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The Kinetic Organisation of Tissues

  • B. Ansari
  • P. A. Hall

Abstract

It is clear that there are significant advantages in an organism being multicellular, in particular as a consequence of increased specialisation of its component parts. The cost of this lies in the considerable investment in the molecular and cellular machinery required to regulate the organisation of the cells that make up metazoa. For example, in normal tissues of metazoan organisms the number of cells with any particular phenotype is very carefully controlled (Hall and Watt 1989a; Hall 1989). In the development of an organism from a fertilised egg there are three key requirements. First, a carefully regulated increase in cell numbers coupled with, second, the differentiation of the appropriate cell types which are, thirdly, arranged in the appropriate spatial organisation. In the adult organism there remains a continuing need to carefully define cell numbers and phenotypes and to form these cells into highly ordered tissues with characteristic spatial and kinetic organisation (see for example Wright and Alison 1984). This is, in part, determined by the proliferative activity of progenitor cell populations within these tissues, but also by the number of growth-arrested cells, loss of cells into terminally differentiated populations and by programmed cell death or apoptosis. The ordered aggregates of cells that form tissues are homeostatically regulated and are capable of responding to diverse insults, with the maintenance of tissue integrity. The balance between proliferative and non-proliferative behaviour is very carefully regulated, there being genes involved in growth arrest as well as the better characterised genes involved in mitogenesis. Many aspects of pathology derive from alterations in the regulation of these processes. Consequently an understanding of regulation of cell numbers and the control of differentiation in these cells is central to our understanding of normal development, adult tissues and the pathological processes that affect them.

Keywords

Stem Cell Programme Cell Death Haemopoietic Stem Cell Proliferative Compartment Outer Root Sheath Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abramson S, Miller RG and Phillips RA (1977) The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med 45:1567–1579Google Scholar
  2. Alberts B, Bray D, Lewis J, Raff M, Roberts K and Watson JD (eds) (1989) Molecular biology of the cell. Garland Publishing Inc., New YorkGoogle Scholar
  3. Ambros V and Horwitz HR (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 266:409–416Google Scholar
  4. Ambros V and Horwitz HR (1987) The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific post-embryonic developmental events. Genes Dev 1:398–414PubMedGoogle Scholar
  5. Arends MJ, Morris RG and Wyllie AH (1990) Apoptosis: The role of endonuclease. Am J Pathol 136: 593–608PubMedGoogle Scholar
  6. Avery L and Horwitz HR (1987) A cell that dies during wild-type C. elegans development can function as a neuron in aced-3 mutant. Cell 51:1071–1078PubMedGoogle Scholar
  7. Bargiello TA, Saez L, Baylies MK, Gasic G, Young MW and Spray DC (1987) The Drosophila clock gene per affects intercellular junctional communication. Nature 328:686–691PubMedGoogle Scholar
  8. Barrandon Y, Morgan JR, Muligan RC and Green H (1989) Restoration of growth potential in paraclones of human keratinocytes by a viral oncogene. Proc Natl Acad Sci (USA) 86: 4102–4106Google Scholar
  9. Bearpark AD and Gordon MY (1989) Adhesive properties distinguish subpopulations of haemopoietic stem cells with different spleen colony forming and marrow repopulating capacities. Bone Marrow Transplant 4:625–628PubMedGoogle Scholar
  10. Bissell MJ, Hall GH and Parry G (1982) How does the extracellular matrix direct gene expression? J Theor Biol 99:31–68PubMedGoogle Scholar
  11. Bissonette R, Lee M-J and Wang E (1990) The differentiation process of intestinal epithelial cells is associated with the appearance of statin, a non-proliferation specific nuclear protein. J Cell Sci 95:247Google Scholar
  12. Bjerknes M, Cheng H and Erlandsen S (1985) Functional gap junctions in mouse small intestinal crypts. Anat Rec 212:364–367PubMedGoogle Scholar
  13. Blau HM and Baltimore D (1991) Differentiation requires continuous regulation. J Cell Biol 112:781–783PubMedGoogle Scholar
  14. Blau HM, Pavlath GK and Hardeman EC et al. (1985) Plasticity of the differentiated state. Science 230:758–766PubMedGoogle Scholar
  15. Cairns J (1975) Mutation selection and the natural history of cancer. Nature 255:197–200PubMedGoogle Scholar
  16. Cheng H, Bjerknes M, Amar J and Gardiner G (1986) Crypt production in normal and diseased human colonic epithelium. Anat Rec 216:44–48PubMedGoogle Scholar
  17. Chwalinski S, Potten CS and Evans G (1988) Double labelling with bromodeoxyuridine and 3H-thymidine of proliferative cells in small intestinal epithelium in the steady state and after irradiation. Cell Tissue Kinet 21:317–329PubMedGoogle Scholar
  18. Ciccarrelli C, Philipson L and Sorrentino V (1990) Regulation of growth arrest-specific genes in mouse fibroblasts. Mol Cell Biol 10:1525–1529Google Scholar
  19. Clausen OPF, Aarnaes E, Kirkhus B, Pedersen S, Thorud E and Bolund L (1984) Subpopulations of slowly cycling cells in S and G2 phase in mouse epidermis. Cell Tissue Kinet 17:351–365PubMedGoogle Scholar
  20. Cotsarelis G, Cheng S-Z, Dong G, Sun T-T and Lavker RM (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57:201–209PubMedGoogle Scholar
  21. Cotsarelis G, Sun T-T and Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle and skin carcinogenesis. Cell 61:1329–1337PubMedGoogle Scholar
  22. Curry JL and Trentin J J (1967) Haemopoietic spleen colony studies. I. Growth and differentiation. Dev Biol 15:395–413PubMedGoogle Scholar
  23. Dexter TM and White H (1990) Growth without inflation. Nature 24:380–381Google Scholar
  24. Dick JE, Magli MC, Huszar D, Phillips RA and Bernstein A (1985) Introduction of a selectable gene into primitive stem cells of long-term reconstitution of the hemopoietic system of W/W v mice. Cell 42:71–79PubMedGoogle Scholar
  25. Eastman A (1990) Activation of programmed cell death by anticancer agents: Cisplatin as a model system. Cancer Cells 2:275–280PubMedGoogle Scholar
  26. Elgjo K, Reichelt KL, Hennings H, Michael D and Yuspa SH (1986) Purified epidermal pentapetide inhibits proliferation and enhances terminal differentiation in cultured mouse epidermal cells. J Invest Dermatol 87:555–558PubMedGoogle Scholar
  27. Ellis HM and Horvitz HR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817–829PubMedGoogle Scholar
  28. Evarts RP, Nagy P, Marsden E and Thorgeirsson SS (1987) A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 8:1737–1740PubMedGoogle Scholar
  29. Fraser SE, Green CR, Bode HR and Gilula NB (1987) Selective disruption of gap junctional communication interferes with patterning process in Hydra. Science 237:49–55PubMedGoogle Scholar
  30. Gallico III GG, O’Connor NE, Compton CC, Kehinde O and Green H (1984) Permanent coverage of large skin wounds with autologus cultured human epithelium. N Engl J Med 311:448–451PubMedGoogle Scholar
  31. Germain L, Noel M, Gourdeau H and Marceau N (1988) Promotion of growth and differentiation of rat ductular oval cells in primary culture. Cancer Res 48:368–378PubMedGoogle Scholar
  32. Gilbert SF (1989) Developmental biology, 2nd edn. Sinauer Asociates Inc., Sunderland, MA, USAGoogle Scholar
  33. Glücksmann A (1950) Cell deaths in normal vertebrate ontogeny. Biol Rev 26: 59–86Google Scholar
  34. Glücksmann A and Spear FG (1945) The quantitative and qualitative histological examination of biopsy material from patients treated by radiation for carcinoma of the cervix uteri. Br J Radiol 18:313–322Google Scholar
  35. Glücksmann A and Way S (1948) On the choice of treatment of individual carcinomas of the cervix based on the analysis of serial biopsies. Br J Obstet Gynaecol 55:573–582Google Scholar
  36. Gordon MY (1988a) Adhesive properties of haemopoietic stem cells. Br J Haematol 68:149–151PubMedGoogle Scholar
  37. Gordon MY (1988b) Extracellular matrix of the marrow microenvironment. Br J Haematol 70:1–4PubMedGoogle Scholar
  38. Gordon MY, Riley GP and Greaves MF (1987) Plastic adherent progenitor cells in human bone marrow. Exp Haematol 15:772–778Google Scholar
  39. Graham GJ, Wright EG and Hewick R et al. (1990) Identification and characterisation of an inhibitor of haemopoietic stem cell proliferation. Nature 344:442–444PubMedGoogle Scholar
  40. Greaves MF (1986) Differentiation linked leukaemogenesis in lymphocytes. Science 234:697–704PubMedGoogle Scholar
  41. Griffiths DFR, Davies SJ, Williams D, Williams GT and Williams ED (1988) Demonstration of somatic mutation and colonic crypt clonality by X-linked enzyme histochemistry. Nature 333:461–463PubMedGoogle Scholar
  42. Hall PA (1989) What are stem cells and how are they controlled? J Pathol 158:275–277PubMedGoogle Scholar
  43. Hall PA (1990) Clonogenic human epidermal keratinocytes have differing adhesive properties which correlate with other functional properties. J Pathol 161:350aGoogle Scholar
  44. Hall PA (1991) Differentiation, stem cells and tumour histogenesis. In: MacSween RNM and Anthony PP (eds) Recent advances in histopathology, vol 15. Churchill Livingstone, EdinburghGoogle Scholar
  45. Hall PA and Levison DA (1990) Assessment of cell proliferation in histological material. J Clin Pathol 43:184–192PubMedGoogle Scholar
  46. Hall PA and Watt FM (1989a) Stem cells: the generation and maintenance of cellular diversity. Development 106:619–633PubMedGoogle Scholar
  47. Hall PA and Watt FM (1989b) Functional characterisation of a stem cell population from cultured human keratinocytes. J Pathol 157: 172aGoogle Scholar
  48. Hall PA and Woods AL (1990) Immunohistological markers of cell proliferation. Cell Tissue Kinet 23:531–549Google Scholar
  49. Hart IK, Richardson WD, Heldin C-H, Westermark B and Raff MC (1989) PDGF receptors on cells of the oligodendrocyte-type 2 astrocyte (0–2A) cell lineage. Development 105:595–603PubMedGoogle Scholar
  50. Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK and Allshire RC (1990) Telomere reduction in human colorectal carcinoma and with aging. Nature 346:866–868PubMedGoogle Scholar
  51. Hockenbury D, Nunez G, Milliman C, Schreiber RD and Korsmeyer SJ (1990) bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334–336Google Scholar
  52. Hughes SM, Lillien LE, Raff MC, Rohrer H and Sendtner M (1988) Ciliary neurotrophic factor induces type-2 astrocyte differentiation in culture. Nature 335:70–73PubMedGoogle Scholar
  53. Hume WJ and Thompson J (1990) Double labelling of cells with tritiated thymidine and bromodeoxyuridine reveals a circadian rhythm-dependent variation in duration of DNA synthesis and S phase flux rates in rodent oral epithelium. Cell Tissue Kinet 23:313–323PubMedGoogle Scholar
  54. Ijiri K and Potten CS (1981) Cell death in cell hierarchies in adult mammalian tissues. In: Potten CS (ed) Perspectives on mammalian cell death. Oxford University Press, OxfordGoogle Scholar
  55. Jhappen C, Stahle C, Harkins RN, Fausto N, Smith GH and Merlino GT (1990) TGFα overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61:1137–1146Google Scholar
  56. Johnson GR and Metcalf M (1977) Pure and mixed erythroid colony formation in vitro stimulated by spleen conditioned medium with no detectable erythropoietin. Proc Natl Acad Sci (USA) 74:3879–3882Google Scholar
  57. Kam E, Watt FM and Pitts JD (1987) Patterns of junctional communication in skin: studies on cultured keratinocytes. Exp Cell Res 173:431–438PubMedGoogle Scholar
  58. Kerk DK, Henry EA, Eaves AC and Eaves CJ (1985) Two classes of primitive pluripotent haemopoietic progenitor cells: separation by adherence. J Cell Physiol 125:127–134PubMedGoogle Scholar
  59. Kinzler KW, Milbert MC and Vogelstein B et al. (1991) Identification of a gene located at chromosome 5q21 that is mutated in colorectal carcinomas. Science 251:1366–1370PubMedGoogle Scholar
  60. Kirkland SC (1988) Clonal origin of columnar, mucous and endocrine cell lineages in human colorectal epithelium. Cancer 61:1359–1363PubMedGoogle Scholar
  61. Laiho M, DeCaprio JA, Ludlow JW, Livingston DM and Massague J (1990) Growth inhibition by TGFp linked to suppression of retinoblastoma protein phosphorylation. Cell 62:175–185PubMedGoogle Scholar
  62. Leblond CP (1964) Classification of cell populations on the basis of their proliferative behaviour. J Natl Cancer Inst Monogr 14:119–148Google Scholar
  63. Leger JG, Montpetit ML, Tenniswood MP (1987) Characterisation and cloning of androgenrepressed mRNAs from rat ventral prostate. Biochem Biophys Res Comm 147:196–203PubMedGoogle Scholar
  64. Lemischka IR, Raulet DH and Mulligan RC (1986) Developmental potential and dynamic behaviour of haematopoietic stem cells. Cell 45:917–927PubMedGoogle Scholar
  65. Lendahl U, Zimmerman LB and McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595PubMedGoogle Scholar
  66. Lenoir M-C, Bernafd BA, Pautrat G, Darmon M and Shroo B (1988) Outer root sheath cells of human hair follicle are able to regenerate a fully differentiated epidermis in vitro. Dev Biol 130:610–620PubMedGoogle Scholar
  67. Manfioletti G, Ruaro ME, Del Sal G, Philipson L and Schneider C (1990) A growth arrest-specific gene (gas) codes for a membrane protein. Mol Cell Biol 10:2924–2930PubMedGoogle Scholar
  68. Marceau N, Blouin M-J, Germain L and Noel M (1989) Role of different epithelial cell types in liver ontogenesis, regeneration and neoplasia. In Vitro Cell Dev Biol 25:336–341Google Scholar
  69. McClung CR, Fox BA and Dunlap JC (1989) The Neurospora clock gene frequency shares an element with the Drospophila clock gene period. Nature 339:558–562PubMedGoogle Scholar
  70. McConkey DJ, Orrenius S and Jondal M (1990) Cellular signalling in programmed cell death (apoptosis). Immunol Today 11:120–121PubMedGoogle Scholar
  71. Metcalf D (1989) The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature 339:27–30PubMedGoogle Scholar
  72. Moses HL, Yang EY and Pietenpol J A (1990) TGFp stimulator and inhibitor of cell proliferation: new mechanistic insights. Cell 63:245–247PubMedGoogle Scholar
  73. Muller-Sieberg CE, Townsend K, Weissman IL and Rennick D (1989) Proliferation and differentiation of highly enriched mouse haematopoietic stem cells and progenitor cells in response to defined growth factors. J Exp Med 167:1825–1840Google Scholar
  74. Muller R, Laucke R, Trimper B and Cossel L (1990) Pancreatic cell proliferation in normal rats studied by in vivo autoradiography with 3H-thymidine. Virchows Archiv 59:133–136PubMedGoogle Scholar
  75. Nuell MJ, Stewart DA and Walker L et al. (1991) Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol Cell Biol 11:1372–1381PubMedGoogle Scholar
  76. Parkinson EK and Balmain A (1990) Chalones revisited a possible role for transforming growth factor beta in tumour promotion. Carcinogenesis 11:195–198PubMedGoogle Scholar
  77. Pearse AGE (1984) Islet development and the APUD concept. In: Kloppel G and Heitz PU (eds) Pancreatic pathology. Churchill Livingstone, Edinburgh, pp 125–132Google Scholar
  78. Pierce GB, Speers WC (1989) Tumours as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res 48:1996–2004Google Scholar
  79. Ponder BAJ, Schmidt GH, Wilkinson MM, Wood MJ, Monk M and Reid A (1985) Derivation of mouse intestinal crypts from single progenitor cells. Nature 313:689–691PubMedGoogle Scholar
  80. Potten CS (1981) Cell replacement in epidermis (Keratopoiesis) via discrete units of proliferation. Int Rev Cytol 69:271–318PubMedGoogle Scholar
  81. Potten CS and Loeffler M (1987) A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol 127:381–391PubMedGoogle Scholar
  82. Potten CS and Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110:1001–1020PubMedGoogle Scholar
  83. Potten CS, Hume WJ, Reid P and Cairns J (1978) The segregation of DNA in epithelial stem cells. Cell 15:899–906PubMedGoogle Scholar
  84. Potter VR (1978) Phenotypic diversity in experimental hepatomas: the concept of partially blocked ontogeny. Br J Cancer 38:1–23PubMedGoogle Scholar
  85. Price J (1987) Retroviruses and the study of cell lineage. Development 101:409–420PubMedGoogle Scholar
  86. Raff MC, Abney ER and Fok-Seang J (1985) Reconstitution of a developmental clock in vitro: a critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell 42:61–69PubMedGoogle Scholar
  87. Raff MC, Lillien LE, Richardson WD, Burne JF and Noble MD (1988) Platelet derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature 333:562–565PubMedGoogle Scholar
  88. Rao MS, Yeldandi AV and Reddy JK (1990) Differentiation and cell proliferation patterns in rat exocrine pancreas: role of type 1 and type 2 injury. Pathobiology 58:37–43PubMedGoogle Scholar
  89. Reid LM (1990) Stem cell biology, hormone/matrix synergies and liver differentiation. Curr Opin Cell Biol 2:121–130PubMedGoogle Scholar
  90. Roberts AB and Sporn MB (1988) Transforming growth factor β. Adv Cancer Res 51:107–145PubMedGoogle Scholar
  91. Roberts RA, Spooncer E, Parkinson EK, Lord TI, Allen TD, Dexter TM (1987) Metabolically inactive 3T3 cells can substitute for marrow stromal cells to promote the proliferation and differentiation of multipotent haemopoietic stem cells. J Cell Physiol 132:203–214PubMedGoogle Scholar
  92. Roberts RA, Gallagher J, Spooncer E, Allen TD, Bloomfield F and Dexter TM (1988) Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature 332:376–378PubMedGoogle Scholar
  93. Ruoslahti E and Yamaglichi Y (1991) Proteoglycans as modulators of growth factor activities. Cell 64:867–869PubMedGoogle Scholar
  94. Ruvkun G and Giousto J (1989) TheCaenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature 338:313–320PubMedGoogle Scholar
  95. Sandgren EP, Quaife CJ. Paulovich AG, Palmiter RD and Brinster RL (1991) Pancreatic tumour pathogenesis reflects the causative genetic lesion. Proc Natl Acad Sci (USA) 88:93–97Google Scholar
  96. Sanes JR (1989) Analysing cell lineage with recombinant retrovirus. Trends Neurol Sci 12:21–28Google Scholar
  97. Saunders JW (1966) Death in embryonic systems. Science 154:604–612PubMedGoogle Scholar
  98. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM and Haslett C (1989) Macrophage phagocytosis of ageing neutrophils in inflammation. J Clin Invest 83:865–875PubMedGoogle Scholar
  99. Savill J, Dransfield I, Hogg N and Haslett C (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170–173PubMedGoogle Scholar
  100. Schneider C, King RM and Philipson L (1988) Genes specifically expressed at growth arrest in mammalian cells. Cell 54:787–793PubMedGoogle Scholar
  101. Schofield R (1978) The relationship between the spleen-colony forming cell and the haemopoietic stem cell. Blood Cells 4:7–35PubMedGoogle Scholar
  102. Schwartz LM, Kosz L and Kay BK (1990) Gene activation is required for developmentally programmed cell death. Proc Natl Acad Sci (USA) 87:6594–6598Google Scholar
  103. Sell S (1990) Is there a liver stem cell? Cancer Res 50:3811–3815PubMedGoogle Scholar
  104. Sporn MB and Roberts AB (1988) Peptide growth factors are multifunctional. Nature 332:217–219PubMedGoogle Scholar
  105. Steel GG (1967) Cell loss factor in the growth of human tumours. Eur J Cancer 30:381–390Google Scholar
  106. Steel GG (1977) The kinetics of tumours. Oxford University Press, OxfordGoogle Scholar
  107. Suda T, Suda J and Ogawa M (1984) Disparate differentiation in mouse haemopoietic colonies derived from paired progenitors. Proc Natl Acad Sci (USA) 81:2520–2524Google Scholar
  108. Temple S and Raff MC (1986) Clonal analysis of oligodendrocyte development in culture: evidence for a clock that counts cell divisions. Cell 44:773–779PubMedGoogle Scholar
  109. Thompson EM, Fleming KA, Evans DJ, Fundele R, Surani MA and Wright NA (1990) Gastric endocrine cells share a clonal origin with other gut cell lineages. Development 110:477–481PubMedGoogle Scholar
  110. Till JE and McCulloch EA (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14:213–222PubMedGoogle Scholar
  111. Trauth BC, Klas C and Peters AMJ et al. (1989) Monoclonal antibody-mediated tumour regression by induction of apoptosis. Science 245:301–304PubMedGoogle Scholar
  112. von Wangenheim K-H (1987) Cell death through differentiation. Potential immortality of somatic cells: a failure in control of differentiation. In: Potten CS (ed) Perspectives on mammalian cell death. Oxford University Press, Oxford.Google Scholar
  113. Wang E (1985) A 57000mol-wt protein uniquely present in non-proliferating cells and senescent human fibroblasts. J Cell Biol 100:545–559PubMedGoogle Scholar
  114. Wang E and Kreuger JG (1985) Application of a unique monoclonal, jitibody as a marker for non-proliferating subpopulations of cells in some tissues. J Histochem Cytochem 33:587PubMedGoogle Scholar
  115. Weinberg DS (1989) The role of cell-cycle activity in the generation of morphologic heterogeneity in non-Hodgkin’s lymphoma. Am J Pathol 135:759–770PubMedGoogle Scholar
  116. Western H and Bainton DF (1979) Association of alkaline phosphatase positive reticulum cells in bone marrow with granulocytic precursors. J Exp Med 150:919–937Google Scholar
  117. Wilson EB (1895) The cell in development and in heredity, 1st edn. Macmillan, New YorkGoogle Scholar
  118. Winton DJ, Blout MA and Ponder BAJ (1988) A clonal marker induced by mutation in mouse intestinal epithelium. Nature 333:463–466PubMedGoogle Scholar
  119. Withers HR (1967) The dose-response relationship for irradiation of epithelial cells of mouse skin. Br J Radiol 40:187–194PubMedGoogle Scholar
  120. Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25:1–47PubMedGoogle Scholar
  121. Wright NA and Alison M (1984) The biology of epithelial cell populations. Oxford University Press, OxfordGoogle Scholar
  122. Wyllie AH (1980) Glucocorticoid induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556PubMedGoogle Scholar
  123. Wyllie AH and Morris RG (1982) Hormone-induced cell death: purification and properties of thymocytes undergoing apoptosis after glucocorticoid treatment. Am J Pathol 109:78–87PubMedGoogle Scholar
  124. Wyllie AH, Morris RG, Smith AL and Dunlop D (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142:67–77PubMedGoogle Scholar
  125. Yuan J and Horwitz HR (1990) The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev Biol 138:33–41PubMedGoogle Scholar
  126. Zajicek G, Yagh C and Michaeli Y (1985) The streaming submandibular gland. Anat Rec 213: 150–158PubMedGoogle Scholar
  127. Zajicek G, Bartfield E, Schwartz-Arad D and Michaeli Y (1987) Computerised extraction of the time dimension in histopathological sections. Appl Optics 26:3408–3412Google Scholar

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  • B. Ansari
  • P. A. Hall

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