Skip to main content

Cell Recognition of Apoptotic Cells

  • Chapter
Macrophages and Related Cells

Part of the book series: Blood Cell Biochemistry ((BLBI,volume 5))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agarwal, S., Drysdale, B.-E., and Shin, H. S., 1988, Tumor necrosis factor mediated cytotoxicity involves ADP-ribosylation, J. Immunol. 140: 4187–4192.

    PubMed  CAS  Google Scholar 

  • 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 

  • Alnemri, E. S., and Litwack, G., 1989, Glucocorticoid induced lymphocytolysis is not mediated by an induced endonuclease, J. Biol. Chem. 264: 4104–4111.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Arends, M. J., Morris, R. G., and Wyllie, A. H., 1990, Apoptosis: The role of the endonuclease, Am. J. Patho!. 136: 593–608.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bellairs, R., 1961, Cell death in chick embryos as studied by electron microscopy, J. Anat. 95: 54–60.

    PubMed  CAS  Google Scholar 

  • Berger, N. A., 1985, Symposium: Cellular response to DNA damage: The role of poly(ADP-ribose), Radial. Res. 101: 4–15.

    Article  CAS  Google Scholar 

  • Berke, G., 1991, Lymphocyte-triggered internal target disintegration, Immunol. Today 12: 396–399.

    Article  PubMed  CAS  Google Scholar 

  • Berridge, M. J., 1984, Inositol triphosphate and diacylglycerol as second messengers, Biochem. J. 220: 345–360.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bourne, H. R., Coffino, P., and Tomkins, G. M., 1975, Selection of a variant lymphoma cell deficient in adenylate cyclase, Science 187: 750–752.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Collard, M. W., and Griswold, M. D., 1987, Biosynthesis and molecular cloning of sulfated glycoprotein-2 (SGP-2), Biochemistry 26: 3297–3303.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Crompton, T., 1991, IL-3-dependent cells die by apoptosis on removal of their growth factors, Growth Factors 4: 109–116.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Durkacz, B. W., Omidiji, O., Gray, D. A., and Shall, S., 1980, ADP-ribose participates in DNA excision repair, Nature (London) 283: 593–596.

    Article  CAS  Google Scholar 

  • Duvall, E., Wyllie, A. H., and Morris, R. G., 1985, Macrophage recognition of cells undergoing programmed cell death (apoptosis), Immunology 56: 351–358.

    PubMed  CAS  Google Scholar 

  • Dynan, W. S., and Tjian, R., 1985, Control of eukaryotic messenger RNA synthesis by sequence specific DNA binding proteins, Nature (London) 316: 774–778.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Ellis, H M, and Horvitz, H. R., 1986, Genetic control of programmed cell death in the nematode C. elegans, Cell 44: 817–829.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Evans, R. M., 1988, The steroid and thyroid hormone receptor super family, Science 240: 889–895.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Farbman, A. I., 1968, Electron microscope study of palate fusion in mouse embryos, Dey. Biol. 18: 93–116.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Fesus, L., Thomazy, V., and Falus, A., 1987, Induction and activation of tissue transglutaminase during programmed cell death, FEBS Lett. 224: 104–108.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Gaal, J. C., and Pearson, C. K., 1986, Covalent modification of proteins by ADP-ribosylation, Trends Biochem. Sci. 11: 171–175.

    Article  CAS  Google Scholar 

  • Gluecksohn-Schoenheimer, S., 1943, The morphological manifestations of a dominant mutation in mice affecting tail and urogenital system, Genetics 28: 341–348.

    PubMed  CAS  Google Scholar 

  • Gluecksohn-Schoenheimer, S., 1949, The effect of lethal mutation responsible for duplications and twinning in mouse embryos, J. Exp. Zool. 110: 47–76.

    Article  PubMed  CAS  Google Scholar 

  • Glücksmann, A., 1951, Cell deaths in normal vertebrate ontogeny, Biol. Rev. 26: 59–86.

    Article  Google Scholar 

  • Glücksmann, A., 1965, Cell death in normal development, Arch. Biol. (Liège) 76: 419–437.

    Google Scholar 

  • Goldsmith, M., 1966, The anatomy of cell death, J. Cell Biol. 31: 41A.

    Google Scholar 

  • Golstein, P., Ojcius, D. M., and Young, J. D.-E., 1991, Cell death mechanisms and the immune system, Immunol. Rev. 121: 29–65.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hasbold, J., and Klaus, G. G. B., 1990, Anti-immunoglobulin antibodies induce apoptosis in immature B cell lymphomas, Eur. J. Immunol. 20: 1685–1690.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Hopwood, D., and Levison, D. A., 1976, Atrophy and apoptosis in the cyclical human endometrium, J. Pathol. 119: 159–166.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kay, M. M. B., 1975, Mechanism of removal of senescent cells by human macrophages in situ, Proc. Natl. Acad. Sci. USA 72: 3521–3525.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kerr, J. F. R., 1971, Shrinkage necrosis: A distinct mode of cellular death, J. Pathol. 105: 13–20.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Koury, M. J., and Bondurant, M. C., 1990, Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells, Science 248: 378–381.

    Article  PubMed  CAS  Google Scholar 

  • Krähenbühl, I. O., and Tschopp, J., 1991, Perforin-induced pore formation, Immunol. Today 12: 399–402.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Lundin, P. M., and Schelin, U., 1965, Ultrastructure of the rat thymus, Acta Pathol. Microbiol. Scand. 65: 379–394.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Matter, A., 1979, Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes, Immunology 36: 179–190.

    PubMed  CAS  Google Scholar 

  • Matthiessen, M., and Andersen, H., 1972, Disintegration of the junctional epithelium of human fetal hard palate, Z. Anat. Entwicklungsgesch. 137: 153–169.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • McConkey, D. J., Hartzell, P., Nicotera, P., and Orrenius, S., 1989c, Calcium-activated DNA fragmentation kills immature thymocytes, FASEB J. 3: 1843–1849.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • McConkey, D. J., Orrenius, S., and Jondal, M., 1990a, Cellular signaling in programmed cell death (apoptosis), Immunol. Today 11: 120–121.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • McConkey, D. J., Orrenius, S., and Jondal, M., 1990d, Agents that elevate cAMP stimulate DNA fragmentation in thymocytes, J. Immunol. 145: 1227–1230.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Menkes, B., Sandor, S., and hies, A., 1970, Cell death in teratogenesis, Adv. Teratol. 4: 169–215.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Montpetit, M. L., Lawless, K. R., and Tenniswood, M., 1986, Androgen-repressed messages in the rat ventral prostate, The Prostate 8: 25–36.

    Article  PubMed  CAS  Google Scholar 

  • Morgan, J. L., and Curren, T., 1986, Role of ion-flux in the control of c fos expression, Nature (London) 322: 552–555.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Oppenheim, R. W., 1985, Naturally occurring cell death during neural development, Trends Neurosci. 8: 487–493.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Potten, C. S., 1977, Extreme sensitivity of some intestinal crypt cells to X and (gamma} irradiation, Nature (London) 269: 518–521.

    CAS  Google Scholar 

  • Pratt, R. M., and Greene, R. M., 1976, Inhibition of palatal epithelial cell death by altered protein synthesis, Dev. Biol. 54: 135–145.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ruoslahti, E., and Pierschbacher, M. D., 1987, New perspectives in cell adhesion: RGD and integrins, Science 238: 491–497.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Sanderson, C. J., 1981, The mechanism of lymphocyte-mediated cytotoxicity, Biol. Rev. 56: 153–197.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Savill, J., Dransfield, I., Hogg, N., and Haslett, C., 1990a, Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis, Nature (London) 343: 170–173.

    CAS  Google Scholar 

  • 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 

  • Schlüter, G., 1973, Ultrastructural observations on cell necrosis during formation of the neural tube in mouse embryos, Z. Anat. Entwicklungsgesch. 141: 251–264.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sellins, K. S., and Cohen, J. J., 1987, Gene induction by y-irradiation leads to DNA fragmentation in lymphocytes, J. Immunol. 139: 3199–3206.

    PubMed  CAS  Google Scholar 

  • Sklar, M. D., 1988, The ras oncogenes increase the intrinsic resistance of NIH 3T3 cells to ionizing radiation, Science 239: 645–647.

    Article  PubMed  CAS  Google Scholar 

  • Slingerland, J. M., Minden, M. D., and Benchimol. S., 1991, Mutation of the p53 gene in human acute myelogenous leukemia, Blood 77: 1500–1507.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Sulston, J. E., and Horvitz, H. R., 1977, Postembryonic cell lineages of the nematode Caenorhabditis elegans, Dev. Biol. 56: 100–156.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Swartzendruber, D. C., and Congdon, C. C., 1963, Electron microscope observations on tingible body macrophages in mouse spleen, J. Cell Biol. 19: 641–646.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Truman, J. W., 1984, Cell death in invertebrate nervous systems, Annu. Rev. Neurosci. 7: 171–188.

    Article  PubMed  CAS  Google Scholar 

  • Truman, J. W., and Schwartz, L. M., 1982, Programmed death in the nervous system of a moth, Trends Neurosci. 5: 270–273.

    Article  Google Scholar 

  • Tsujimoto, Y., 1989, Stress resistance conferred by high level of bc1–2 a protein in human ß-lymphoblastoid cell, Oncogene 4: 1331–1336.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ucker, D., 1991, Death by suicide: One way to go in mammalian cellular development, The New Biol. 3: 103–109.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Weber, R., 1964, Ultrastructural changes in regressing tail muscles of Xenopus larvae at metamorphosis, J. Cell Biol. 22: 481–487.

    Article  PubMed  CAS  Google Scholar 

  • Webster, D. A., and Gross, J., 1970, Studies on possible mechanisms of programmed cell death in the chick embryo, Dev. Biol. 22: 157–184.

    Article  PubMed  CAS  Google Scholar 

  • Weedon, D., Searle, J., and Kerr, J. F. R., 1979, Apoptosis. Its nature and implications for dermatopathology, Am. J. Dermatopathol. 1: 133–144.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Williams, G. T., 1991, Programmed cell death: Apoptosis and oncogenesis, Cell 65: 1097–1098.

    Article  PubMed  CAS  Google Scholar 

  • Williams, G. T., and Johnstone, A. P., 1983, ADP-ribosyl transferase, rearrangement of DNA and cell differentiation, Biosci. Rep. 3: 815–830.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Wyllie, A. H., 1980, Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation, Nature (London) 284: 555–556.

    CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Wyllie, A. H., Kerr, J. F. R., and Currie, A. R., 1980, Cell death: The significance of apoptosis, Int. Rev. Cytol. 68: 251–306.

    Article  PubMed  CAS  Google Scholar 

  • Wyllie, A. H., Beattie, G. J., and Hargreaves, A. D., 1981, Chromatin changes in apoptosis, Histochem. J. 13: 681–692.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, T., and Ohyama, H., 1988, Radiation-induced interphase death of rat thymocytes is internally programmed (apoptosis), Int. J. Radial. Biol. 53: 65–75.

    Article  CAS  Google Scholar 

  • Yamamoto, K. R., 1985, Steroid receptor regulated transcription of specific genes and gene networks, Annu. Rev. Genet. 19: 209–252.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Young, J. D.-E., and Liu, C. C., 1988, Multiple mechanisms of lymphocyte mediated killing, Immunol. Today 9: 140–144.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Zwilling, E., 1942, The development of the dominant rumplessness in chick embryos, Genetics 27: 641–656.

    PubMed  CAS  Google Scholar 

  • Zwilling, E., 1945, The embryology of recessive rumpless condition of chickens, I. Exp. Zool. 99: 79–91.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer Science+Business Media New York

About this chapter

Cite this chapter

Smith, C.A., McCarthy, N.J., Williams, G.T. (1993). Cell Recognition of Apoptotic Cells. In: Horton, M.A. (eds) Macrophages and Related Cells. Blood Cell Biochemistry, vol 5. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9534-9_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-9534-9_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-9536-3

  • Online ISBN: 978-1-4757-9534-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics