Cell Recognition of Apoptotic Cells

  • Christopher A. Smith
  • Nicola J. McCarthy
  • Gwyn T. Williams
Part of the Blood Cell Biochemistry book series (BLBI, volume 5)


In recent years it has become clear that actively controlled cell death by apoptosis plays a fundamental role in many biological systems in both physiological and pathological situations (Williams et al., 1992). The specific recognition and disposal of apoptotic cells is essential to allow such cell death to occur in the closely regulated and nondisruptive fashion required in very diverse biological processes. Although this chapter focuses on mammalian cells, with particular emphasis on blood cells, other cells are also discussed where they provide useful illustrations of generally important principles.


Cell Death Apoptotic Cell Programme Cell Death Phorbol Ester Apoptotic Body 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Agarwal, S., Drysdale, B.-E., and Shin, H. S., 1988, Tumor necrosis factor mediated cytotoxicity involves ADP-ribosylation, J. Immunol. 140: 4187–4192.PubMedGoogle Scholar
  2. Alan, D. J., and Harmon, B. V., 1986, The morphologic categorization of cell death induced by mild hyperthermia and comparison with death induced by ionizing radiation and cytotoxic drugs, Scanning Electron Microsc. 1986(111):1121–1133.Google Scholar
  3. Alnemri, E. S., and Litwack, G., 1989, Glucocorticoid induced lymphocytolysis is not mediated by an induced endonuclease, J. Biol. Chem. 264: 4104–4111.PubMedGoogle Scholar
  4. Alnemri, E. S., and Litwack, G., 1990, Activation of internucleosomal DNA cleavage in human CEM lymphocytes by glucocorticoid and novobiocin, J. Biol. Chem. 265: 17323–17333.PubMedGoogle Scholar
  5. Arends, M. J., Morris, R. G., and Wyllie, A. H., 1990, Apoptosis: The role of the endonuclease, Am. J. Patho!. 136: 593–608.Google Scholar
  6. Ballard, K. J., and Holt, S. J., 1968, Cytological and cytochemical studies on cell death and digestion in the foetal rat foot: The role of macrophages and hydrolytic enzymes, J. Cell Sci. 3: 245–262.PubMedGoogle Scholar
  7. Bansal, N., Houle, A., and Melnykovych, G., 1991, Apoptosis: Mode of cell death induced in T cell leukemia lines by dexamethasone and other agents, FASEB J. 5: 211–216.PubMedGoogle Scholar
  8. Barry, M. A., Behnke, C. A., and Eastman, A., 1990, Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia, Biochem. Pharmacol. 40: 2353–2362.PubMedCrossRefGoogle Scholar
  9. Baxter, G. D., Collins, R. J., Harmon, B. V., Kumar, S., Prentice, R. L., Smith, P. J., and Lavin, M. F., 1989a, Cell death by apoptosis in acute leukemia, J. Pathol. 158: 123–129.PubMedCrossRefGoogle Scholar
  10. Baxter, G. D., Smith, P. J., and Lavin, M. F., 1989b, Molecular changes associated with induction of cell death in a human T-cell leukemia line: Putative nuclease identified as histones, Biochem. Biophys. Res. Commun. 162: 30–37.PubMedCrossRefGoogle Scholar
  11. Behnke, O., 1963, Demonstration of acid phosphatase-containing granules and cytoplasmic bodies in the epithelium of foetal rat during certain stages of differentiation, J. Cell Biol. 18: 251–265.PubMedCrossRefGoogle Scholar
  12. Bellairs, R., 1961, Cell death in chick embryos as studied by electron microscopy, J. Anat. 95: 54–60.PubMedGoogle Scholar
  13. Berger, N. A., 1985, Symposium: Cellular response to DNA damage: The role of poly(ADP-ribose), Radial. Res. 101: 4–15.CrossRefGoogle Scholar
  14. Berke, G., 1991, Lymphocyte-triggered internal target disintegration, Immunol. Today 12: 396–399.PubMedCrossRefGoogle Scholar
  15. Berridge, M. J., 1984, Inositol triphosphate and diacylglycerol as second messengers, Biochem. J. 220: 345–360.PubMedGoogle Scholar
  16. Bertazzoni, U., Scovassi, A. I., and Shall, S., 1989, Fourth European meeting on ADP-ribosylation of proteins, Pavia, Italy, 20–23 April 1989, Mutat. Res. 219: 303–307.PubMedCrossRefGoogle Scholar
  17. Bourne, H. R., Coffino, P., and Tomkins, G. M., 1975, Selection of a variant lymphoma cell deficient in adenylate cyclase, Science 187: 750–752.PubMedCrossRefGoogle Scholar
  18. Buttyan, R., Zakeri, Z., Lockshin, R., and Wolgemuth, D., 1988, Cascade induction of c fos, c-myc and heat shock 70K transcripts during regression of the rat ventral prostate gland, Mol. Endocrinol. 2: 650–657.PubMedCrossRefGoogle Scholar
  19. Buttyan, R., Olsson, C. A., Pintar, J., Chang, C., Bandyk, M., Ng, P., and Sawczuk, I. S., 1989, Induction of the TRPM-2 gene in cells undergoing programmed cell death, Mol. Cell. Biol. 9: 3473–3481.PubMedGoogle Scholar
  20. Cameron, J. A., and Fallon, J. F., 1977, The absence of cell death during development of free digits in amphibians, Dev. Biol. 55: 331–338.PubMedCrossRefGoogle Scholar
  21. Carson, D. A., Seto, S., Wasson, D. B., and Carrera, C. J., 1986, DNA strand breaks, NAD metabolism and programmed cell death, Exp. Cell Res. 164: 273–281.PubMedCrossRefGoogle Scholar
  22. Cheng, C. Y., Chern, C. L., Feng, Z. M., Marshall, A., and Bardin, C. W., 1988, Rat clusterin isolated from primary Sertoli cell enriched culture medium is sulfated glycoprotein 2 (SGP-2), Biochem. Biophys. Res. Commun. 155: 398–404.PubMedCrossRefGoogle Scholar
  23. Cleary, M. L., Smith, S. D., and Sklar, J., 1986, Cloning and structural analysis of cDNAs for bc1–2 and a hybrid be!-2/immunoglobulin transcript resulting from the t(14;18) translocation, Cell 47: 19–28.PubMedCrossRefGoogle Scholar
  24. Cohen, J. J., and Duke, R. C., 1984, Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death, J. Immunol. 132: 38–42.PubMedGoogle Scholar
  25. Collard, M. W., and Griswold, M. D., 1987, Biosynthesis and molecular cloning of sulfated glycoprotein-2 (SGP-2), Biochemistry 26: 3297–3303.PubMedCrossRefGoogle Scholar
  26. Crawford, A. M., Kerr, J. F. R., and Currie, A. R., 1972, The relationship of acute mesodermal cell death to the teratogenic effects of 7-OHM-12-MBA in the foetal rat, Br. J. Cancer 26: 498–503.PubMedCrossRefGoogle Scholar
  27. Crompton, T., 1991, IL-3-dependent cells die by apoptosis on removal of their growth factors, Growth Factors 4: 109–116.PubMedCrossRefGoogle Scholar
  28. Curren, T., Bravo, R., and Muller, R., 1985, Transient induction of cfos and c-myc is an immediate consequence of growth factor stimulation, Cancer Surveys 4: 656–681.Google Scholar
  29. Dive, C., and Hickman, J. A., 1991, Drug-target interactions: Only the first step in the commitment to a programmed cell death? Br. J. Cancer 64: 192–196.PubMedCrossRefGoogle Scholar
  30. Duke, R. C., and Cohen, J. J., 1986, IL-2 addiction: Withdrawal of growth factor activates a suicide program in dependent T cells, Lymphokine Res. 5: 289–299.PubMedGoogle Scholar
  31. Duke, R. C., Persechini, P. M., Chang, S., Liu, C.-C., Cohen, J. J., and Young, J. D.-E., 1989, Purified perforin induces target cell lysis but not DNA fragmentation, J. Exp. Med. 170: 1451–1456.PubMedCrossRefGoogle Scholar
  32. Durkacz, B. W., Omidiji, O., Gray, D. A., and Shall, S., 1980, ADP-ribose participates in DNA excision repair, Nature (London) 283: 593–596.CrossRefGoogle Scholar
  33. Duvall, E., Wyllie, A. H., and Morris, R. G., 1985, Macrophage recognition of cells undergoing programmed cell death (apoptosis), Immunology 56: 351–358.PubMedGoogle Scholar
  34. Dynan, W. S., and Tjian, R., 1985, Control of eukaryotic messenger RNA synthesis by sequence specific DNA binding proteins, Nature (London) 316: 774–778.Google Scholar
  35. Dyson, J. E. D., Simmons, D. M., Daniel, J, McLaughlin, J. M., Quirke, P., and Bird, C. C., 1986, Kinetic and physical studies of cell death induced by chemotherapeutic agents or hyperthermia, Cell Tissue Kinet. 19: 311–324.PubMedGoogle Scholar
  36. Ellis, H M, and Horvitz, H. R., 1986, Genetic control of programmed cell death in the nematode C. elegans, Cell 44: 817–829.PubMedCrossRefGoogle Scholar
  37. El-Shershaby, A. M., and Hinchliffe, J. R., 1974, Cell redundancy in the zona-intacta preimplantation mouse blastocyst: A light and electron microscope study of dead cells and their fate, J. Embryol. Exp. Morphol. 31: 643–654.PubMedGoogle Scholar
  38. Evans, R. M., 1988, The steroid and thyroid hormone receptor super family, Science 240: 889–895.PubMedCrossRefGoogle Scholar
  39. Fadok, V. A., Voelker, D. R., Campbell, B. A., and Henson, P. M., 1990, Evidence for macrophage recognition of phosphatidyl serine on apoptotic lymphocytes, J. Leukocyte Biol. Suppl. 1: 38.Google Scholar
  40. Fallon, J. F., and Cameron, J., 1977, Interdigital cell death during limb development of the turtle and lizard with an interpretation of evolutionary significance, J. Embryol. Exp. Morphol. 40: 285–289.PubMedGoogle Scholar
  41. Farbman, A. I., 1968, Electron microscope study of palate fusion in mouse embryos, Dey. Biol. 18: 93–116.CrossRefGoogle Scholar
  42. Fehsel, K., Kolb-Bachofen, V., and Kolb, H., 1991, Analysis of TNF a-induced DNA strand breaks at the single cell level, Am. J. Pathol. 139: 251–254.PubMedGoogle Scholar
  43. Fesus, L., Thomazy, V., and Falus, A., 1987, Induction and activation of tissue transglutaminase during programmed cell death, FEBS Lett. 224: 104–108.PubMedCrossRefGoogle Scholar
  44. Fesus, L., Thomazy, V., Autuori, F., Ceru, M. P., Tarcsa, E., and Piancentini, M., 1989, Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action, FEBS Lett. 245: 150–154.PubMedCrossRefGoogle Scholar
  45. Furguson, D. J. P., and Anderson, T. J., 1981, Ultrastructural observations on cell death by apoptosis in the `resting’ human breast, Virchows Arch. Pathol. Anat. 393: 193–203.Google Scholar
  46. Gaal, J. C., and Pearson, C. K., 1986, Covalent modification of proteins by ADP-ribosylation, Trends Biochem. Sci. 11: 171–175.CrossRefGoogle Scholar
  47. Gluecksohn-Schoenheimer, S., 1943, The morphological manifestations of a dominant mutation in mice affecting tail and urogenital system, Genetics 28: 341–348.PubMedGoogle Scholar
  48. Gluecksohn-Schoenheimer, S., 1949, The effect of lethal mutation responsible for duplications and twinning in mouse embryos, J. Exp. Zool. 110: 47–76.PubMedCrossRefGoogle Scholar
  49. Glücksmann, A., 1951, Cell deaths in normal vertebrate ontogeny, Biol. Rev. 26: 59–86.CrossRefGoogle Scholar
  50. Glücksmann, A., 1965, Cell death in normal development, Arch. Biol. (Liège) 76: 419–437.Google Scholar
  51. Goldsmith, M., 1966, The anatomy of cell death, J. Cell Biol. 31: 41A.Google Scholar
  52. Golstein, P., Ojcius, D. M., and Young, J. D.-E., 1991, Cell death mechanisms and the immune system, Immunol. Rev. 121: 29–65.PubMedCrossRefGoogle Scholar
  53. Goodman, G. C., Miranda, A. G., Deitch, A. D., and Tanenbaum, S. W., 1975, Action of cytochalasin D on cells of established lines. III. Zeiosis and movements at the cell surface, J. Cell Biol. 64: 644–667.CrossRefGoogle Scholar
  54. Gregory, C. D., Dive, C., Henderson, S., Smith, C. A., Williams, G. T., Gordon, J., and Rickinson, A. B., 1991, Activation of Epstein-Barr virus latent genes protects human B-cells from death by apoptosis, Nature (London) 349: 612–614.Google Scholar
  55. Grigg, J. M., Savill, J. S., Sarraf, C., Haslett, C., and Silverman, M., 1991, Neutrophil apoptosis and clearance from neonatal lungs, Lancet 338: 720–722.PubMedCrossRefGoogle Scholar
  56. Gromkowski, S. H., Brown, T. C., Masson, D., and Tschopp, J., 1988, Lack of DNA degradation in target cells lysed by granules derived from cytolytic T lymphocytes, J. Immunol. 141: 774–778.PubMedGoogle Scholar
  57. Hall, S., Savill, J. S., and Haslett, C., 1990, Fibroblast recognition of aged neutrophils is mediated by the RGD adhesion signal and is modulated by charged particles, Clin. Sci. 78: 17 p.Google Scholar
  58. Hammar, S. P., and Mottet, N. K., 1971, Tetrazolium salt and electron-microscope studies of cellular degeneration and necrosis in the interdigital areas of the developing chick limb, J. Cell Sci. 8: 229–251.PubMedGoogle Scholar
  59. Harmon, B., Bell, L., and Williams, L., 1984, An ultrastructural study on the “meconium corpuscles” in rat foetal intestinal epithelium with particular reference to apoptosis, Anat. Embryol. 169: 119–124.PubMedCrossRefGoogle Scholar
  60. Harrigan, M., Baughman, G., Campbell, N. F., and Bourgeois, S., 1989, Isolation and characterization of glucocorticoid-and cyclic AMP-induced genes in T-lymphocytes, Mol. Cell. Biol. 9: 3438–3446.PubMedGoogle Scholar
  61. Hasbold, J., and Klaus, G. G. B., 1990, Anti-immunoglobulin antibodies induce apoptosis in immature B cell lymphomas, Eur. J. Immunol. 20: 1685–1690.PubMedCrossRefGoogle Scholar
  62. Hedgecock, E. M., Sulston, J. E., and Thomson, J. N., 1983, Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans, Science 220: 1277–1279.PubMedCrossRefGoogle Scholar
  63. Henderson, S., Rowe, M., Gregory, C., Croom-Carter, D., Wang, F., Longnecker, R., Kieff, E., and Rickinson, A., 1991, Induction of bd-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death, Cell 65: 1107–1115.PubMedCrossRefGoogle Scholar
  64. Hinchliffe, J. R., and Ede, D. A., 1973, Cell death and the development of limb and skeletal pattern in normal and wingless (ws) chick embryos, J. Embryol. Exp. Morphol. 30: 753–772.PubMedGoogle Scholar
  65. Hirota, Y., Yoshioka, A., Tanaka, S., Watanabe, K., Otani, T., Minowada, J., Matsuda, A., Ueda, T., and Wataya, Y., 1989, Imbalance of deoxyribonucleoside triphosphates, DNA double strand breaks and cell death caused by 2-chlorodeoxyadenosine in mouse FM3A cells, Cancer Res. 49: 915–919.PubMedGoogle Scholar
  66. Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R. D., and Korsmeyer, S. J., 1990, Bd-2 is an inner mitochondrial membrane protein that blocks programmed cell death, Nature (London) 348: 334–336.Google Scholar
  67. Hopwood, D., and Levison, D. A., 1976, Atrophy and apoptosis in the cyclical human endometrium, J. Pathol. 119: 159–166.PubMedCrossRefGoogle Scholar
  68. Houdry, J., 1972, Effets de l’hypophysectomie et de la thyroïdectomie de la larve de Xenopus laevis D. sur le développment de son epithélium intestinal, J. Ultrastruct. Res. 39: 327–344.CrossRefGoogle Scholar
  69. Hurle, J. M., Lafarga, M., and Ojeda, J. L., 1977, Cytological and cytochemical studies of the necrotic area of the bulbus of the chick embryo heart: Phagocytosis by developing myocardial cells, J. Embryol. Exp. Morphol. 41: 161–170.PubMedGoogle Scholar
  70. Hurwitz, C., and Tolmach, L. J., 1969, Timelapse cinematographic studies of X-irradiated HeLa S3 cells I. Cell progression and cell disintegration, Biophys. J. 9: 607–633.PubMedCrossRefGoogle Scholar
  71. Itoh, N., Yonehara, S., Ishii, A., Yonehara, M., Mizushima, S.-I., Sameshima, M., Hase, A., Seto, Y., and Nagata, S., 1991, The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis, Cell 66: 233–243.PubMedCrossRefGoogle Scholar
  72. Jenkins, M. K., Pardoll, D. M., Mizuguchi, J., Chused, T. M., and Schwartz, R. H., 1987, Molecular events in the induction of a non-responsive state in interleukin 2-producing helper T-lymphocyte clones, Proc. Natl. Acad. Sci. USA 84: 5409–5413.PubMedCrossRefGoogle Scholar
  73. Jenkins, M. K., Ashwell, J. D., and Schwartz, R. H., 1988, Allogeneic non-T spleen cells restore the responsiveness of normal T-cell clones stimulated with antigen and chemically modified antigen presenting cells, J. Immunol. 140: 3324–3330.PubMedGoogle Scholar
  74. Jenkinson, E. J., Kingston, R., Smith, C. A., Williams, G. T., and Owen, J. J. T., 1989, Antigen-induced apoptosis in developing T-cells: A mechanism for negative selection of the T-cell receptor repertoire, Eur. J. Immunol. 19: 2175–2177.PubMedCrossRefGoogle Scholar
  75. Kay, M. M. B., 1975, Mechanism of removal of senescent cells by human macrophages in situ, Proc. Natl. Acad. Sci. USA 72: 3521–3525.PubMedCrossRefGoogle Scholar
  76. Kerr, J. F. R., 1965, A histochemical study of hypertrophy and ischemic injury of rat liver with special reference to changes in lysosomes, J. Pathol. Bacteriol. 90: 419–435.PubMedCrossRefGoogle Scholar
  77. Kerr, J. F. R., 1971, Shrinkage necrosis: A distinct mode of cellular death, J. Pathol. 105: 13–20.PubMedCrossRefGoogle Scholar
  78. Kerr, J. F. R., and Searle, J., 1972, A suggested explanation for the paradoxically slow growth rate of basal-cell carcinomas that contain numerous mitotic figures, 1 Pathol. 107: 41–44.Google Scholar
  79. Kerr, J. F. R., Wyllie, A. H., and Currie, A. R., 1972, Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics, Br. J. Cancer 26: 239–257.PubMedCrossRefGoogle Scholar
  80. Kerr, J. F. R., Harmon, B., and Searle, J., 1974, An electron-microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibers, J. Cell Sci. 14: 571–585.PubMedGoogle Scholar
  81. Koury, M. J., and Bondurant, M. C., 1990, Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells, Science 248: 378–381.PubMedCrossRefGoogle Scholar
  82. Krähenbühl, I. O., and Tschopp, J., 1991, Perforin-induced pore formation, Immunol. Today 12: 399–402.PubMedCrossRefGoogle Scholar
  83. Lanotte, M., Riviere, J. B., Hermouet, S., Houge, G., Vintermyr, O. K., Gjertsen, B. T., and Doskeland, S. O., 1991, Programmed cell death (apoptosis) is induced rapidly and with positive co-operativity by activation of cyclic adenosine monophosphate-kinase 1 in a myeloid leukemia cell line, J. Cell. Physiol. 146: 73–80.PubMedCrossRefGoogle Scholar
  84. Laster, S. M., Wood, J. G., and Gooding, L. R., 1988, Tumor necrosis factor can induce both apoptotic and necrotic forms of cell lysis, J. Immunol. 141: 2629–2634.PubMedGoogle Scholar
  85. Leger, J. G., Montpetit, M. L., and Tenniswood, M. P., 1987, Characterization and cloning of androgen-repressed mRNAs from rat ventral prostate, Biochem. Biophys. Res. Commun. 147: 196–203.PubMedCrossRefGoogle Scholar
  86. Levine, A. J., and Momand, J., 1990, Tumor suppressor genes: The p53 and retinoblastoma sensitivity genes and gene products, Biochim. Biophys. Acta 1032: 119–136.PubMedGoogle Scholar
  87. Liu, Y.-J., Joshua, D. E., Williams, G. T., Smith, C. A., Gordon, J. and MacLennan, I. C. M., 1989, Mechanism of antigen-driven selection in germinal centers, Nature (London) 342: 929–931.CrossRefGoogle Scholar
  88. Lockshin, R. A., and Williams, C. M., 1965, Programmed cell death I. Cytology of degeneration in the intersegmental muscles of the silkmoth, J. Insect Physiol. 11: 123–133.PubMedCrossRefGoogle Scholar
  89. Luisi, B. F., Xu, W. X., Otwinowski, Z., Freedman, L. P., Yamamoto, K. R., and Sigler, P. B., 1991, Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA, Nature (London) 352: 497–505.Google Scholar
  90. Lundin, P. M., and Schelin, U., 1965, Ultrastructure of the rat thymus, Acta Pathol. Microbiol. Scand. 65: 379–394.PubMedGoogle Scholar
  91. Martin, S. J., Lennon, S. U., Bonham, A. M., and Cotter, T. G., 1990, Induction of apoptosis (programmed cell death) in human leukemic HL-60 cells by inhibition of RNA or protein synthesis, J. Immunol. 145: 1859–1867.PubMedGoogle Scholar
  92. Matter, A., 1979, Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes, Immunology 36: 179–190.PubMedGoogle Scholar
  93. Matthiessen, M., and Andersen, H., 1972, Disintegration of the junctional epithelium of human fetal hard palate, Z. Anat. Entwicklungsgesch. 137: 153–169.PubMedCrossRefGoogle Scholar
  94. McCarthy, N. J., Smith, C. A., and Williams, G. T., 1992, Apoptosis in the development of the immune system: growth factors, clonal selection and bc1–2, Cancer Metastasis Rev. 11: 157–178.PubMedCrossRefGoogle Scholar
  95. McConkey, D. J., Hartzell, P., Duddy, S. K., Hâkansson, H., and Orrenius, S., 1988, Tetrachlorodibenzo-p-dioxin kills immature thymocytes by Ca“-mediated endonuclease activation, Science 242: 256–259.PubMedCrossRefGoogle Scholar
  96. McConkey, D. J., Nicotera, P., Hartzell, P., Bellomo, G., Wyllie, A. H., and Orrenius, S., 1989a, Glucocorticoids activate a suicide process in thymocytes through an elevation of cytosolic Ca’ concentration, Arch. Biochem. Biophys. 269: 365–370.PubMedCrossRefGoogle Scholar
  97. McConkey, D. J., Hartzell, P., Jondal, M., and Orrenius, S., 1989b, Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C, J. Biol. Chem. 264: 13399–13402.PubMedGoogle Scholar
  98. McConkey, D. J., Hartzell, P., Nicotera, P., and Orrenius, S., 1989c, Calcium-activated DNA fragmentation kills immature thymocytes, FASEB J. 3: 1843–1849.PubMedGoogle Scholar
  99. McConkey, D. J., Hartzell, P., Amador-Perez, J. F., Orrenius, S., and Jondal, M., 1989d, Calcium-dependent killing of immature thymocytes by stimulation via the CD3/T-cell receptor complex, J. Immunol. 143: 1801–1806.PubMedGoogle Scholar
  100. McConkey, D. J., Orrenius, S., and Jondal, M., 1990a, Cellular signaling in programmed cell death (apoptosis), Immunol. Today 11: 120–121.PubMedCrossRefGoogle Scholar
  101. McConkey, D. J., Hartzell, P., Chow, S. C., Orrenius, S., and Jondal, M., 1990b, Interleukin-1 inhibits T-cell receptor-mediated apoptosis in immature thymocytes, J. Biol. Chem. 265: 3009–3011.PubMedGoogle Scholar
  102. McConkey, D. J., Chow, S. C., Orrenius, S., and Jondal, M., 1990c, NK cell-induced cytotoxicity is dependent on a Ca“ increase in the target, FASEB J. 4: 2661–2664.PubMedGoogle Scholar
  103. McConkey, D. J., Orrenius, S., and Jondal, M., 1990d, Agents that elevate cAMP stimulate DNA fragmentation in thymocytes, J. Immunol. 145: 1227–1230.PubMedGoogle Scholar
  104. McDonnell, T. J., and Korsmeyer, S. J., 1991, Progression from lymphoid hyperplasia to a high-grade malignant lymphoma in mice transgenic for the t(14;18), Nature (London) 349: 254–256.Google Scholar
  105. McDonnell, T. J., Nunez, G., Platt, F. M., Hockenberry, D., London, L., McKearn, J. P., and Korsmeyer, S. J., 1990, Deregulated bcl-2-immunoglobulin transgene expands a resting but responsive immunoglobulin M and D-expressing B-Cell population, Mol. Cell. Biol. 10: 1901–1907.PubMedGoogle Scholar
  106. Menkes, B., Sandor, S., and hies, A., 1970, Cell death in teratogenesis, Adv. Teratol. 4: 169–215.Google Scholar
  107. Meyer, A. S., Schlechte, J. A., and Schmidt, T. J., 1990, Potentiation of glucocorticoid-induced cytolysis in sensitive human leukemic cells by an inhibitor of ADP-ribosylation, Leuk. Res. 14: 909–914.PubMedCrossRefGoogle Scholar
  108. Michaels, J. E., Albright, J. T., and Patt, D. I., 1971, Fine structural observations on cell death in the epidermis of the external gills of the larval frog, Rana pipiens, Am. J. Anat. 132: 301–318.PubMedCrossRefGoogle Scholar
  109. Montpetit, M. L., Lawless, K. R., and Tenniswood, M., 1986, Androgen-repressed messages in the rat ventral prostate, The Prostate 8: 25–36.PubMedCrossRefGoogle Scholar
  110. Morgan, J. L., and Curren, T., 1986, Role of ion-flux in the control of c fos expression, Nature (London) 322: 552–555.CrossRefGoogle Scholar
  111. Morris, R. G., Hargreaves, A. D., Duvall, E., and Wyllie, A. H., 1984, Hormone-induced cell death: 2. Surface charges in thymocytes undergoing apoptosis, Am. J. Pathol. 115: 426–436.PubMedGoogle Scholar
  112. Mullinger, A. M., and Johnson, R. T., 1976, Perturbation of mammalian cell division III. The topography and kinetics of extrusion subdivision, J. Cell Sci. 22: 243–285.PubMedGoogle Scholar
  113. Nelipovich, P. A., Nikonova, L. V., and Umansky, S. R., 1988, Inhibition of poly(ADP-ribose) polymerase as a possible reason for activation of Ca2+/Mg2+-dependent endonuclease in thymocytes of irradiated rats, Int. J. Radial. Biol. 53: 749–765.CrossRefGoogle Scholar
  114. Newman, S. L., Henson, J. E., and Henson, P. M., 1982, Phagocytosis of senescent neutrophile by human monocyte-derived macrophages and rabbit inflammatory macrophages, J. Exp. Med. 156: 430–442.PubMedCrossRefGoogle Scholar
  115. Nieto, M. A., and Lopez-Rivas, A., 1989, IL-2 protects T-lymphocytes from glucocorticoid induced DNA fragmentation and cell death, J. Immunol. 143: 4166–4170.PubMedGoogle Scholar
  116. Oehm, A., Behrmann, I., Falk, W., Pawlita, M., Maier, G., Klas, C., Li-Weber, M., Richards, S., Dhein, J., Trauth, B. C., Ponsting, H., and Krammer P. H., 1992, Purification and molecular cloning of the APO-1 cell surface antigen, a member of the Tumor Necrosis Factor/Nerve Growth Factor Receptor superfamily: sequence identity with the Fas antigen, J. Biol. Chem. 267: 10709–10715.PubMedGoogle Scholar
  117. Oppenheim, R. W., 1985, Naturally occurring cell death during neural development, Trends Neurosci. 8: 487–493.CrossRefGoogle Scholar
  118. Ortiz, E., 1945, The embryological development of the Wollfian and Müllerian ducts and the accessory reproductive organs of the golden hamster (Cricetus auratus), Anat. Rec. 92: 371–389.CrossRefGoogle Scholar
  119. O’Shea, J. D., Nightingale, M. G., and Chamley, W. A., 1977, Changes in small blood vessels during cyclical luteal regression in sheep, Biol. Reprod. 17: 162–177.PubMedCrossRefGoogle Scholar
  120. O’Shea, J. D., Hay, M. F., and Cran, D. G., 1978, Ultrastructural changes in the theca interna during follicular atresia in sheep, J. Reprod. Fertil. 54: 183–187.PubMedCrossRefGoogle Scholar
  121. Owens, G. P., Hahn, W. E., and Cohen, J. J., 1991, Identification of mRNAs associated with programmed cell death in immature thymocytes, Mol. Cell. Biol. 11: 4177–4188.PubMedGoogle Scholar
  122. Pautou, M. P., 1974, Evolution comparée de la nécrose morphogène interdigitale dans le pied de l’embryon de poulet et de canard, C. R. Acad. Sci., D 278: 2209–2212.Google Scholar
  123. Penfold, P. L., and Provis, J. M., 1986, Cell death in the development of the human retina: Phagocytosis of pyknotic and apoptotic bodies by retinal cells, Grade’s Arch. Clin. Exp. Opthalmol. 224: 549–553.CrossRefGoogle Scholar
  124. Potten, C. S., 1977, Extreme sensitivity of some intestinal crypt cells to X and (gamma} irradiation, Nature (London) 269: 518–521.Google Scholar
  125. Pratt, R. M., and Greene, R. M., 1976, Inhibition of palatal epithelial cell death by altered protein synthesis, Dev. Biol. 54: 135–145.PubMedCrossRefGoogle Scholar
  126. Quill, H., and Schwartz, R. H., 1987, Stimulation of normal inducer T cell clones with antigen presented by purified la molecules in planar lipid membranes: Specific induction of a long-lived state of proliferative nonresponsiveness, J. Immunol. 138: 3704–3712.PubMedGoogle Scholar
  127. Rodriguez-Tarduchy, G., and Lopez-Rivas, A., 1989, Phorbol esters inhibit apoptosis in IL-2-dependent T-lymphocytes, Biochem. Biophys. Res. Commun. 164: 1069–1075.PubMedCrossRefGoogle Scholar
  128. Rodriguez-Tarduchy, G., Collins, M., and Lopez-Rivas, A., 1990, Regulation of apoptosis in interleukin- 3-dependent hemopoietic cells by interleukin-3 and calcium ionophores, EMBO J. 9: 2997–3002.PubMedGoogle Scholar
  129. Rosoff, P. M., Savage, N., and Dinarello, C. A., 1988, Interleukin-1 stimulates diacylglycerol production in T-lymphocytes by a novel mechanism, Cell 54: 73–81.PubMedCrossRefGoogle Scholar
  130. Ruoslahti, E., and Pierschbacher, M. D., 1987, New perspectives in cell adhesion: RGD and integrins, Science 238: 491–497.PubMedCrossRefGoogle Scholar
  131. Sanderson, C. J., 1976, The mechanism of T cell mediated cytotoxicity II. Morphological studies of cell death by time-lapse microcinematography, Proc. R. Soc. London B 192: 241–255.CrossRefGoogle Scholar
  132. Sanderson, C. J., 1981, The mechanism of lymphocyte-mediated cytotoxicity, Biol. Rev. 56: 153–197.PubMedCrossRefGoogle Scholar
  133. Sandford, M. L., Searle, J. W., and Kerr, J. F. R., 1984, Successive waves of apoptosis in the rat prostate after repeated withdrawal of testosterone stimulation, Pathology 16: 406–410.PubMedCrossRefGoogle Scholar
  134. Sarraf, C. E., and Bowen, I. D., 1986, Kinetic studies on a murine sarcoma and an analysis of apoptosis, Br. J. Cancer 54: 989–998.PubMedCrossRefGoogle Scholar
  135. Saunders, J. W., Jr., 1966, Death in embryonic systems. Death of cells is the usual accompaniment of embryonic growth and differentiation, Science 154: 604–612.PubMedCrossRefGoogle Scholar
  136. Saunders, J. W., Jr., and Fallon, J. F., 1966, Cell death in morphogenesis, in Major Problems in Developmental Biology ( M. Locke, ed.), pp. 292–314, Academic Press, London.Google Scholar
  137. Saunders, J. W., Jr., Gasseling, M. T., and Saunders, L. L., 1962, Cellular death in the morphogenesis of the avian wing, Dev. Biol. 5: 147–178.PubMedCrossRefGoogle Scholar
  138. Savill, J. S., Henson, P. M., and Haslett, C. 1989a, Phagocytosis of aged human neutrophils by macrophages is mediated by a novel `charge-sensitive’ recognition mechanism, J. Clin. Invest. 84: 1518–1527.PubMedCrossRefGoogle Scholar
  139. Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., and Haslett, C., 1989b, Macrophage phagocytosis of aging neutrophils in inflammation: Programmed cell death in the neutrophil leads to its recognition by macrophages, J. Clin. Invest. 83: 865–875.PubMedCrossRefGoogle Scholar
  140. Savill, J., Dransfield, I., Hogg, N., and Haslett, C., 1990a, Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis, Nature (London) 343: 170–173.Google Scholar
  141. Savill, J., Hogg, N., and Haslett, C., 1990b, Thrombospondin and CD36 modulate macrophage vitronectin receptor (VnR)-mediated phagocytosis of neutrophils undergoing programmed cell death (apoptosis), J. Leukocyte Biol. Suppl. 1: 38.Google Scholar
  142. Schlüter, G., 1973, Ultrastructural observations on cell necrosis during formation of the neural tube in mouse embryos, Z. Anat. Entwicklungsgesch. 141: 251–264.PubMedCrossRefGoogle Scholar
  143. Schneider, E., Ralph, R. K., and Lawson, P. A., 1989, Inhibition of protein synthesis reduces the cytotoxicity of 4-(9-acridinylamino)methane-sulphon-m-aniside without affecting DNA breakage and DNA topoisomerase II in a murine mastocytoma line, Biochem. Pharmacol. 38: 263–269.PubMedCrossRefGoogle Scholar
  144. Schwartz, J. L., Morgan, W. F., Brown-Lindquist, P., Afzal, V., Wiechselbaum, R. R., and Wolff, S., 1985, Comutagenic effects of 3-aminobenzamide in Chinese hamster ovary cells, Cancer Res. 45: 1556–1559.PubMedGoogle Scholar
  145. Searle, J., Lawson, T. A., Abbott, P. J., Harmon, B., and Kerr, J. F. R., 1975, An electron-microscope study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplastic cells, J. Pathol. 116: 129–138.PubMedCrossRefGoogle Scholar
  146. Sellins, K. S., and Cohen, J. J., 1987, Gene induction by y-irradiation leads to DNA fragmentation in lymphocytes, J. Immunol. 139: 3199–3206.PubMedGoogle Scholar
  147. Sklar, M. D., 1988, The ras oncogenes increase the intrinsic resistance of NIH 3T3 cells to ionizing radiation, Science 239: 645–647.PubMedCrossRefGoogle Scholar
  148. Slingerland, J. M., Minden, M. D., and Benchimol. S., 1991, Mutation of the p53 gene in human acute myelogenous leukemia, Blood 77: 1500–1507.PubMedGoogle Scholar
  149. Smith, C. A., Williams, G. T., Kingston, R., Jenkinson, E. J., and Owen, J. J. T., 1989, Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T-cells in thymic cultures, Nature (London) 337: 181–184.Google Scholar
  150. Sodicoff, M., Pratt, N. E., and Sholley, M. M., 1974, Ultrastructural radiation injury of rat parotid gland: A histopathological dose—response study, Radial. Res. 58: 196–208.CrossRefGoogle Scholar
  151. Spivak, J. L., Pham, T., Isaacs, M., and Hankins, W. D., 1991, Erythropoietin is both a mitogen and a survival factor, Blood 77: 1228–1233.PubMedGoogle Scholar
  152. Stacey, N. H., Bishop, C. J., Halliday, J. W., Halliday, W. J., Cooksley, W. E. G., Powell, L. W., and Kerr, J. F. R., 1985, Apoptosis as the mode of cell death in antibody-dependent lymphocytotoxicity, J. Cell Sci. 74: 169–179.PubMedGoogle Scholar
  153. Strasser, A., Harris, A. W., Bath, M. L., and Cory, S., 1991, Novel primitive lymphoid tumors induced in transgenic mice by cooperation between myc and bc1–2, Nature (London) 348: 331–333.Google Scholar
  154. Sulston, J. E., and Horvitz, H. R., 1977, Postembryonic cell lineages of the nematode Caenorhabditis elegans, Dev. Biol. 56: 100–156.CrossRefGoogle Scholar
  155. Sulston, J. E., Schierenberg, E., White, J. G., and Thompson, J. E., 1983, The embryonic cell lineage of the nematode Caenorhabditis elegans, Dev. Biol. 100: 64–119.PubMedCrossRefGoogle Scholar
  156. Swartzendruber, D. C., and Congdon, C. C., 1963, Electron microscope observations on tingible body macrophages in mouse spleen, J. Cell Biol. 19: 641–646.PubMedCrossRefGoogle Scholar
  157. Tanaka, Y., Yashihara, K., Itaya, A., Kamiya, T., and Koide, S. S., 1984, Mechanism of the inhibition of Cat+, Mg2+-dependent endonuclease of bull seminal plasma induced by ADP-ribosylation, J. Biol. Chem. 259: 6579–6585.PubMedGoogle Scholar
  158. Tata, J. R., 1966, Requirement for RNA and protein synthesis for induced regression of the tadpole tail in organ culture, Dev. Biol. 13: 77–94.PubMedCrossRefGoogle Scholar
  159. Tomei, L. D., Noyes, I., Blocker, D., Holliday, J., and Glaser, R., 1987, Phorbol ester and Epstein-Barr virus dependent transformation of normal primary human skin epithelial cells, Nature (London) 329: 73–75.Google Scholar
  160. Tomei, L. D., Kanter, P., and Wenner, C. E., 1988, Inhibition of radiation-induced apoptosis in vitro by tumor promoters, Biochem. Biophys. Res. Commun. 155: 324–331.PubMedCrossRefGoogle Scholar
  161. Trauth, B. C., Klas, C., Peters, A. M. J., Matzku, S., Möller, P., Falk, W., Debatin, K.-M., and Krammer, P. H., 1989, Monoclonal antibody-mediated tumor regression by induction of apoptosis, Science 245: 301–305.PubMedCrossRefGoogle Scholar
  162. Truman, J. W., 1984, Cell death in invertebrate nervous systems, Annu. Rev. Neurosci. 7: 171–188.PubMedCrossRefGoogle Scholar
  163. Truman, J. W., and Schwartz, L. M., 1982, Programmed death in the nervous system of a moth, Trends Neurosci. 5: 270–273.CrossRefGoogle Scholar
  164. Tsujimoto, Y., 1989, Stress resistance conferred by high level of bc1–2 a protein in human ß-lymphoblastoid cell, Oncogene 4: 1331–1336.PubMedGoogle Scholar
  165. Tsujimoto, Y., and Croce, C. M., 1988, Recent progress on the human bcl-2 gene involved in follicular lymphoma: Characterization of the protein products, Curr. Top. Microbiol. Immunol. 141: 337–340.PubMedCrossRefGoogle Scholar
  166. Tsujimoto, Y., Finger, L. R., Yunis, J., Nowell, P. C., and Croce, C. M., 1984, Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation, Science 226: 1097–1099.PubMedCrossRefGoogle Scholar
  167. Ucker, D., 1991, Death by suicide: One way to go in mammalian cellular development, The New Biol. 3: 103–109.Google Scholar
  168. Ucker, D. S., Ashwell, J. D., and Nickas, G. 1989, Activation driven T-cell death. Requirements for de novo transcription and translation and association with genome fragmentation, J. Immunol. 143: 3461–3469.PubMedGoogle Scholar
  169. Vaux, D. L., Cory, S., and Adams, J. M., 1988, Bc1–2 gene promotes hemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells, Nature (London) 335: 440–442.Google Scholar
  170. Vedeckis, W. V., and Bradshaw, H. D., 1983, DNA fragmentation in S49 lymphoma cells killed with glucocorticoids and other agents, Mol. Cell. Endocrinol. 30: 215–227.PubMedCrossRefGoogle Scholar
  171. Walker, N. I., Bennett, R. E., and Kerr, J. F. R., 1989, Cell death by apoptosis during involution of the lactating breast in mice and rats, Am. J. Anat. 185: 19–32.PubMedCrossRefGoogle Scholar
  172. Weber, R., 1964, Ultrastructural changes in regressing tail muscles of Xenopus larvae at metamorphosis, J. Cell Biol. 22: 481–487.PubMedCrossRefGoogle Scholar
  173. Webster, D. A., and Gross, J., 1970, Studies on possible mechanisms of programmed cell death in the chick embryo, Dev. Biol. 22: 157–184.PubMedCrossRefGoogle Scholar
  174. Weedon, D., Searle, J., and Kerr, J. F. R., 1979, Apoptosis. Its nature and implications for dermatopathology, Am. J. Dermatopathol. 1: 133–144.PubMedCrossRefGoogle Scholar
  175. Whetton, A. D., Bazill, G. W., and Dexter, T. M., 1984, Haemopoietic cell growth factor mediates cell survival via its action on glucose transport, EMBO J. 3: 409–413.PubMedGoogle Scholar
  176. Whetton, A. D., Heyworth, C. M., and Dexter, T. M., 1986a, Phorbol esters activate protein kinase C and glucose transport and can replace the requirement for growth factor in interleukin-3-dependent multipotent stem cells, J. Cell Sci. 84: 93–104.PubMedGoogle Scholar
  177. Whetton, A. D., Monk, P. N., Consalvey, S. D., and Downes, C. P., 1986b, The haemopoietic growth factors interleukin 3 and colony stimulating factor-1 stimulate proliferation but do not induce inositol lipid breakdown in murine bone marrow derived macrophages, EMBO J. 5: 3281–3286.PubMedGoogle Scholar
  178. Wielckens, K., and Delfs, T., 1986, Glucocorticoid-induced cell death and poly[adenosine diphosphate (ADP)-ribosyl]ation: Increased toxicity of dexamethasone on mouse 549.1 lymphoma cells with the poly(ADP-ribosyl)ation inhibitor benzamide, Endocrinology 119: 2383–2392.PubMedCrossRefGoogle Scholar
  179. Wielckens, K., Delfs, T., Muth, A., Freese, V., and Kleeberg, H. J., 1987, Glucocorticoid-induced lymphoma cell death: The good and evil, J. Steroid Biochem. 27: 413–419.PubMedCrossRefGoogle Scholar
  180. Wielckens, K., Bittner, S., and Delfs, T., 1989, Mechanisms of glucocorticoid-induced growth inhibition and cell lysis in mouse lymphoma cells Haematol. Bluttransfus. 32: 226–232.Google Scholar
  181. Williams, G. T., 1991, Programmed cell death: Apoptosis and oncogenesis, Cell 65: 1097–1098.PubMedCrossRefGoogle Scholar
  182. Williams, G. T., and Johnstone, A. P., 1983, ADP-ribosyl transferase, rearrangement of DNA and cell differentiation, Biosci. Rep. 3: 815–830.PubMedCrossRefGoogle Scholar
  183. Williams, G. T., Smith, C. A., Spooncer, E., Dexter, T. M., and Taylor, D. R., 1990, Hemopoietic colony stimulating factors promote cell survival by suppressing apoptosis, Nature (London) 343: 76–79.Google Scholar
  184. Williams, G. T., Smith, C. A., McCarthy, N. J., and Grimes, E. A., 1992, Apoptosis: final control point in cell biology, Trends Cell Biol. 2: 263–267.PubMedCrossRefGoogle Scholar
  185. Wyllie, A. H., 1980, Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation, Nature (London) 284: 555–556.Google Scholar
  186. Wyllie, A. H., 1981, Cell death: A new classification separating apoptosis from necrosis, in Cell Death in Biology and Pathology (I. D. Bowen and R. A. Locksin, eds.), pp. 9–34, Chapman and Hall, London. Wyllie, A. H., 1987, Apoptosis: Cell death in tissue regulation, J. Pathol. 153: 313–316.Google Scholar
  187. Wyllie, A. H., and Morris, R. G., 1982, Hormone-induced cell death: Purification and properties of thymocytes undergoing apoptosis after glucocorticoid treatment, Am. J. Pathol. 109: 78–87.PubMedGoogle Scholar
  188. Wyllie, A. H., Kerr, J. F. K., and Currie, A. R., 1972, Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics, Br. J. Cancer 26: 239–257.PubMedCrossRefGoogle Scholar
  189. Wyllie, A. H., Kerr, J. F. R., and Currie, A. R., 1973a, Cell death in the normal neonatal rat adrenal cortex, J Pathol. 111: 255–261.PubMedCrossRefGoogle Scholar
  190. Wyllie, A. H., Kerr, J. F. R., Macaskill, I. A. M., and Currie, A. R., 1973b, Adrenocortical cell deletion: The role of ACTH, J. Pathol. 111: 85–94.PubMedCrossRefGoogle Scholar
  191. Wyllie, A. H., Kerr, J. F. R., and Currie, A. R., 1980, Cell death: The significance of apoptosis, Int. Rev. Cytol. 68: 251–306.PubMedCrossRefGoogle Scholar
  192. Wyllie, A. H., Beattie, G. J., and Hargreaves, A. D., 1981, Chromatin changes in apoptosis, Histochem. J. 13: 681–692.PubMedCrossRefGoogle Scholar
  193. Wyllie, A. H., Morris, R. G., Smith, A. L., and Dunlop, D., 1984, Chromatin cleavage in apoptosis: Association with condensed chromatin morphology and dependence on macromolecular synthesis, J. Pathol. 142: 67–77.PubMedCrossRefGoogle Scholar
  194. Wyllie, A. H., Rose, K. A., Morris, R. G., Steel, C. M., Foster, E., and Spandidos, D. A., 1987, Rodent fibroblast tumours expressing human myc and ras genes: Growth, metastasis and endogenous oncogene expression, Br. J. Cancer 56: 251–259.PubMedCrossRefGoogle Scholar
  195. Yamada, T., and Ohyama, H., 1988, Radiation-induced interphase death of rat thymocytes is internally programmed (apoptosis), Int. J. Radial. Biol. 53: 65–75.CrossRefGoogle Scholar
  196. Yamamoto, K. R., 1985, Steroid receptor regulated transcription of specific genes and gene networks, Annu. Rev. Genet. 19: 209–252.PubMedCrossRefGoogle Scholar
  197. Yonish-Rouach, E., Resnitzky, D., Lotem, J., Sachs, L., Kimchi, A., and Oren, M., 1991, Wild-type p53 induces apoptosis of myeloid leukemic cells that is inhibited by interleukin 6, Nature (London) 352: 345–347.Google Scholar
  198. Yoshimasa, T., Sibley, D. R., Bouvier, M., Lelkowitz, R. J., and Caron, M. G., 1987, Cross-talk between cellular signaling pathways suggested by phorbol-ester-induced adenylate cyclase phosphorylation, Nature (London) 327: 67–70.Google Scholar
  199. Young, J. D.-E., and Liu, C. C., 1988, Multiple mechanisms of lymphocyte mediated killing, Immunol. Today 9: 140–144.PubMedCrossRefGoogle Scholar
  200. Yuan, J., and Horvitz, H. R., 1990, The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death, Dey. Biol. 138: 33–41.CrossRefGoogle Scholar
  201. Zwilling, E., 1942, The development of the dominant rumplessness in chick embryos, Genetics 27: 641–656.PubMedGoogle Scholar
  202. Zwilling, E., 1945, The embryology of recessive rumpless condition of chickens, I. Exp. Zool. 99: 79–91.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Christopher A. Smith
    • 1
  • Nicola J. McCarthy
    • 1
  • Gwyn T. Williams
    • 1
  1. 1.Department of AnatomyUniversity of Birmingham Medical SchoolBirminghamUK

Personalised recommendations