulate
1
to initiate another cycle; once made, this decision is irreversible. It is DNA synthesis. Checkpoint 2 requires M-phase promoting factor
also the phase in which most of the molecular machinery required to (mitotic cyclin B bound to M-phase Cdk1) to trigger the assembly of
complete another cell cycle is generated. Centrosomes duplicate during the mitotic spindle, breakdown of the nuclear envelope, arrest of gene
S phase in preparation for mitosis. Cells that retain the capacity for transcription and condensation of chromosomes. During metaphase of
proliferation, but which are no longer dividing, have entered a phase mitosis, M-phase promoting factor activates APC/C, which determines
called G and are described as quiescent even though they may be quite the breakdown of cohesins, the protein complex holding sister chroma-
0
active physiologically. Growth factors can stimulate quiescent cells to tids together. Then, at anaphase, separated chromatids move to the
leave G and re-enter the cell cycle, whereas the proteins encoded by opposite poles of the spindle. Finally, B cyclins are destroyed following
0 | 55 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
18.e1
1
RETPaHC
The targets for proteolysis are marked for destruction by E3 ubiquitin
ligases, which decorate them with polymers of the small protein ubiq-
uitin, a sign for recognition by the 26S proteasome. | 56 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell division and the cell cycle
19
1
RETPaHC
their attachment to ubiquitin, targeting them for destruction by the 26S Prophase
proteasome. As G starts, cyclins D, bound to Cdk4, start preparation
1 Nuclear
for a new cell cycle. membrane Centriole centre
Quality control checkpoint 2 operates to delay cell-cycle progression of aster (or spindle pole)
Centromere
when DNA has been damaged by radiation or chemical mutagens. Cells
with checkpoint defects, such as loss of the protein p53, which is a Microtubules
Two sister of spindle
major negative control element in the division cycle of all cells, are
chromatids
commonly associated with the development of malignancy. An example attached at
is Li Fraumeni syndrome, where a defective p53 gene leads to a high centromere
frequency of cancer in affected individuals. In cells, p53 protein binds
DNA and stimulates another gene to produce p21 protein, which inter-
acts with Cdk2 to prevent S-phase promoting activity. When mutant
p53 can no longer bind DNA to stimulate production of p21 to stop Prometaphase
DNA synthesis, cells acquire oncogenic properties. The p53 gene is an
example of a tumour suppressor gene. For further reading on p53 muta- Spindle pole
tions and cancer, see Muller and Vousden (2013).
Nuclear
Mitosis and meiosis membrane Microtubule
vesicles
Mitosis is the process that results in the distribution of identical copies
of the parent cell genome to the two daughter somatic cells. In meiosis,
the divisions immediately before the final production of gametes halve
the number of chromosomes to the haploid number, so that at fertiliza- Metaphase
tion the diploid number is restored. Moreover, meiosis includes a phase Cell equator
in which exchange of genetic material occurs between homologous
chromosomes. This allows a rearrangement of genes to take place,
which means that the daughter cells differ from the parental cell in both
their precise genetic sequence and their haploid state. Mitosis and
meiosis are alike in many respects, and differ principally in chromo-
somal behaviour during the early stages of cell division. In meiosis, two
divisions occur in succession, without an intervening S phase. Meiosis
I is distinct from mitosis, whereas meiosis II is more like mitosis.
Mitosis
New DNA is synthesized during the S phase of the cell cycle interphase. Anaphase
This means that the amount of DNA in diploid cells has doubled to
the tetraploid value by the onset of mitosis, although the chromosome
number is still diploid. During mitosis, this amount is halved between
the two daughter cells, so that DNA quantity and chromosome number Chromatids pulled
are diploid in both cells. The cellular changes that achieve this distribu- toward pole of spindle
as their microtubules
tion are conventionally divided into four phases called prophase, meta- shorten
phase, anaphase and telophase (Figs 1.14–1.15, Video 1.1).
Prophase
During prophase, the strands of chromatin, which are highly extended
during interphase, shorten, thicken and resolve themselves into recog-
nizable chromosomes. Each chromosome is made up of duplicate chro- Telophase
matids (the products of DNA replication) joined at their centromeres. Chromosomes decondense and
Outside the nucleus, the two centriole pairs begin to separate, and move detach from microtubules
towards opposite poles of the cell. Parallel microtubules are assembled
between them to create the mitotic spindle, and others radiate to form
the microtubule asters, which come to form the spindle poles or mitotic
centre. As prophase proceeds, the nucleoli disappear, and the nuclear
envelope suddenly disintegrates to release the chromosomes, an event
that marks the end of prophase. Nuclear membrane
reforms
Prometaphase–metaphase
As the nuclear envelope disappears, the spindle microtubules extend
into the central region of the cell, attaching to the chromosomes, which Cytokinesis
subsequently move towards the equator of the spindle (prometaphase).
The spindle consists of kinetochore microtubules attached to the kine-
tochore, a multiprotein structure assembled at the centromeric DNA
region, and polar microtubules, which are not attached to chromo- Centriole
somes but instead overlap with each other at the centre of the cell. The
grouping of chromosomes at the spindle equator is called the meta-
phase or equatorial plate. The chromosomes, attached at their centro-
Nuclear
meres, appear to be arranged in a ring when viewed from either pole membrane
of the cell, or to lie linearly across this plane when viewed from above.
Cytoplasmic movements during late metaphase effect the approxi-
mately equal distribution of mitochondria and other cell structures Actin–myosin belt
around the cell periphery.
Fig . 1 .14 The stages in mitosis, including the appearance and distribution
of the chromosomes .
anaphase
By the end of metaphase every chromosome consists of a pair of sister
chromatids attached to opposing spindle poles by bundles of microtu- microtubule-dependent pulling forces. Proteolytic cleavage releases the
bules associated with the kinetochore. The onset of anaphase begins cohesion between sister chromatids, which then move towards opposite
with the proteolytic cleavage by the enzyme separase of a key subunit spindle poles while the microtubule bundles attached to the kineto-
of protein complexes known as cohesins. The latter hold the replicated chores shorten and move polewards. At the end of anaphase the sister
sister chromatids together to resist separation even when exposed to chromatids are grouped at either end of the cell, and both clusters are | 57 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
20
1
NOITCES
Fig . 1 .15 diploid in number. An infolding of the cell equator begins, deepening
Immunofluorescence during telophase as the cleavage furrow.
images of stages in
mitosis in human Telophase
carcinoma cells in During telophase the nuclear envelopes reform, beginning with the
culture . A, Metaphase, association of membranous vesicles with the surface of the chromo-
with spindle somes. Later, after the vesicles have fused and the nuclear envelope is
microtubules (green), complete, the chromosomes decondense and the nucleoli reform. At
the microtubule-
the same time, cytoplasmic division, which usually begins in early
stabilizing protein
A anaphase, continues until the new cells separate, each with its derived
(HURP; red) and
nucleus. The spindle remnant now disintegrates. While the cleavage
chromosomal DNA
furrow is active, a peripheral band or belt of actin and myosin appears
(blue) . B, Anaphase,
in the constricting zone; contraction of this band is responsible for
with spindle
furrow formation.
microtubules (green),
the central spindle Failure of disjunction of chromatids, so that sister chromatids pass
(Aurora-B kinase, red) to the same pole, may sometimes occur. Of the two new cells, one will
and segregated have more, and the other fewer, chromosomes than the diploid number.
chromosomes (blue) . Exposure to ionizing radiation promotes non-disjunction and may, by
C, Late anaphase, with chromosomal damage, inhibit mitosis altogether. A typical symptom of
spindle microtubules radiation exposure is the failure of rapidly dividing epithelia to replace
B (green), the central lost cells, with consequent ulceration of the skin and mucous mem-
spindle (Plk1 kinase, branes. Mitosis can also be disrupted by chemical agents, particularly
red, appearing yellow vinblastine, paclitaxel (taxol) and their derivatives. These compounds
where co-localized with either disassemble spindle microtubules or interfere with their dynam-
microtubule protein) ics, so that mitosis is arrested in metaphase.
and segregated
chromosomes (blue) . Meiosis
(Courtesy of Dr Herman
There are two consecutive cell divisions during meiosis: meiosis I and
Silljé, Max-Planck-
meiosis II (Fig. 1.16). Details of this process differ at a cellular level for
Institut für Biochemie,
male and female lineages.
Martinsried, Germany .)
C
A Events preceding meiosis
Centromere Paired sister
centromeres
Premeiotic Meiotic
S phase prophase
B Meiotic prophase
A a A
b a
B paP ta ei rr nin ag l ao nf d B b Meiosis I
maternal
homologues
Leptotene Zygotene Pachytene Diplotene Diakinesis
C Meiosis I
A
A B Chiasmata A B B
b
a b a b Meiosis I a Meiosis II
Interphase
Metaphase I Anaphase I (no S phase)
D Meiosis II
A
B
a
b
Prophase II Metaphase II Anaphase II Haploid gametes
Fig . 1 .16 The stages in meiosis, depicted by two pairs of maternal and paternal homologues (dark and pale colours) . DNA and chromosome
complement changes and exchange of genetic information between homologues are indicated . | 58 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell polarity and domains
21
1
RETPaHC
meiosis I equatorial plane of the spindle. The centromeres of each pair of sister
Prophase I chromatids function as a single unit, facing a single spindle pole.
Meiotic prophase I is a long and complex phase that differs consider- Homologous chromosomes are pulled towards opposite spindle poles,
ably from mitotic prophase and is customarily divided into five sub- but are held paired at the spindle midzone by chiasmata. Errors in
stages, called leptotene, zygotene, pachytene, diplotene and diakinesis. chromosome segregation (known as non-disjunction) lead to the pro-
There are three distinctive features of male meiotic prophase that are duction of aneuploid progeny. Most human aneuploid embryos are
not seen during mitotic prophase: the pairing, or synapse, of homolo- non-viable and this is the major cause of fetal loss (spontaneous abor-
gous chromosomes of paternal and maternal origin to form bivalent tion), particularly during the first trimester of pregnancy in humans.
structures; the organization of nucleoli by autosomal bivalents; and The most common form of viable aneuploid progeny in humans is
significant non-ribosomal RNA synthesis by autosomal bivalents (in Down’s syndrome (trisomy for chromosome 21), which exhibits a dra-
contrast to the transcriptional inactivity of the XY chromosomal pair) matic increase with maternal age.
(see Tres 2005). In the female, meiotic prophase I starts during fetal
Anaphase and telophase I
gonadogenesis, is arrested at the diplotene stage and resumes at puberty.
In the male, meiosis starts at puberty. Anaphase I of meiosis begins with the release of cohesion between the
arms of sister chromatids, much as it does during mitosis. As position-
Leptotene stage During leptotene, homologous chromosomes ing of bivalent pairs is random, assortment of maternal and paternal
(maternal and paternal copies of the same chromosome), replicated in chromosomes in each telophase nucleus is also random. Critically,
a preceding S phase and each consisting of sister chromatids joined at sister centromeres, and thus chromatids, do not separate during ana-
the centromere (see above), locate one another within the nucleus, and phase I.
the process of genetic recombination is initiated. Cytologically, chro- During meiosis I, cytoplasmic division occurs by specialized mecha-
mosomes begin to condense, appearing as individual threads that are nisms. In females, the division is highly asymmetric, producing one egg
attached via their telomeres to the nuclear envelope. They often show and one tiny cell known as a polar body. In males, the process results
characteristic beading throughout their length. in production of spermatocytes that remain joined by small cytoplas-
mic bridges.
Zygotene stage During zygotene, the homologous chromosomes
meiosis II
initiate pairing or synapsis, during which they become intimately asso-
ciated with one another. Synapsis may begin near the telomeres at the Meiosis II commences after only a short interval during which no DNA
inner surface of the nuclear membrane, and during this stage the tel- synthesis occurs. The centromeres of sister chromatids remain paired,
omeres often cluster to one side of the nucleus (a stage known as the but rotate so that each one can face an opposite spindle pole. Onset of
bouquet because the chromosomes resemble a bouquet of flowers). The anaphase II is triggered by loss of cohesion between the centromeres,
pairs of synapsed homologues, also known as bivalents, are linked as it is in mitosis. This second division is more like mitosis, in that
together by a tripartite ribbon, the synaptonemal complex, which con- chromatids separate during anaphase, but, unlike mitosis, the separat-
sists of two lateral dense elements and a central, less dense, linear ing chromatids are genetically different (the result of genetic recombi-
element. nation). Cytoplasmic division also occurs and thus, in the male, four
The sex chromosomes also start to synapse during zygotene. In haploid cells, interconnected by cytoplasmic bridges, result from
males, with distinct X and Y chromosomes, synapsis involves a region meiosis I and II.
of shared DNA sequence known as the pseudoautosomal region. The
XY bivalent adopts a special condensed structure, known as the sex
CELL POLARITY AND DOMAINS
vesicle, which becomes associated later at pachytene with migratory
nucleolar masses originating in the autosomal bivalents.
Chromosome behaviour in meiosis is intimately linked with the Epithelia are organized into sheets or glandular structures with very
process of genetic recombination. This begins during leptotene, as different environments on either side. These cells actively transfer mac-
homologous chromosomes first locate one another at a distance. Syn- romolecules and ions between the two surfaces and are thus polarized
apsis, stabilized by the synaptonemal complex, facilitates recombina- in structure and function. In polarized cells, particularly in epithelia,
tion, as sites of genetic exchange are turned into specialized structures the cell is generally subdivided into domains that reflect the polariza-
known as chiasmata, which are topological crossing-over points that tion of activities within it. The free surface, e.g. that facing the intestinal
hold homologous chromosomes together. lumen or airway, is the apical surface, and its adjacent cytoplasm is the
apical cell domain. This is where the cell interfaces with a specific body
Pachytene stage When synapsis is complete for all chromosomes, compartment (or, in the case of the epidermis, with the outside world).
the cell is said to be in pachytene. Each bivalent looks like a single thick The apical surface is specialized to act as a barrier, restricting access of
structure, but is actually two pairs of sister chromatids held together by substances from this compartment to the rest of the body. Specific
the synaptonemal complex. Genetic recombination between non-sister components are selectively absorbed from, or added to, the external
chromatids is completed at this point, with sites where it has occurred compartment by the active processes, respectively, of active transport
(usually one per chromosome arm) appearing as recombination and endocytosis inwardly or exocytosis and secretion outwardly.
nodules in the centre of the synaptonemal complex. The apical surface is often covered with small protrusions of the cell
surface, microvilli, which increase the surface area, particularly for
Diplotene stage During diplotene, the synaptonemal complex disas- absorption.
sembles and pairs of homologous chromosomes, now much shortened, The surface of the cell opposite to the apical surface is the basal
separate, except where crossing over has occurred (chiasmata). This surface, with its associated basolateral cell domain. In a single-layered
process is called disjunction. At least one chiasma forms between each epithelium, this surface faces the basal lamina. The remaining surfaces
homologous pair, exchanging maternal and paternal sequences; up to are known as the lateral cell surfaces. In many instances, the lateral and
five have been observed. In the ovaries, primary oocytes become diplo- basal surfaces perform similar functions and the cellular domain is
tene by the fifth month in utero and each remains at this stage until the termed the basolateral domain. Cells actively transport substances, such
period before ovulation (up to 50 years). as digested nutrients from the intestinal lumen or endocrine secretions,
across their basal (or basolateral) surfaces into the subjacent connective
Diakinesis Diakinesis is the prometaphase of the first meiotic divi- tissue matrix and the blood capillaries within it. Dissolved non-polar
sion. The chromosomes, still as bivalents, become even shorter and gases (oxygen and carbon dioxide) diffuse freely between the cell and
thicker. They gradually attach to the spindle and become aligned at a the blood stream across the basolateral surface. Apical and basolateral
metaphase plate. In eggs, the spindle forms without centrosomes. surfaces are separated by a tight intercellular seal, the tight junction
Microtubules first nucleate and are stabilized near the chromosomes; (occluding junction, zonula adherens), which prevents the passage of
the action of various motor molecules eventually sorts them into a even small ions through the space between adjacent cells and thus
bipolar spindle. Perhaps surprisingly, this spindle is as efficient a maintains the difference between environments on either side of the
machine for chromosome segregation as the spindle of mitotic cells epithelium.
with centrosomes at the poles.
Metaphase I Cell surface apical differentiations
Metaphase I resembles mitotic metaphase, except that the bodies attach-
ing to the spindle microtubules are bivalents, not single chromosomes. The surfaces of many different types of cell are specialized to form
These become arranged so that the homologous pairs occupy the structures that project from the surface. These projections may permit | 59 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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1
NOITCES
movement of the cell itself (flagella), or of fluids across the apical cell its distal region, called the transition zone. The continued elongation
surface (cilia), or increase the surface area available for absorption of the cilium requires the import and intraciliary transport of tubulin
(microvilli). Infoldings of the basolateral plasma membrane also dimers to the distal tip by bidirectional motor-driven proteins of the
increase the area for transport across this surface of the cell. In most intraflagellar transport complex.
non-dividing epithelial cells, the centriole-derived basal body gives rise The constant length of cilia is maintained by a steady-state balance
to a non-motile primary cilium, which has an important mechanosen- between tubulin turnover and addition of new tubulin dimers at the
sory role. ciliary tip.
Several filamentous structures are associated with the 9 + 2 doublet
Cilia and flagella microtubule of the axoneme in the cilium or flagellum shaft, e.g. radial
Cilia and flagella are motile, hair-like projections of the cell surface, spokes extend inwards from the outer doublet microtubules towards
which create currents in the surrounding fluid or movements of the cell the central pair, surrounded by an inner sheath (see Fig. 1.17). The outer
to which they are attached, or both. There are two categories of cilia: doublet microtubules bear two rows of tangential dynein arms attached
single non-motile primary cilia and multiple motile cilia. Primary cilia to the complete A subfibre of the doublet (consisting of 13 protofila-
are immotile but can detect physical and biochemical signals. Motile ments), which point towards the incomplete B subfibre of the adjacent
cilia are present in large numbers on the apical epithelial domain of doublet (consisting of 10–11 protofilaments). Adjacent doublets are
the upper respiratory tract and oviducts, and beat in a wave-like motion also linked by thin nexin filaments. Tektins are scaffolding filamentous
to generate fluid movement. Cilia also occur, in modified form, at the proteins extending along the axonemal microtubules.
dendritic endings of olfactory receptor cells, vestibular hair cells (kino- In motile cilia, arrays of dynein arms with ATPase activity cause outer
cilium), and the photoreceptor rods and cones of the retina. Flagella, microtubule doublets to move past one another, resulting in a large-
with a primary function in cell locomotion, are found on single-cell scale bending motion. Microtubules do not change in length. Move-
eukaryotes and in spermatozoa, which each possess a single flagellum ments of cilia and flagella are broadly similar. In addition to the
70 µm long. axoneme, spermatozoan flagella have outer dense fibres and a fibrous
A cilium or flagellum consists of a shaft (0.25 µm diameter) consti- sheath surrounding the axoneme. Flagella move by rapid undulation,
tuting most of its length, a tapering tip and a basal body at its base, which passes from the attached to the free end. In human spermatozoa,
which lies within the surface cytoplasm of the cell (Fig. 1.17). Other there is an additional helical component to this motion. In cilia, the
than at its base, the entire structure of the cilium is covered by plasma beating is planar but asymmetric. In the effective stroke, the cilium
membrane. The core of the cilium is the axoneme, a cylinder of nine remains stiff except at the base, where it bends to produce an oar-like
microtubule doublets that surrounds a central pair of single microtu- stroke. The recovery stroke follows, during which the bend passes from
bules (see Fig. 1.17). Ciliogenesis of primary cilia and motile cilia base to tip, returning the cilium to its initial position for the next cycle.
involves distinct steps. A centriole-derived basal body migrates to the The activity of groups of cilia is usually coordinated so that the bending
apical cell domain and axonemal microtubule doublets emerge from of one is rapidly followed by the bending of the next and so on,
Dynein ‘arms’
Inner sheath
Central
microtubules
Rootlet
Fig . 1 .17 A, The structure of a cilium shown in longitudinal (left) and transverse (right) section . A and B are subfibres of the peripheral microtubule
doublets (see text); the basal body is structurally similar to a centriole, but with microtubule triplets . B, The apical region of respiratory epithelial cells,
showing the proximal parts of three cilia sectioned longitudinally, anchored into the cytoplasm by basal bodies (BB) . Other cilia project out of the plane
of section and are cut transversely, showing the ‘9 + 2’ arrangement of microtubules . (B, With permission from Young B, Heath JW . Wheater’s Functional
Histology . 4th ed . Edinburgh: Elsevier, Churchill Livingstone; 2000 .)
A B
B Nexin-linking
protein
A
Tubulin subunits
Radial spoke
Microtubule
doublets
Plasma membrane
Basal body
Microtubule
triplets
BB
BB | 60 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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As indicated on page 15, the IFT-B protein complex participates in
intraciliary/intraflagellar anterograde transport of cargoes, a step essen-
tial for the assembly and maintenance of cilia and flagella; the IFT-A
protein complex is required for retrograde transport of cargoes to the
cell body for turnover. The movement of IFT proteins along microtu-
bules is catalysed by kinesin-2 (towards the ciliary tip; anterograde
direction) and cytoplasmic dynein-2 motor proteins (towards the cell
body; retrograde direction). A cargo includes axonemal components,
ciliary/flagellar membrane proteins (including the BBSome) and ciliary
signal transduction proteins. | 61 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Cell polarity and domains
23
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RETPaHC
resulting in long travelling waves of metachronal synchrony. These pass a very thick cell coat or glycocalyx, which reflects the presence of integral
over the tissue surface in the same direction as the effective stroke. membrane glycoproteins, including enzymes concerned with digestion
Ciliary motion is important in clearing mucus from airways, moving and absorption. Irregular microvilli, filopodia, are also found on the
eggs along oviducts, and circulating cerebrospinal fluid in brain ventri- surfaces of many types of cell, particularly free macrophages and fibro-
cles. In the node of the developing embryo, cilium-driven flow is essen- blasts, where they may be associated with phagocytosis and cell motil-
tial for determining left–right visceral asymmetry (developing ity. For further reading on the cytoskeleton of microvilli, see Brown and
patterning). Cilia also have a sensory function, determined by the pres- McKnight (2010).
ence of receptor and channel proteins on the ciliary membrane. Primary Long and branching microvilli are called stereocilia, an early misno-
cilia in the collecting ducts of the uriniferous tubule sense the flow of mer, as they are not motile and lack microtubules. An appropriate name
urine and also modulate duct morphogenesis. Cilia are essential for is stereovilli. They are found on cochlear and vestibular receptor cells,
signalling through the hedgehog pathway, a mechanism involved in where they act as sensory transducers, and also in the absorptive epi-
organizing the body plan, organogenesis and tumorigenesis in verte- thelium of the epididymis.
brates. For additional reading on hedgehog signalling and primary cilia,
see Briscoe and Thérond (2013). Intercellular junctions
There is a group of genetic diseases in which cilia beat either inef-
fectively or not at all, e.g. Kartagener’s immotile cilia syndrome. Affected The basolateral region of the plasma membrane of epithelial cells estab-
cilia exhibit deficient function or a lack of dynein arms. Males are typi- lishes junctions with adjacent cells and with structural components of
cally sterile because of the loss of spermatozoan motility, and half have the extracellular matrix. Intercellular junctions are resilient and dynamic,
an alimentary tract that is a mirror image of the usual pattern (situs and prevent epithelial tissues from dissociating into their component
inversus), i.e. it rotates in the opposite direction during early develop- cells. In adults, the epidermis withstands imposed deformations because
ment. Defects in ciliary motility disrupt airway mucus clearance, leading of the interplay of two components of intercellular junctions, the junc-
to chronic sinusitis and bronchiectasis. Defects in sensory cilia deter- tional cytoskeleton and cell adhesion molecules (Fig. 1.19). The estab-
mine polycystic kidney disease, anosmia and retinal degeneration. lishment and maintenance of cell polarity in an epithelial layer depends
on two circumferential apical belts, the tight junctions and the zonulae
Microvilli
adherentes, running in parallel to each other and associated with
Microvilli are finger-like cell surface extensions usually 0.1 µm in diam-
F-actin. These two belts control epithelial permeability and determine
eter and up to 2 µm long (Fig. 1.18).
epithelial cell polarity. The apical cell domain resides above the belts;
Microvilli are covered by plasma membrane and supported inter-
the basolateral cell domain resides below the belts. Desmosomes
nally by closely packed bundles of actin filaments linked by cross-
(maculae adherentes) are a third class of spot-like intercellular adhe-
bridges of the actin-bundling proteins, fascin and fimbrin. Other
sion. In contrast to tight junctions and the zonulae adherentes, desmo-
bridges composed of myosin I and calmodulin connect the filament
somes do not form belts and link instead to intermediate filaments. The
bundles to the plasma membrane. At the tip of each microvillus, the
hemidesmosome, anchoring epithelial cells to the basal lamina, also
free ends of microfilaments are inserted into a dense mass that includes
links to intermediate filaments. Gap junctions are unique: they provide
the protein, villin. The actin filament bundles of microvilli are embed-
direct connection between adjacent cells and are not linked to the
ded in the apical cytoplasm amongst a meshwork of transversely
cytoskeleton. Molecular aspects of cell adhesion molecules will be con-
running actin filaments stabilized by spectrin to form the terminal web,
sidered first and then integrated with the junctional cytoskeleton to
which is underlain by keratin intermediate filaments. The web is
define specific structural and molecular aspects of different intercellular
anchored laterally to the tight junctions and zonula adherens of the
junctions.
apical epithelial junctional complex. Myosin II and tropomyosin are
also found in the terminal web, which may explain its contractile Cell adhesion molecules
activity. Cell adhesion molecules are transmembrane or membrane-anchored
Microvilli greatly increase the area of cell surface (up to 40 times), glycoproteins that bridge the intercellular space from the plasma mem-
particularly at sites of active absorption. In the small intestine, they have brane to form adhesive contacts. There are a number of molecular
subgroups, which are broadly divisible on the basis of their dependence
on calcium for function. Calcium-dependent cell adhesion molecules
include cadherins and selectins. Calcium-independent cell adhesion
molecules include the immunoglobulin-like superfamily of cell adhe-
sion molecules (Ig-CAMs), including nectins, and integrins, the only
cell adhesion molecules consisting of two subunits (α and β subunits).
Calcium-dependent cell adhesion molecules:
cadherins and selectins
Cadherins are single-pass transmembrane glycoproteins, with five
heavily glycosylated calcium-binding external domains and an intra-
cellular catenin-binding cytoplasmic tail. Catenins are intracellular
proteins linking cadherins to F-actin in the belt-arranged zonula adhe-
rens. The extracellular segment of cadherins participates in Ca2+-depend-
ent homophilic trans-interactions in which a cadherin molecule on one
cell binds to an identical cadherin molecule on an adjacent cell. After
binding, cadherins cluster laterally (cis-interaction) at cell–cell junc-
tions to form a zipper-like structure that stabilizes tight adhesion
between cells.
Different cell types possess different members of the cadherin family,
e.g. N-cadherins in nervous tissue, E-cadherins in epithelia, and
P-cadherins in the placenta. Two further members of the cadherin
family are the desmogleins and the desmocollins. Cadherins are present
in macula adherens and desmosomes but not in tight junctions or
hemidesmosomes (see below). Alterations in the expression of cadher-
ins in the epidermis produce pathological conditions such as blisters
and ulcerations. See Brieher and Yap (2013) for further reading on
cadherins and their associated cytoskeleton.
As with cadherins, selectins are Ca2+-dependent. In contrast to cad-
Fig . 1 .18 Microvilli sectioned longitudinally in the striated border of an
herins, selectins do not establish homophilic trans-interactions. Instead,
intestinal absorptive cell in a human duodenal biopsy specimen . Actin
filaments fill the cores of the microvilli and insert into the apical they bind to carbohydrates and belong to the group of lectins. Each
cytoplasm . A prominent glycocalyx (formed by the extracellular domains selectin has an extracellular carbohydrate recognition domain (CRD)
of plasma membrane glycoproteins) is seen as a fuzzy coat at the tips of with binding affinity to a specific oligosaccharide attached to a protein
and between microvilli; it includes enzymes concerned with the final or lipid. The molecular configuration and binding affinity of the CRD
stages of digestion . (Courtesy of Dr Bart Wagner, Histopathology to carbohydrate moieties is Ca2+-dependent. Selectins participate in
Department, Sheffield Teaching Hospitals, UK .) the homing of leukocytes circulating in blood towards tissues by | 62 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
23.e1
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When arranged in a regular parallel series, as typified by the absorp-
tive surfaces of the epithelial enterocytes of the small intestine and the
proximal convoluted tubule of the nephron of the kidneys, microvilli
acquire a fuzzy appearance like the bristles of a paintbrush (the designa-
tions brush border or striated border are used at the light microscope
level).
The cytoplasmic tail recruits proteins of the catenin complex:
β-catenin is the first to be recruited and the cadherin–β-catenin complex
rapidly recruits α-catenin; α-catenin binds directly to F-actin and coor-
dinates the activity of actin nucleating proteins and actin binding part-
ners (such as vinculin and α-actinin) to provide the dynamic forces to
modulate cell–cell adhesion; p120-catenin binds to the cytoplasmic tail
of cadherin and becomes a positive regulator of cadherin function. | 63 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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NOITCES
Claudin
Occludin Afadin–nectin complex
APICAL DOMAIN
Catenin complex ZO-1, ZO-2 and ZO-3 Tight
(occluding)
junction
Tight (occluding) junction
Afadin–nectin complex
Zonula
Zonula adherens Actin adherens Tight (occluding) junction
Cadherins
Macula adherens Intermediate
filaments Gap
Plakoglobin, plakophilin Cadherins junction
and desmoplakin
Ig-CAMs
Selectins
Intermediate filaments
Talin Actin
Hemidesmosome
Vinculin
Integrin
Integrin
Macula
S S
Fibronectin Perlecan adherens
S S
Laminin
Type IV collagen
Collagens
Nidogen (entactin)
Fig . 1 .19 Intercellular junctions: the apical junctional complex and other junctional specializations, illustrating the protein components of each junction
and of the basal lamina . An anastomotic network of contacts between adjacent cell membranes forms a tight occluding junction . Basal plasma
membrane is attached to a basal lamina at a hemidesmosome . In a gap junction, numerous channels (pores within connexons) are clustered to form a
plaque-like junctional region between adjacent plasma membranes . (A and C are transmission electron micrographs; B and D are freeze-fractured
preparations .) A, An apical junctional complex . B, A tight junction . C, A hemidesmosome . D, A gap junction . (B, Courtesy of Dr Andrew Kent, King’s
College London . D, Courtesy of Professor Dieter Hülser, University of Stuttgart . A,C, From human tissue, courtesy of Dr Bart Wagner, Histopathology
Department, Sheffield Teaching Hospitals, UK . Diagram modified from Kierszenbaum AL, Tres LL . 2012 . Histology and Cell Biology: An Introduction to
Pathology . 3rd ed, Philadelphia: Elsevier, Saunders; 2011 .)
extravasation across the endothelium. For additional reading on the loops, a transmembrane segment and a cytoplasmic tail. The nectins
significance and mechanism of homing, see Girard et al (2012). and Necls consist of four and five members, respectively. These are
Three major types of selectin include L-selectin (for lymphocytes), present in the belt-like tight junctions and zonula adherens.
E-selectin (for endothelial cells) and P-selectin (for platelets). The nectin–afadin complex initiates the formation of a zonula
adherens and after cell–cell contacts are formed between adjacent
Calcium-independent cell adhesion molecules:
cells, cadherins are recruited to these contact sites. Afadin and α-catenin
Ig-Cams, nectins and integrins interact with one another and also with F-actin through adaptor
Ig-CAMs are cell-surface glycoproteins with an extracellular domain proteins.
characterized by a variable number of immunoglobulin-like loops. Integrins mediate cell–extracellular matrix and cell–cell interactions,
Most Ig-CAMs have a transmembrane domain; others are attached to and integrate extracellular signals with the cytoskeleton and cellular
the cell surface by a glycophosphatidyl inositol (GPI) anchor. As in signalling pathways. Because integrins can be activated by proteins
cadherins, Ig-CAMs establish homophilic interactions contributing to binding to their extracellular or their intracellular domains, they can
cell–cell adhesion, although in a Ca2+-independent manner. The cyto- function in a bidirectional fashion by transmitting information
plasmic tail of Ig-CAMs also interacts with cytoskeletal components outside-in (cues from the extracellular environment) and inside-out
such as F-actin, ankyrins and spectrin. Ig-CAMs can directly or indirectly (cues from the intracellular environment) of the cell. The integrin
bind growth factor receptors and control their internalization. family of proteins consists of α subunits and β subunits forming trans-
Different types are expressed in different tissues. Neural cell adhe- membrane heterodimers. The amino-acid sequence arginine–glycine–
sion molecules (N-CAMs) are found on a number of cell types but are aspartic acid, or RGD motif, on target ligands (such as fibronectin,
expressed widely by neural cells. Intercellular adhesion molecules laminin and other extracellular matrix proteins) has binding affinity
(ICAMs) are expressed on vascular endothelial cells. Cell adhesion to the extracellular binding head of integrins. For further reading on
molecule binding is predominantly homophilic, although some use a integrins and their ligands properties, see Barczyk et al (2010).
heterophilic mechanism, e.g. vascular intercellular adhesion molecule The actin-binding protein talin binds the cytoplasmic domain of
(VCAM), which can bind to integrins. integrin β subunit and activates integrins. Vinculin interacts with talin
Nectins and nectin-like molecules (Necls) are members of the and α-actinin cross-links two filaments of actin. Kindlins, named after
Ig-CAM superfamily (see Takai et al (2008) for further reading on the gene mutated in Kindler’s syndrome, a skin blistering disease, inter-
nectins and Necls). They have an extracellular domain with three Ig-like act with talin to activate integrins.
NIAMOD
LARETALOSAB
ANIMAL
LASAB
XELPMOC
LANOITCNUJ
LACIPA
A B
C D
Hemidesmosome Gap junction | 64 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
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Homing, a process that also enables thymus-derived T cells (see
Ch. 4) to home in on lymph nodes, consists of two phases. In the first,
selectin phase, carbohydrate ligands on the surface of leukocytes adhere
loosely to selectins present on the surface of endothelial cells. During
the second, cooperative sequential integrin phase, strong adhesion
permits the transendothelial migration of leukocytes into the extravas-
cular space in cooperation with cell adhesion molecules of the Ig-CAM
superfamily.
Nectins can interact homophilically or heterophilically with other
nectins to mediate, primarily, adhesion. The intracellular domain of
nectins binds to the cytoplasmic adaptor protein afadin, which links to
actin, whereas Necls interact with scaffolding proteins but not to afadin.
Necls are involved in a large variety of cellular functions, including
axon–glial interaction, Schwann cell differentiation and myelination.
In humans there are about 18 α-subunit subtypes and 8 β-subunit
subtypes, which produce 24 integrin heterodimers. The subunits are
associated by non-covalent interactions and consist of an extracellular
ligand-binding head, two multidomain segments, two single-pass trans-
membrane segments and two cytoplasmic tails. Upon binding of extra-
cellular ligands, integrins undergo a conformational change (integrin
activation), which allows the recruitment of several cytoplasmic F-actin
activator proteins (such as talin, vinculin, α-actinin and kindlins) to
their short cytoplasmic domain. This results in the formation of a
protein complex that interacts with the actin cytoskeleton.
In addition, the protein complex promotes the recruitment and
activation of several protein kinases (such as focal adhesion kinase),
leading to the activation of signalling pathways essential for several
cellular activities such as cell migration, proliferation, survival and gene
expression. | 65 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
ageing, cellular senescence, cancer and apoptosis
25
1
RETPaHC
Genetic mutations in integrins or integrin regulators have been asso- smooth muscle cells, in the intercalated discs of cardiac muscle cells
ciated with Glanzmann’s thrombasthenia (caused by mutations in and between glial cells and neurones. The junctions involve cadherins
integrin β3 subunit), the immunodeficiency disorder leukocyte adhe- attached indirectly to actin filaments on the inner side of the
sion deficiency types I and III (determined by mutations in integrin β2 membrane.
subunit and kindlin 3, respectively) and skin diseases (caused by muta-
tions in kindlin 1 and integrin α2, α6 and β3 subunits). Integrins are Desmosomes (maculae adherentes)
essential in the homing process, following the selectin phase, and are Desmosomes are limited, plaque-like areas of particularly strong inter-
also involved in tumour progression and metastasis. cellular contact. In epithelial cells, they may be located subjacent to the
tight junction and zonula adherens belts, forming collectively the epi-
Specialized intercellular junctions thelial apical junctional complex (see Fig. 1.19A). The intercellular gap
Specialized cell–cell junctions are the hallmark of all epithelial tissues. is approximately 25 nm; it is filled with electron-dense filamentous
There are two major categories: symmetric junctions and asymmetric material (the intercellular cadherins) running transversely across it and
junctions. Symmetric junctions may be subdivided into three types: is also marked by a series of densely staining bands (the cytoplasmic
tight junctions (also known as occluding junctions or zonulae occlu- dense plaques) running parallel to the cell surfaces. Adhesion is medi-
dentes); anchoring junctions (including zonulae adherentes, or belt ated by Ca2+-dependent cadherins, desmogleins and desmocollins.
desmosomes, and maculae adherentes, or spot desmosomes); and com- Within the cells on either side, each cytoplasmic dense plaque underlies
munication junctions, represented by gap junctions. Tight junctions and the plasma membrane and consists of the proteins plakophilin, desmo-
anchoring junctions are components of the epithelial apical junctional plakin and plakoglobin (γ-catenin), into which the ends of intermedi-
complex. Hemidesmosomes are asymmetric junctions (see Fig. 1.19). ate filaments are inserted. The type of intermediate filament depends
on the cell type, e.g. keratins are found in epithelia and desmin fila-
Tight junctions (occluding junctions, ments are found in cardiac muscle cells. Desmosomes form strong
zonulae occludentes) anchorage points, likened to spot-welds, between cells subject to
Tight junctions are the most apical component of the epithelial apical mechanical stress, e.g. in the prickle cell layer of the epidermis, where
junctional complex. The main functions of tight junctions are the regu- they are extremely numerous and large.
lation of the paracellular permeability of the epithelial layer and the
Hemidesmosomes
formation of an apical–basolateral intramembrane diffusion barrier,
the hallmark of epithelial cell polarity. Tight junctions form a continu- Hemidesmosomes are asymmetric anchoring junctions found between
ous belt (zonula) around the cell perimeter, near the apical domain of the basal side of epithelial cells and the associated basal lamina.
epithelial cells, and are connected to the actin cytoskeleton. At the site The latter is a component of the basement membrane and contains
of the tight junction, the plasma membranes of adjacent cells come into laminin, an integrin ligand. The other component of the basement
close contact, so that the space between them is obliterated. Freeze- membrane is the reticular lamina, a collagen-containing layer produced
fracture electron microscopy shows that the contact between these by fibroblasts that also contains fibronectin, another integrin ligand.
membranes is represented by branching and anastomosing sealing Hemidesmosomes resemble a single-sided desmosome, anchored on
strands of protein particles on the P (protoplasmic) face of the lipid one side to the plasma membrane, and on the other to the basal lamina
bilayer (Fig. 1.19A,B). A tight junction contains numerous proteins: and adjacent collagen fibrils (Fig. 1.19C). The plaque has distinct pro-
occludins and claudins, members of the tetraspanin family of proteins, teins not seen in the plaques of a zonula adherens or a macula adher-
containing four transmembrane domains, two loops and two cytoplas- ens: BPAG1 (bullous pemphigoid antigen 1), a member of the plakin
mic tails – occludins and tetraspanins provide the molecular basis for family, and BPAG2 (bullous pemphigoid antigen 2), which possesses
the formation of the branching and anastomosing strands seen in an extracellular collagenous domain. BPAG1 and BPAG2 were initially
freeze-fracture preparations; the afadin–nectin complex and junctional detected in patients with bullous pemphigoid, an autoimmune blister-
adhesion molecules (JAMs), each forming cis-homodimers and interact- ing disease. On the cytoplasmic side of the dense plaque there is a less
ing with each other through their extracellular domains (forming trans- dense plate into which keratin filaments are inserted, where they inter-
homodimers) – nectins and JAMs are members of the immunoglobulin act with the protein plectin associated with integrin α6β4. Hemidesmo-
superfamily, and the afadin component of the afadin–nectin complex somes use integrins and anchoring filaments (laminin 5) as their
interacts with F-actin; and cytosolic zonula occludens proteins 1, 2 and adhesion molecules anchored to the basal lamina, whereas desmo-
3 (ZO-1, ZO-2 and ZO-3). ZO-1 protein is associated with afadin and somes use cadherins.
the intracellular domain of JAMs. All three ZO proteins facilitate the
Focal adhesion plaques
reciprocal interaction of occludins, claudins and JAMs with F-actin.
Defects in paracellular magnesium permeability and reabsorption in Less highly structured attachments with a similar arrangement exist
kidneys occur when there is a mutation in claudin 16 and claudin 19 between many other cell types and their surrounding matrices, e.g.
(renal magnesium wasting). For further reading on claudins, see between smooth muscle cells and their matrix fibrils, and between the
Escudero-Esparza et al (2011). For further reading on JAMs, see Bazzoni ends of skeletal muscle cells and tendon fibres. The smaller, punctate
(2003). adhesions resemble focal adhesion plaques, which are regions of local
attachment between cells and the extracellular matrix. They are typically
anchoring junctions situated at or near the ends of actin filament bundles (stress fibres),
In contrast to tight junctions, zonulae adherentes and maculae adher- anchored through intermediary proteins to the cytoplasmic domains of
entes are characterized by the presence, along the cytosolic sides of the integrins. In turn, these are attached at their external ends to collagen
plasma membranes of adjacent epithelial cells, of symmetric dense or other filamentous structures in the extracellular matrix. They are
plaques connected to each other across the intercellular space by cad- usually short-lived; their formation and subsequent disruption are part
herins. They differ in that F-actin is associated with plaques in zonulae of the motile behaviour of migratory cells. See Geiger et al (2009) for
adherentes and intermediate filaments are linked to plaques in maculae further reading on focal adhesions.
adherentes.
Gap junctions (communicating junctions)
Zonula adherens (belt desmosome) Gap junctions resemble tight junctions in transverse section, but the
A zonula adherens is a continuous belt-like zone of adhesion parallel two apposed lipid bilayers are separated by an apparent gap of 3 nm,
and just basal to a tight junction and also encircling the apical perimeter which is bridged by a cluster of transmembrane channels (connexons).
of epithelial cells. Ca2+-dependent cell adhesion molecules (members Each connexon is formed by a ring of six connexin proteins whose
of the desmoglein and desmocollin families of cadherins) are key com- external surfaces meet those of the adjacent cell in the middle. A minute
ponents of a zonula adherens. In addition to the cadherin–catenin central pore links one cell to the next (Fig. 1.19D). Larger assemblies
complex, a zonula adherens also houses the afadin–nectin complex. of many thousands of channels are often packed in hexagonal arrays.
A specific component of a zonula adherens is a cytoplasmic dense Gap junctions occur between numerous cells, including hepatocytes
plaque attached to the cytosolic side of the plasma membrane. It con- and cardiac myocytes.
sists of desmoplakin, plakophilin and plakoglobin proteins (the latter
is also known as γ-catenin). A similar plaque is seen in a macula adhe-
AGEING, CELLULAR SENESCENCE, CANCER
rens or spot desmosome (see below).
AND APOPTOSIS
Fascia adherens
A fascia adherens is similar to a zonula adherens, but is more Ageing is a universal feature of biological organisms, defined by a
limited in extent and forms a strip or patch of adhesion, e.g. between gradual decline over time in cell and tissue function that often, but not | 66 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
25.e1
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Essentially, two molecules, cadherins and afadin, link to the actin
cytoskeleton. In cultured cells, nectins appear to initiate the formation
of a zonula adherens before the involvement of cadherins. | 67 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
BaSIC STRuCTuRE aNd fuNCTION Of CEllS
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always, decreases the longevity of an individual. The hallmarks of A Granzyme B pathway B FasL pathway
ageing are reviewed in López-Otín et al (2013).
Fas ligand
Cellular senescence is defined by an irreversible arrest in cell prolif- Granzyme B
eration when cells experience DNA damage at telomeres and a decrease
in mitogenic signalling. In contrast to reversibly arrested quiescent cells Death receptors
in G of the cell cycle, senescent growth arrest is irreversible; cells in this
0 Perforin
state cannot be stimulated to proliferate by known stimuli and cannot
be prompted to re-enter the cell cycle by physiological mechanisms. For Active caspase 8
further reading on senescence and the cell cycle, see Chandler and Peters FADD
(2013). Senescent cells can cause or foster degenerative diseases. In old Granzyme B Caspase 8
age, cellular senescence in humans determines typical pathologies, in-
BIDD
cluding atherosclerosis leading to stroke, osteoporosis, macular degen-
eration, cardiopulmonary and renal failure, and neurodegenerative
diseases such as Alzheimer’s and Parkinson’s disease. BAX–BAK
Senescent cells undergo changes in gene expression, which result in channels
the secretion of proinflammatory cytokines, growth factors and pro-
Mitochondrion
teases, activities that collectively define a senescence-associated secre-
tory phenotype capable of triggering angiogenesis, inflammatory
responses, stem cell renewal and differentiation, and which may also
determine resistance to cancer chemotherapy. Senescent cells can be C Cytochrome c pathway
Caspase 3
identified histochemically by their expression of either senescence-
Cytochrome c
associated β-galactosidase, a lysosomal marker which is overexpressed
in these cells, or the tumour suppressor protein p16INK4a, which pro- Apoptosome Caspase 7
motes the formation of senescence-associated chromatin. For further Caspase 9
reading on ageing, cellular senescence and cancer, see Campisi (2013).
Cellular senescence can be caused by a disruption of metabolic Caspase 3
signalling pathways, derived from mitogens and proliferation factors,
and the activation of tumour suppressors, combined with telomere
shortening and genomic damage. See Sahin and DePinho (2012) for Caspase 6 Caspase 2
further reading.
Cellular senescence suppresses tumorigenesis because cell prolifera-
tion is required for cancer development. However, senescent cells can Caspase 8 Caspase 10
stimulate the proliferation and malignant progression of adjacent pre-
malignant cells by the release of senescence-inducing oncogenic stimuli.
Cancer cells must harbour mutations to prevent telomere-dependent Fig . 1 .20 Caspase activation pathways during apoptosis . A, The
granzyme B extrinsic pathway activates caspase 8 and caspase 3
and oncogene-induced senescence, such as in the p53 and p16-
following entry of granzyme B across the plasma membrane pore-forming
retinoblastoma protein pathways. See López-Otín et al (2013) for
protein, perforin . This pathway is observed in cytotoxic T cells or natural
further reading on the pathogenesis of ageing.
killer cells for delivery of the protease granzyme B to target cells . B, The
Fas ligand (FasL) extrinsic pathway is initiated by binding of FasL to
Apoptosis clustered transmembrane death receptors that recruit adaptor proteins,
such as the Fas-associated death-domain protein (FADD) to their
intracellular domain, which in turn recruits and aggregates caspase 8
Cells die as a result of either tissue injury (necrosis) or the internal molecules, which become activated . Activated caspase 8 activates
activation of a ‘suicide’ programme (apoptosis) in response to extrinsic caspase 7 and caspase 3 . C, The cytochrome c intrinsic pathway starts
or intrinsic cues. Apoptosis (programmed cell death) is defined by the when granzyme B or activated caspase 8 causes the truncation by
controlled demolition of cellular constituents and the ultimate uptake proteolysis of the protein BIDD (BH3-interacting domain death agonist),
of apoptotic cell fragments by other cells to prevent immune responses. which penetrates a mitochondrion through BAX–BAK (BCL-2 associated
Some senescent cells become resistant to cell-death signalling, i.e. they X protein–BCL-2 antagonist killer) channel proteins on the outer
are apoptosis-resistant. In effect, senescence blocks growth of damaged mitochondrial membrane, causing the release of cytochrome c.
or stressed cells, whereas apoptosis quickly disposes of them. Apoptosis Cytochrome c enables the assembly of the apoptosome (consisting of
is a central mechanism controlling multicellular development. During seven molecules of apoptosis protease-activating factor-1 (APAF1) and
morphogenesis, apoptosis mediates activities such as the separation of seven molecules of caspase 9), which in turn activates caspase 3 and
the developing digits, and plays an important role in regulating the caspase 7 . Finally, the proteolytic activation cascade of caspase 6,
number of neurones in the nervous system (the majority of neurones caspase 2, caspase 8 and caspase 10 executes cell deconstruction .
die during development). Apoptosis also ensures that inappropriate
or inefficient T cells are eliminated in the thymus during clonal
enter the cell. The intrinsic mitochondrial route involves the release of
selection.
cytochrome c from the space between the inner and outer mitochon-
The morphological changes exhibited by necrotic cells are very dif-
drial membranes into the cytosol. Extrinsic and intrinsic pathways
ferent from those seen in apoptotic cells. Necrotic cells swell and sub-
work cooperatively in the subsequent activation of a family of initiator-
sequently rupture, and the resulting debris may induce an inflammatory
effector proteases, known as caspases (cysteine aspartic acid-specific
response. Apoptotic cells shrink, their nuclei and chromosomes frag-
proteases), which are present in healthy cells as inactive precursor
ment, forming apoptotic bodies, and their plasma membranes undergo
enzymes or zymogens. Activation of caspases 3, 6 and 7 mediates apop-
conformational changes that act as a signal to local phagocytes. The
tosis by initiating a cascade of degradative processes that target major
dead cells are removed rapidly, and as their intracellular contents are
constituents of the cell cytoskeleton, producing membrane blebbing, a
not released into the extracellular environment, inflammatory reactions
distinctive feature of apoptosis caused by cytosolic and nuclear frag-
are avoided; the apoptotic fragments also stimulate macrophages to
ments flowing into the developing apoptotic bodies. Caspase cleavage
release anti-inflammatory cytokines.
inactivates many systems that normally promote damage repair and
Apoptosis and cell proliferation are intimately coupled; several cell
support cell viability, and activates a number of proteins that promote
cycle regulators can influence both cell division and apoptosis. The
the death and disassembly of the cell. For further reading on apoptosis,
signals that trigger apoptosis include withdrawal of survival factors or
see Taylor et al (2008).
exposure to inappropriate proliferative stimuli. Three main routes to
the induction of apoptosis have been established (Fig. 1.20). Two, the
Fas ligand (FasL) pathway and the granzyme B pathway, are extrinsic,
Bonus e-book video
whereas the mitochondrial route is intrinsic. The Fas ligand (FasL)
pathway involves binding of FasL to death receptors on the plasma
membrane and recruitment of adaptor proteins, such as the Fas-associ-
ated death domain proteins, followed by the recruitment and activation Video 1 .1 Mitosis in a cell with fluorescently-labelled chromosomes
of caspase 8. The granzyme B pathway involves creation of a perforin and microtubules .
plasma membrane channel enabling the caspase-like granzyme B to | 68 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Basic structure and function of cells
26.e1
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The ends of the chromosomes, or telomeres, become shorter and
more dysfunctional with each DNA replication round. Telomere short-
ening has been shown to activate DNA damage responses, leading to
mitochondrial dysfunction (a decrease in production of ATP and an
increase in reactive oxygen species) and the activation of p53, which
induces growth arrest, apoptosis and senescence of stem cells and pro-
genitor cells. p53 interconnects with different longevity metabolic sig-
nalling pathways, including the insulin, insulin-like growth factor I
(IGFI) and mammalian target of rapamycin (mTOR) pathways, which
are known to regulate lifespan by increasing the expression of genes
involved in stress resistance and energy balance. Mutations in TERC (the
RNA component of telomerase) and TERT (the catalytic component of
telomerase) are found in patients with the premature ageing syndrome,
dyskeratosis congenita (poor growth of fingernails and toenails, skin
pigmentation and oral leukoplakia). Other important contributors to
cell senescence are dysregulated autophagy and lack of disposal of
misfolded proteins by the ubiquitin–26S proteasome machinery.
These responses are collectively designated telomere-initiated cellular
senescence. | 69 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
27
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Key references
KEY REFERENCES
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A comprehensive presentation of the structural and molecular features of the gradual loss of physiological integrity leading to major human pathological
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movement in living cells. loss of proteolysis and mitochondrial dysfunction are considered.
Burke B, Stewart CL 2013 The nuclear lamins: flexibility in function. Nat Rev Pollard TD, Earnshaw WC 2008 Cell Biology. Philadelphia: Elsevier,
Mol Cell Biol 14:13–24. Saunders.
An up-to-date, detailed description of the nuclear lamina and its major A detailed and comprehensive account of structural and molecular aspects of
components, lamins, members of the intermediate filament protein family. cell biology, including abnormalities related to human disease.
Chinnery PF, Hudson G 2013 Mitochondrial genetics. Br Med Bull 106: Porter RM, Lane EB 2003 Phenotypes, genotypes and their contribution to
135–59. understanding keratin function. Trends Genet 19:278–85.
A detailed survey of the involvement of mitochondrial DNA (mtDNA) A correlation of human epithelial pathological conditions with mouse
defects in human disease, with a specific focus on the mechanisms mutant studies focused on keratin diversity required for cells to attune to
controlling mtDNA inheritance. mechanical and biochemical signalling.
Girard JP, Moussion C, Förster R 2012 HEVs, lymphatics and homeostatic Saftig P, Klumperman J 2009 Lysosome biogenesis and lysosomal mem-
immune cell trafficking in lymph nodes. Nat Rev Immunol 12: brane proteins: trafficking meets function. Nat Rev Mol Cell Biol 10:
762–73. 623–35.
A comprehensive description of the continuous trafficking of immune cells The participation of lysosomes in the degradation of extracellular material
across the vascular endothelium (homing) engaging cell adhesion molecules. internalized by endocytosis and lysosomal sorting pathways, reviewed within
the context of human diseases resulting from defective lysosomal biogenesis.
Kierszenbaum AL, Tres LL 2012 Histology and Cell Biology: An Introduction
to Pathology. Philadelphia: Elsevier, Saunders. Scholey JM 2008 Intraflagellar transport motors in cilia: moving along the
An integrated visual view of histology, cell biology and basic pathology cell’s antenna. J Cell Biol 180:23–9.
focused on structure and function, including human pathological examples Ciliopathies derived from the defective assembly, maintenance and function
from a molecular viewpoint. of the axoneme in motile and sensory cilia, considered within the framework
of intraflagellar transport proteins and associated molecular motors.
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153:1194–217. | 71 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
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CHAPTER
2
Integrating cells into tissues
Cells evolved as single, free-living organisms, but natural selection basal lamina, which is synthesized predominantly by the epithelial
favoured more complex communities of cells, multicellular organisms, cells. The basal lamina is described on page 34.
where groups of cells specialize during development to carry out specific Epithelia can usually regenerate when injured. Indeed, many epithe-
functions for the body as a whole. This allowed the emergence of larger lia continuously replace their cells to offset cell loss caused by mechani-
organisms with greater control over their internal environment and the cal abrasion (reviewed in Blanpain et al (2007)). Blood vessels do not
evolution of highly specialized organic structures such as the brain. penetrate typical epithelia and so cells receive their nutrition by diffu-
The human body contains more than 200 different cell types, sharing sion from capillaries of neighbouring connective tissues. This arrange-
the same genome but with different patterns of gene expression. ment limits the maximum thickness of living epithelial cell layers.
Some cells in the body are essentially migratory, but most exist as Epithelia, together with their supporting connective tissue, can often be
cellular aggregates in which individual cells carry out similar or closely removed surgically as one layer, which is collectively known as a mem-
related functions in a coordinated manner. These aggregates are termed brane. Where the surface of a membrane is moistened by mucous
tissues, and can be classified into a fairly small number of broad catego- glands it is called a mucous membrane or mucosa, whereas a similar
ries on the basis of their structure, function and molecular properties. layer of connective tissue covered by mesothelium is called a serous
On the basis of their structure, most tissues are divided into four major membrane or serosa.
types: epithelia, connective or supporting tissue, muscle and nervous
tissue. Epithelia are continuous layers of cells with little intercellular
space, which cover or line surfaces, or have been so derived. In connec- CLASSIFICATION
tive tissues, the cells are embedded in an extracellular matrix, which,
typically, forms a substantial and important component of the tissue. Epithelia can be classified as unilaminar (single-layered, simple), in
Muscle consists largely of specialized contractile cells. Nervous tissue which a single layer of cells rests on a basal lamina; or multilaminar,
consists of cells specialized for conducting and transmitting electrical in which the layer is more than one cell thick. The latter includes:
and chemical signals and the cells that support this activity. stratified squamous epithelia, in which flattened superficial cells are
There is molecular evidence that this structure-based scheme of clas- constantly replaced from the basal layers; urothelium (transitional epi-
sification has validity. Thus the intermediate filament proteins charac- thelium), which serves special functions in the urinary tract; and other
teristic of all epithelia are keratins (Pan et al 2012); those of connective multilaminar epithelia such as those lining the largest ducts of some
tissue are vimentins; those of muscle are desmins; and those of nervous exocrine glands, which, like urothelium, are replaced only very slowly
tissue are neurofilament and glial fibrillary acidic proteins. However, under normal conditions. Seminiferous epithelium is a specialized
cells such as myofibroblasts, neuroepithelial sensory receptors and multilaminar tissue found only in the testis.
ependymal cells of the central nervous system have features of more
than one tissue type. Despite its anomalies, the scheme is useful for Unilaminar (simple) epithelia
descriptive purposes; it is widely used and will be adopted here.
In this chapter, two of the major tissue categories, epithelia and
Unilaminar epithelia are further classified according to the shape of
general connective and supporting tissues, will be described. Special-
their cells, into squamous, cuboidal, columnar and pseudostratified
ized skeletal connective tissues, i.e. cartilage and bone, together with
types. Cell shape may, in some cases, be related to cell volume. Where
skeletal muscle, are described in detail in Chapter 5 as part of the mus-
little cytoplasm is present, there are generally few organelles and there-
culoskeletal system overview. Smooth muscle and cardiac muscle are
fore there is low metabolic activity and cells are squamous or low
described in Chapter 6. Nervous system tissues are described in Chapter
cuboidal. Highly active cells, e.g. secretory epithelia, contain abundant
3. Specialized defensive cells, which also form a migrant population
mitochondria and endoplasmic reticulum, and are typically tall cuboi-
within the general connective tissues, are considered in more detail in
dal or columnar. Unilaminar epithelia can also be subdivided into
Chapter 4, with blood, lymphoid tissues and haemopoiesis.
those that have special functions, such as those with cilia, numerous
microvilli, secretory vacuoles (in mucous and serous glandular cells) or
EPITHELIA sensory features. Myoepithelial cells, which are contractile, are found as
isolated cells associated with glandular structures, e.g. salivary and
mammary glands.
The term epithelium is applied to the layer or layers of cells that cover
the body surfaces or line the body cavities that open on to it. The fate Squamous epithelium
of embryonic epithelial populations is illustrated in Figure 12.3. Epi- Simple squamous epithelium is composed of flattened, tightly apposed,
thelia function generally as selective barriers that facilitate, or inhibit, polygonal cells (squames). This type of epithelium is described as tes-
the passage of substances across the surfaces they cover. In addition, sellated when the cells have complex, interlocking borders rather than
they may: protect underlying tissues against dehydration, chemical or straight boundaries. The cytoplasm may in places be only 0.1 µm thick
mechanical damage; synthesize and secrete products into the spaces and the nucleus usually bulges into the overlying space (Fig. 2.2A).
that they line; and function as sensory surfaces. In this respect, many These cells line the alveoli of the lungs, where their surface area is huge
features of nervous tissue can be regarded as those of a modified and cytoplasmic volume correspondingly large, and they also form the
epithelium and the two tissue types share an origin in embryonic outer capsular wall of renal corpuscles, the thin segments of the renal
ectoderm. tubules and various parts of the inner ear. Because it is so thin, simple
Epithelia (Fig. 2.1) are predominantly cellular and the little extracel- squamous epithelium allows rapid diffusion of gases and water across
lular material they possess is limited to the basal lamina. Intercellular its surface; it may also engage in active transport, as indicated by the
junctions, which are usually numerous, maintain the mechanical cohe- presence of numerous endocytic vesicles in these cells. Tight junctions
siveness of the epithelial sheet and contribute to its barrier functions. (occluding junctions, zonulae adherentes) between adjacent cells
A series of three intercellular junctions forms a typical epithelial junc- ensure that materials pass primarily through cells, rather than between
tional complex: in sequence from the apical surface, this consists of a them.
tight junctional zone, an adherent (intermediate) junctional zone and
Cuboidal and columnar epithelia
a region of discrete desmosome junctions. Epithelial cell shape is most
usually polygonal and partly determined by cytoplasmic features such Cuboidal and columnar epithelia consist of regular rows of cylindrical
as secretory granules. The basal surface of an epithelium lies in contact cells (Figs 2.2B, C). Cuboidal cells are approximately square in vertical
with a thin layer of filamentous protein and proteoglycan termed the section, whereas columnar cells are taller than their diameter, and both | 72 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Epithelia
29
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RETPAHC
UNILAMINAR (SIMPLE) MULTILAMINAR
Squamous Stratified squamous
See also:
Mesothelium – lining body cavities
Endothelium – lining blood and lymphatic vessels
Non-keratinizing Keratinizing
Cuboidal Specializations Stratified cuboidal/columnar
Ciliated Secretory
Columnar Urothelial (transitional)
Without surface With microvilli Pseudostratified Relaxed Stretched
specialization (brush/striated border)
COMPLEX DERIVED STRUCTURES
• Multicellular – exocrine and endocrine glands • Nervous tissue – often classified separately, but retains many
• Sensory structures – e.g. taste buds characteristics of its epithelial origins
• Tooth germ • Seminiferous epithelium
Fig. 2.1 Classification of epithelial tissues and cells.
are polygonal when sectioned horizontally. Commonly, microvilli are Sensory epithelia
found on their free surfaces, which considerably increases the absorp-
Sensory epithelia are found in special sense organs of the olfactory,
tive area, e.g. in the epithelia of the small intestine (columnar cells with
gustatory and vestibulocochlear receptor systems. All of these contain
a striated border of very regular microvilli), the gallbladder (columnar
sensory cells surrounded by supportive non-receptor cells. Olfactory
cells with a brush border of microvilli); proximal convoluted tubules
receptors are modified neurones and their axons pass directly to the
of the kidney (large cuboidal to low columnar cells with brush borders);
brain, but the other types are specialized epithelial cells that synapse
and the epididymis (columnar cells with extremely long microvilli,
with terminals of afferent (and sometimes efferent) nerve fibres.
erroneously termed stereocilia).
Ciliated columnar epithelium lines most of the respiratory tract, Myoepithelial cells
except for the lower pharynx and vocal folds, and it is pseudostratified
(Fig. 2.2D) as far as the larger bronchioles; it also lines some of the
Myoepithelial cells, which are also sometimes termed basket cells, are
tympanic cavity and auditory tube; the uterine tube; and the efferent
fusiform or stellate in shape (Fig. 2.3), contain actin and myosin fila-
ductules of the testis. Submucosal mucous glands and mucosal goblet
ments, and contract when stimulated by nervous or endocrine signals.
cells secrete mucus on to the luminal surface of much of the respira-
They surround the secretory portions and ducts of some glands, e.g.
tory tract, and cilia sweep a layer of mucus, trapped dust particles and
mammary, lacrimal, salivary and sweat glands, and lie between the
so on from the lung towards the pharynx in the mucociliary rejection
basal lamina and the glandular or ductal epithelium. Their contraction
current, which clears the respiratory passages of inhaled particles. Cilia
assists the initial flow of secretion into larger conduits. Myoepithelial
in the uterine tube assist the passage of oocytes and fertilized ova to
cells are ultrastructurally similar to smooth muscle cells in the arrange-
the uterus.
ment of their actin and myosin, but differ from them because they
Some columnar cells are specialized for secretion, and aggregates of
originate, like the glandular cells, from embryonic ectoderm or endo-
such cells may be described as glandular tissue. Their apical domains
derm. They can be identified immunohistochemically on the basis of
typically contain mucus- or protein-filled (zymogen) vesicles, e.g.
the co-localization of myofilament proteins (which signify their con-
mucin-secreting and chief cells of the gastric epithelium. Where mucous
tractile function (Fig. 2.4)) and keratin intermediate filaments (which
cells lie among non-secretory cells, e.g. in the intestinal epithelium,
accords with their epithelial lineage).
their apical cytoplasm and its secretory contents often expand to
produce a characteristic cell shape, and they are known as goblet cells
Multilaminar (stratified) epithelia
(see Fig. 2.2D). For further details of glandular tissue, see page 32, and
for the characteristics of mucus, see page 40.
Multilaminar epithelia are found at surfaces subjected to mechanical
Pseudostratified epithelium
damage or other potentially harmful conditions. They can be divided
Pseudostratified epithelium is a single-layered (simple) columnar epi- into those that continue to replace their surface cells from deeper layers,
thelium in which nuclei lie at different levels in a vertical section (Fig. designated stratified squamous epithelia, and others in which replace-
2.2D). All cells are in contact with the basal lamina throughout their ment is extremely slow except after injury.
lifespan, but not all cells extend through the entire thickness of the
Stratified squamous epithelia
epithelium. Some constitute an immature basal cell layer of smaller
cells, which are often mitotic and able to replace damaged mature cells. Stratified squamous epithelia are multilayered tissues in which the
Migrating lymphocytes and mast cells within columnar epithelia may formation, maturation and loss of cells is continuous, although the
also give a similar, pseudostratified appearance because their nuclei are rates of these processes can change, e.g. after injury. New cells are
found at different depths. Much of the ciliated lining of the respiratory formed in the most basal layers by the mitotic division of stem cells
tract is of the pseudostratified type, and so is the sensory epithelium of and transit (or transient) amplifying cells. The daughter cells move
the olfactory area. more superficially, changing gradually from a cuboidal shape to a more | 73 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
INTEgRATINg CEllS INTO TISSuES
30
1
NOITCES
U
RC
U
A B
C D
Fig. 2.2 A, Simple squamous epithelium lining the outer parietal layer (arrows) of a Bowman’s capsule in the renal corpuscle (RC), stained with the
trichrome, Martius Scarlet Blue (MSB). Oval epithelial nuclei project into the urinary space (U), within a highly attenuated cytoplasm. B, Simple cuboidal
epithelium lining a group of collecting ducts sectioned longitudinally in the renal medulla. The basement membranes are stained magenta with periodic–
acid Schiff (PAS) reagent. C, Simple columnar epithelium covering the tip (off field, right) of a villus in the ileum. Tall, columnar absorptive cells with oval,
vertically orientated nuclei bear a striated border of microvilli, just visible as a deeper-stained apical fringe. Numerous interspersed goblet cells are
present, with pale apical cytoplasm filled with mucinogen secretory granules and dark, flattened, basally situated nuclei. D, Ciliated columnar
pseudostratified epithelium in the respiratory tract, and interspersed goblet cells, with pale, mucinogen granule-filled apical cytoplasm. All human tissues.
(All human tissues, courtesy of Mr Peter Helliwell and the late Dr Joseph Mathew, Department of Histopathology, Royal Cornwall Hospitals Trust, UK.)
FF
FF
MM
MM
CC
CC
MM
Fig. 2.3 Stellate myoepithelial cells (M) wrapped around secretory acini in
the lactating mouse mammary gland, seen in the scanning electron
microscope after enzymatic depletion of extracellular matrix. Blood
Fig. 2.4 Myoepithelial cells (stained brown), in a human breast duct,
capillaries (C) and fibroblasts (F) are also indicated. (Courtesy of
demonstrated immunohistochemically using antibody to smooth muscle
Prof. Toshikazu Nagato, Fukuoka Dental College, Japan.)
actin. (Courtesy of Mr Peter Helliwell and the late Dr Joseph Mathew,
Department of Histopathology, Royal Cornwall Hospitals Trust, UK.) | 74 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Epithelia
31
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RETPAHC
K
A B
C D
Fig. 2.5 A, Keratinized stratified squamous epithelium in thin skin. Pigmented melanocytes are seen in the basal layer and a few keratinocytes of the
prickle cell layer also contain melanin granules. The dead, keratinized layer (K) lacks nuclei. B, Non-keratinized stratified squamous epithelium of the
uterine ectocervix, stained with periodic–acid Schiff (PAS) reagent. The basement membrane (short arrows) and superficial squames, which retain their
nuclei, are PAS-positive; squames sloughing off the surface are indicated (long arrow). C, Stratified low columnar epithelium of an interlobular excretory
duct of the sublingual salivary gland. D, Urothelium (transitional epithelium) lining the relaxed urinary bladder. The most superficial cells have a thickened
plasma membrane as a result of the presence of intramembranous plaques, which give an eosinophilic appearance to the luminal surface (arrows). All
human tissues. (All human tissues, courtesy of Mr Peter Helliwell and the late Dr Joseph Mathew, Department of Histopathology, Royal Cornwall
Hospitals Trust, UK.)
flattened form, and are eventually shed from the surface as a highly general shape as are seen in the keratinized type, but they do not fill
flattened squame. Typically, the cells are held together by numerous completely with keratin or secrete glycolipid, and they retain their
desmosomes to form strong, contiguous cellular sheets that provide nuclei until they desquamate at the surface. In sites where considerable
protection to the underlying tissues against mechanical, microbial and abrasion occurs, e.g. parts of the buccal cavity, the epithelium is thicker
chemical damage. Stratified squamous epithelia may be broadly subdi- and its most superficial cells may partly keratinize, so that it is referred
vided into keratinized and non-keratinized types. to as parakeratinized, in contrast to the orthokeratinized state of fully
keratinized epithelium. Diets deficient in vitamin A may induce kerati-
Keratinized epithelium nization of such epithelia, and excessive doses may lead to its transfor-
Keratinized epithelium (Fig. 2.5A) is found at surfaces that are subject mation into mucus-secreting epithelium.
to drying or mechanical stresses, or are exposed to high levels of abra-
Stratified cuboidal and columnar epithelia
sion. These include the entire epidermis and the mucocutaneous junc-
tions of the lips, nostrils, distal anal canal, outer surface of the tympanic Two or more layers of cuboidal or low columnar cells (Fig. 2.5C) are
membrane and parts of the oral lining (gingivae, hard palate and fili- typical of the walls of the larger ducts of some exocrine glands, e.g. the
form papillae on the anterior part of the dorsal surface of the tongue). pancreas, salivary glands and the ducts of sweat glands, and they pre-
Their cells, keratinocytes, are described in more detail on page 141. A sumably provide more strength than a single layer. Parts of the male
distinguishing feature of keratinized epithelia is that cells of the super- urethra are also lined by stratified columnar epithelium. The layers are
ficial layer, the stratum corneum, are anucleate, dead, flattened squames not continually replaced by basal mitoses and there is no progression
that eventually flake off from the surface. In addition, the tough keratin of form from base to surface, but they can repair themselves if damaged.
intermediate filaments become firmly embedded in a matrix protein.
Urothelium (urinary or
This unusual combination of strongly coherent layers of living cells and
transitional epithelium)
more superficial strata made of plates of inert, mechanically robust
protein complexes, interleaved with water-resistant lipid, makes this Urothelium (Fig. 2.5D) is a specialized epithelium that lines much of
type of epithelium an efficient barrier against different types of injury, the urinary tract and prevents its rather toxic contents from damaging
microbial invasion and water loss. surrounding structures. It extends from the ends of the collecting ducts
of the kidneys, through the ureters and bladder, to the proximal portion
Non-keratinized epithelium of the urethra. In males it lines the urethra as far as the ejaculatory ducts,
Non-keratinized epithelium is present at surfaces that are subject to then becomes intermittent and is finally replaced by stratified columnar
abrasion but protected from drying (Fig. 2.5B). These include: the epithelium in the membranous urethra. In females it extends as far as
buccal cavity (except for the areas noted above); oropharynx and laryn- the urogenital membrane.
gopharynx; oesophagus; part of the anal canal; vagina; distal uterine The epithelium appears to be 4–6 cells thick and lines organs that
cervix; distal urethra; cornea; inner surfaces of the eyelids; and the undergo considerable distension and contraction. It can therefore
vestibule of the nasal cavities. Cells go through the same transitions in stretch greatly without losing its integrity. In stretching, the cells become | 75 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
INTEgRATINg CEllS INTO TISSuES
32
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NOITCES
flattened without altering their positions relative to each other, because secrete small amounts of protein by a merocrine mechanism, and have
they are firmly connected by numerous desmosomes. However, the been reclassified as merocrine glands.
urothelium appears to be reduced to only 2–3 cells thick. The epithe- In apocrine glands, some of the apical cytoplasm is pinched off with
lium is called transitional because of the apparent transition from a the contained secretions, which are stored in the cell as membrane-free
stratified cuboidal epithelium to a stratified squamous epithelium, droplets (see Fig. 2.6). The best-understood example of this is the secre-
which occurs as it is stretched to accommodate urine, particularly in tion of milk fat by mammary gland cells, in which a small amount of
the bladder. The basal cells are basophilic and contain many ribosomes; cytoplasm is incorporated into the plasma membrane-bound lipid
they are uninucleate (diploid), and cuboidal when relaxed. More api- globule as it is released from the cell. Larger amounts of cytoplasm are
cally, they form large binucleate or, more often, polyploid uninucleate included in secretions by specialized apocrine sweat glands in the axilla
cells. The surface cells are the largest and may even be octoploid; in the (Stoeckelhuber et al 2011) and anogenital regions of the body. In some
relaxed state they typically bulge into the lumen as dome-shaped cells tissues there is a combination of different types of secretion, e.g.
with a thickened, eosinophilic glycocalyx or cell coat. Their luminal mammary gland cells secrete milk fat by apocrine secretion and milk
surfaces are covered by a specialized plasma membrane in which protein, casein, by merocrine secretion.
plaques of intramembranous glycoprotein particles are embedded to In holocrine glands (see Fig. 2.6), e.g. sebaceous glands in the skin,
stiffen the membrane. When the epithelium is relaxed, the surface area the cells first fill with secretory products (lipid droplets or sebum, in
of the cells is reduced and the plaques are partially internalized by the this instance), after which the entire cell disintegrates to liberate the
hinge-like action of the more flexible interplaque membrane regions. accumulated mass of secretion into the adjacent duct or, more usually,
The plaques re-emerge on to the surface when it is stretched. hair follicle.
Normally, cell turnover is very slow; cell division is infrequent and
is restricted to the basal layer. However, when damaged, the epithelium Structural and functional classification
regenerates quite rapidly.
Seminiferous epithelium Exocrine glands are either unicellular or multicellular. The latter may
be in the form of simple sheets of secretory cells, e.g. the lining of the
Seminiferous epithelium is a highly specialized, complex stratified epi-
stomach, or may be structurally more complex and invaginated to a
thelium. It consists of a heterogeneous population of cells that form
variable degree. Such glands (see Fig. 2.6) may be simple units or their
the lineage of the spermatozoa (spermatogonia, spermatocytes, sper-
connection to the surface may be branched. Simple unbranched tubular
matids), together with supporting cells (Sertoli cells). It is described in
glands exist in the walls of many of the hollow viscera, e.g. the small
detail on page 1275.
intestine and uterus, whereas some simple glands have expanded, flask-
like ends (acini or alveoli). Such glands may consist entirely of secretory
GLANDS cells, or may have a blind-ending secretory portion that leads through
a non-secretory duct to the surface, in which case the ducts may modify
the secretions as they pass along them.
One of the features of many epithelia is their ability to alter the environ-
Glands with ducts may be branched (compound) and sometimes
ment facing their free surfaces by the directed transport of ions, water
form elaborate ductal trees. Such glands generally have acinar or alveo-
or macromolecules. This is particularly well demonstrated in glandular
lar secretory lobules, as in the exocrine pancreas, but the secretory units
tissue, in which the metabolism and structural organization of the cells
may alternatively be tubular or mixed tubulo-acinar. More than one
are specialized for the synthesis and secretion of macromolecules,
type of secretory cell may occur within a particular secretory unit, or
usually from the apical surface. Such cells may exist in isolation amongst
individual units may be specialized to just one type of secretion (e.g.
other non-secretory cells of an epithelium, e.g. goblet cells in the
serous acini of salivary glands).
absorptive lining of the small intestine, or may form highly coherent
Exocrine glands are also classified by their secretory products. Secre-
sheets of epithelium with a common secretory function, e.g. the mucous
tory cells in mucus-secreting or mucous glands have frothy cytoplasm
lining of the stomach and, in a highly invaginated structure, the complex
and basal, flattened nuclei. They stain deeply with metachromatic stains
salivary glands.
and periodic acid–Schiff (PAS) methods that detect carbohydrate resi-
Glands may be subdivided into exocrine glands and endocrine
dues. However, in general (i.e. non-specific) histological preparations,
glands. Exocrine glands secrete, usually via a duct, on to surfaces that
they are weakly stained because much of their content of water-rich
are continuous with the exterior of the body, including the alimentary
mucin has been extracted by the processing procedures. Secretory cells
tract, respiratory system, urinary and genital ducts and their derivatives,
in serous glands have centrally placed nuclei and eosinophilic secretory
and the skin. Endocrine glands are ductless and secrete hormones
storage granules in their cytoplasm. They secrete mainly glycoproteins
directly into interstitial fluid and thence the circulatory system, which
(including lysozyme) and digestive enzymes.
conveys them throughout the body to affect the activities of other cells.
Some glands are almost entirely mucous (e.g. the sublingual salivary
In addition to strictly epithelial glands, some tissues derived from the
gland), whereas others are mainly serous (e.g. the parotid salivary
nervous system, including the suprarenal medulla and neurohypophy-
gland). The submandibular gland is mixed, in that some lobules are
sis, are neurosecretory.
predominantly mucous and others serous. Mucous acini may share a
Paracrine glandular cells are similar to endocrine cells but their
lumen with clusters of serous cells (seen in routine preparations as
secretions diffuse locally to cellular targets in the immediate vicinity;
serous demilunes). Although this simple approach to classification is
many are classed as neuroendocrine cells because they secrete mole-
useful for general descriptive purposes, the diversity of molecules syn-
cules used elsewhere in the nervous system as neurotransmitters or
thesized and secreted by glands is such that complex mixtures often
neuromodulators. Modes of signalling by secretory cells are illustrated
exist within the same cell.
in Figure 1.6.
ENDOCRINE GLANDS
EXOCRINE GLANDS
Endocrine glands secrete directly into connective tissue interstitial fluid
Types of secretory process
and thence the circulation. Their cells are grouped around beds of capil-
laries or sinusoids, which typically are lined by fenestrated endothelia
The mechanism of secretion varies considerably. If the secretions are to allow the rapid passage of macromolecules through their walls.
initially packaged into membrane-bound vesicles, these are conveyed Endocrine cells may be arranged in clusters within vascular networks,
to the cell surface, where they are discharged. In merocrine secretion, in cords between parallel vascular channels or as hollow structures (fol-
which is by far the most common secretory mechanism, vesicle mem- licles) surrounding their stored secretions. In addition to the cells of
branes fuse with the plasma membrane to release their contents to the specialized ductless endocrine glands (e.g. pituitary, pineal, thyroid and
exterior (Fig. 2.6). Specialized transmembrane molecules in the secre- parathyroid), hormone-producing cells also form components of other
tory vesicle wall recognize marker proteins on the cytoplasmic side of organ systems. These include: the cells of the pancreatic islets; thymic
the plasma membrane and bind to them. This initiates interactions with epithelial cells; renin-secreting cells of the kidney juxtaglomerular appa-
other proteins that cause the fusion of the two membranes and the ratus; erythropoietin-secreting cells of the kidney; circumventricular
consequent release of the vesicle contents. The stimulus for secretion organs; interstitial testicular (Leydig) cells; interstitial follicular and
varies with the type of cell but often appears to involve a rise in intracel- luteal ovarian cells; and placental cells (in pregnancy). Some cardiac
lular calcium. Glands such as the simple sweat glands of the skin, where myocytes, particularly in the walls of the atria, also have endocrine
ions and water are actively transported from plasma as an exudate, were functions. These cells are all described in detail within the appropriate
once classified as eccrine glands. They are now known to synthesize and regional sections. | 76 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
glands
33
2
RETPAHC
Mechanisms of secretion Arrangement of cells
A. Merocrine B. Apocrine C. Holocrine A. Unicellular B. Multicellular sheet
Structural classification of glands – Simple glands with unbranched ducts
A. Simple tubular without duct B. Simple tubular with duct C. Simple branched tubular D. Simple coiled tubular E. Simple acinar or alveolar
Structural classification of glands – Ductal branching pattern of complex glands
A. Branched tubular B. Branched acinar/alveolar C. Branched tubulo-acinar
Fig. 2.6 Classification of the different types of epithelial gland.
Isolated endocrine cells also exist scattered amongst other tissues as glands have a rich vascular supply and their blood flow is controlled
part of the dispersed (diffuse) neuroendocrine system, e.g. throughout by autonomic vasomotor nerves, which can thus modify glandular
the alimentary and respiratory tracts. Neuroendocrine cells are generally activity.
situated within a mucosal epithelium and their bases often rest on the Glandular activity may also be controlled directly by autonomic
basal lamina (see below). In response to an external stimulus, they secretomotor fibres, which may either form synapses on the bases of
secrete their product basally into interstitial fluid. A typical neuroendo- gland cells (e.g. in the suprarenal medulla) or release neuromediators
crine cell is shown in Figure 2.7. The secretory granules vary in shape, in the vicinity of the glands and reach them by diffusion. Alternatively,
size and ultrastructure according to cell type. Cells often take the name the autonomic nervous system may act indirectly on gland cells, e.g.
of the secretion they produce, e.g. gastrin-secreting G cells of the small on neuroendocrine G cells via histamine, released neurogenically
intestine. Neuroendocrine cells share many of their secretory products from another neuroendocrine cell in the gastric lining. Such paracrine
with chemical mediators in the nervous system. activities of neuroendocrine cells are also important in the respiratory
system.
Circulating hormones from the adenohypophysis stimulate syn-
CONTROL OF GLANDULAR SECRETION thesis and secretion by target cells in many endocrine glands. Such
signals, mostly detected by receptors at the cell surface and mediated
The activities of cells in the various tissue and organ systems of the body by second messenger systems, may increase the synthetic activity of
are tightly regulated by the coordinated activity of the endocrine and gland cells, and may cause them to discharge their secretions by exocy-
autonomic nervous systems. Endocrine (and paracrine) signals reach tosis. Secretions from certain exocrine glandular cells are expressed
target cells in interstitial fluid, often via blood plasma, and together rapidly from those glands by the contraction of associated myoepithe-
with autonomic nervous signals they ensure that the body responds to lial cells (see Figs 2.3, 2.4) that enclose the secretory units and smaller
normal physiological stimuli and adjusts to changes in the external ducts. Myoepithelial cells may be under direct neural control, as in the
environment. Hormone secretion is itself controlled in a number of salivary glands, or they may respond to circulating hormones, as in the
ways, e.g. by neural control, regulatory feedback loops or according to mammary gland, where they respond to the concentration of circulat-
various cyclical, rhythmical or pulsatile patterns of release. Endocrine ing oxytocin. | 77 | Gray's Anatomy | temp.pdf | https://archive.org/download/GraysAnatomy41E2015PDF/Grays%20Anatomy-41%20E%20%282015%29%20%5BPDF%5D.pdf | PDFPlumberTextLoader |
Subsets and Splits