Apoptosis and programmed cell death in immunity

Annual Review of Immunology

Volumn 10, Issue , 1992, Pages 267-293

  Cohen, J John ^a   Duke, Richard C ^a   Fadok, Valerie A ^b   Sellins, Karen S ^c  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^c UNIVERSITY OF COLORADO DENVER   (United States)

Author keywords

activation induced death; apoptosis; cell death; CTL; DNA fragmentation; glucocorticoids

Indexed keywords

GLUCOCORTICOID;

ANIMAL CELL; APOPTOSIS; B LYMPHOCYTE; CELL DEATH; CYTOTOXIC T LYMPHOCYTE; DNA DEGRADATION; HUMAN; HUMAN CELL; MORPHOLOGY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

EID: 0026680874     PISSN: 03013782     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.iy.10.040192.001411     Document Type: Review

References (174)

1. Sarraf, C. E., Bowen, I. D. 1988. Proportions of mitotic and apoptotic cells in a range of untreated experimental tumours. Cell Tissue Kinet. 21: 45-49
2. Hayflick, L. 1981. Cell death in vitro. In Cell Death in Biology and Pathology, ed. I. D. Bowen, R. A. Lockshin, pp. 243-85. London: Chapman & Hall
3. Kerr, J. F. R., Wyllie, A. H., Currie, A. R. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239-57
4. Wyllie, A. H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous nuclease activation. Nature 284: 555-56
5. Clarke, P. G. H. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181: 195-213
6. Alles, A., et al. 1991. Apoptosis: a general comment. FASEB J. 5: 2127-28
7. Touchette, N., Fogle, S. 1991. Apoptosis: it chimes with mitosis. J. NIH Res. 3: 75-78
8. Wyllie, A. H. 1988. Apoptosis. In ISI Atlas of Science: Immunology, pp. 192-96. Philadelphia: ISI Press
9. Wyllie, A. H. 1981. Cell death: a new classification separating apoptosis from necrosis. In Cell Death in Biology and Pathology, ed. I. D. Bowen, R. A. Lockshin, pp. 9-34. London: Chapman & Hall
10. Wyllie, A. H. 1987. Cell death. Int. Rev. Cytol. Suppl. 17: 755-85
11. Duvall, E., Wyllie, A. H. 1986. Death and the cell. Immunol. Today 7: 115-19
12. Wyllie, A. H., Kerr, J. F. R., Currie, A. R. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68: 251-356
13. Golstein, P., Ojcius, D. M., Young, D.-E. 1991. Cell death mechanisms and the immune system. Immunol. Rev. 121: 29-65
14. Berke, G. 1989. Functions and mechanisms of lysis induced by cytotoxic T lymphocytes and natural killer cells. In Fundamental Immunology, ed. W. E. Paul, pp. 735-64. New York: Raven Press
15. Walker, N. I., Harmon, B. V., Gobe, G. C., Kerr, J. F. R. 1988. Patterns of cell death. Methods Achiev. Exp. Pathol. 13: 18-54
16. Cohen, J. J. 1991. Programmed cell death in the immune system. Adv. Immunol. 50: 55-85
17. Kerr, J. F. R. 1971. Shrinkage necrosis: a distinct mode of cellular death. J. Pathol. 105: 13-20
18. Thomas, N., Bell, P. A. 1981. Glucocorticoid-induced cell size changes and nuclear fragility in rat thymocytes. Mol. Cell. Endocrinol. 22: 71-84
19. Ohyama, H., Yamada, T., Watanabe, I. 1981. Cell volume reduction associated with interphase death in rat thymocytes. Radiat. Res. 85: 333-39
20. Sanderson, C. J. 1982. Morphological aspects of lymphocyte mediated cytotoxicity. In Mechanisms of Cell-Mediated Cytotoxicity, ed. W. R. Clark, P. Golstein, pp. 3-21. New York: Plenum
21. Godman, G. C., Miranda, A. F., Deitch, A. D., Tanenbaum, S. W. 1975. Action of cytochalasin D on cells of established lines. III. Zeiosis and movements of the cell surface. J. Cell Biol. 64: 644-67
22. Afanas'ev, V. N., Korol', B. A., Matylevich, N. P., Pechatnikov, V. A., Umansky, S. R. 1988. [The patterns of colchicine-induced death of lymphoid cells.] Tsitologiia 30: 1108-16
23. Martin, S. J., Cotter, T. G. 1990. Disruption of microtubules induces an endogenous suicide pathway in human leukaemia HL-60 cells. Cell Tissue Kinet. 23: 545-59
24. Kolber, M. A., Brochat, K. O., Landa-Gonzalez, B. 1990. Cytochalasin B induces cellular DNA fragmentation. FASEB J. 4: 3021-27
25. Amenta, J. S., Baccino, F. M. 1989. Proteolysis and cell death. Revis. Biol. Cellular 21: 401-22
26. Henson, P. M., Johnston, R. B. Jr. 1987. Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins. J. Clin. Invest. 79: 669-74
27. Singer, J. A., Jennings, L. K., Jackson, C. W., Dockter, M. E., Morrison, M., Walker, W. S. 1986. Erythrocyte hpmeostasis: antibody-mediated recognition of the senescent state by macrophages. Proc. Natl. Acad. Sci. USA 83: 5498-5501
28. Duvall, E., Wyllie, A. H., Morris, R. G. 1985. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56: 351-58
29. Savill, J. S., Henson, P. M., Haslett, C. 1989. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge-sensitive" recognition mechanism. J. Clin. Invest. 84: 1518-27
30. Savill, J. S., Dransfield, I., Hogg, N., Haslett, C. 1990. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343: 170-73
31. Savill, J. S., Hogg, N., Haslett, C. 1990. Thrombospondin and CD36 modulate macrophage vitronectin receptor (VnR)-mediated phagocytosis of neutrophils undergoing programmed cell death (apoptosis). J. Leukocyte Biol. Supp. 1: 38 (Abs.)
32. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., Henson, P. M. 1991. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. Submitted
33. Op den Kamp, J. A. F. 1979. Lipid asymmetry in membranes. Annu. Rev. Biochem. 48: 47-71
34. Rawyler, A., Roelofsen, B., Op den Kamp, J. A. F. 1984. The use of fluorescamine as a permeant probe to localize phosphatidylethanolamine in intact Friend erythroleukemia cells. Biochim. Biophys. Acta 769: 330-36
35. Rawyler, A., van der Schaft, P. H., Roelofsen, B., Op den Kamp, J. A. F. 1985. Phospholipid localization in the plasma membrane of Friend erythroleukemia cells and mouse erythrocytes. Biochemistry 24: 1777-83
36. Jackson, C. M., Nemerson, Y. 1980. Blood coagulation. Annu. Rev. Biochem. 49: 765-811
37. Beyers, E. M., Comfurius, P., Van Rijn, J. L. M. L., Heinker, H. C., Zwaal, R. F. A. 1982. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur. J. Biochem. 122: 429-36
38. Connor, J., Bucanan, C., Fidler, I. J., Schroit, A. J. 1989. Difierentiation-dependent exposure of phosphatidyl-serine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipids by prothrombinase complex formation. Proc. Natl. Acad. Sci. USA 86: 3184-88
39. Chiu, D., Lubin, B., Roelofsen, B., Van Deenan, L. L. M. 1981. Sickled erythrocytes accelerate clotting in vitro: an effect of abnormal membrane lipid asymmetry. Blood 58: 398-401
40. Fidler, I. J., Raz, A., Fogler, W. E., Kirsh, R., Bugelski, P., Poste, G. 1980. Design of liposomes to improve delivery of macrophage-augmenting agents to alveolar macrophages. Cancer Res. 40: 4460-66
41. Schroit, A. J., Fidler, I. J. 1982. Effects of liposome structure and lipid composition on the activation of the tumoricidal properties of macrophages by liposomes containing muramyl dipeptide. Cancer Res. 42: 161-67
42. Tanaka, Y., Schroit, A. J. 1983. Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells: recognition by autologous macrophages. J. Biol. Chem. 258: 11,335-43
43. Schroit, A. J., Madsen, J. W., Tanaka, Y. 1985. In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J. Biol. Chem. 260: 5131-38
44. Allen, T. M., Williamson, P., Schlegel, R. A. 1988. Phosphatidylserine as a determinant of reticuloendothelial cell recognition of liposome models of the erythrocyte surface. Proc. Natl. Acad. Sci. USA 85: 8067-71
45. Mietto, L., Boarato, E., Toffano, G., Bruni, A. 1989. Internalization of phosphatidylserine by adherent and non-adherent rat mononuclear cells. Biochim. Biophys. Acta 1013: 1-6
46. Cohen, J. J. 1989. Lymphocyte death induced by glucocorticoids. In Anti-Inflammatory Steroid Action: Basic and Clinical Aspects, ed. R. P. Schleimer, H. N. Claman, A. Oronsky, pp. 110-31. San Diego: Academic
47. Arends, M. J., Morris, R. G., Wyllie, A. H. 1990. Apoptosis. The role of the endonuclease. Am. J. Pathol. 136: 593-608
48. Cohen, J. J., Duke, R. C. 1984. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132: 38-42
49. Williamson, R. 1970. Properties of rapidly labelled DNA fragments isolated from the cytoplasm of primary cultures of embryonic mouse liver cells. J. Mol. Biol. 51: 157-68
50. Hewish, D. R., Burgoyne, L. A. 1973. Chromatin substructure. The digestion of chromatin at regularly spaced sites by a nuclear deoxyribonuclease. Biochem. Biophys. Res. Commun. 52: 504-10
51. Hewish, D. R., Burgoyne, L. A. 1973. The calcium dependent endonuclease activity in isolated nuclear preparations. Relationships between its occurrence and the occurrence of other classes of enzymes found on nuclear preparation. Biochem. Biophys. Res. Commun. 52: 475-81
52. Burgoyne, L. A., Hewish, D. R., Mobbs, J. 1974. Mammalian cromatin substructure studies with the calcium-magnesium endonuclease and two dimensional polyacrylamide-gel electrophoresis. Biochem. J. 143: 67-72
53. Cohen, J. J., Duke, R. C., Chervenak, R., Sellins, K. S., Olson, L. K. 1985. DNA fragmentation in targets of CTL: an example of programmed cell death in the immune system. In Mechanisms of Cell-Mediated Cytotoxicity, II, ed. P. Henkart, E. Martz, pp. 493-506. New York: Plenum
54. Alnemri, E. S., Litwack, G. 1989. Glucocorticoid-induced lymphocytolysis is not mediated by an induced endonuclease. J. Biol. Chem. 264: 4104-11
55. 2+)-dependent endodeoxyribonuclease. Biochem. J. 261: 17-21
56. 2+-dependent endonuclease in thymocytes of irradiated rats. Int. J. Radiat. Biol. 53: 749-65
57. Compton, M. M., Cidlowski, J. A. 1987. Identification of a glucocorticoid-induced nuclease in thymocytes. J. Biol. Chem. 262: 8288-92
58. 2+ dependent endodeoxyribonuclease from calf thymus chromatin. J. Biochem. 89: 143-52
59. Vanderbilt, J. N., Bloom, K. S., Anderson, J. N. 1982. Endogenous nuclease: properties and effects on transcribed genes in chromatin. J. Biol. Chem. 257: 13009-17
60. Stratling, W. H., Grade, C., Horz, W. 1984. Calcium-magnesium dependent endonuclease from porcine liver. Purification, properties, and sequence specificity. J. Biol. Chem. 259: 5893-98
61. 2+)-dependent endonuclease associated with differentiating erythroid cells. Fed. Procs. 42: 2151 (Abstr.)
62. Sellins, K. S., Cohen, J. J. 1989. Polyoma viral DNA is damaged in target cells during cytotoxic T lymphocyte-mediated killing. J. Virol. 63: 572-78
63. McConkey, D. J., Hartzell, P., Nicotera, P., Orrenius, S. 1989. Calcium-activated DNA fragmentation kills immature thymocytes. FASEB J. 3: 1843-49
64. Shi, Y. F., Szalay, M. G., Paskar, L., Boyer, M., Singh, B., Green, D. R. 1990. Activation-induced cell death in T cell hybridomas is due to apoptosis. Morphologic aspects and DNA fragmentation. J. Immmol. 144: 3326-33
65. Sellins, K. S., Cohen, J. J. 1991. Cytotoxic T lymphocytes induce different types of DNA damage in target cells of different origins. J. Immunol. 147: 795-803
66. Sellins, K. S., Cohen, J. J. 1991. Hyperthermia induces apoptosis in thymocytes. Radiat. Res. 126: 88-95
67. Finkel, T. H., Marrack, P., Kappler, J. W., Kubo, R. T., Cambier, J. C. 1989. αβ T cell receptor and CD3 transduce different signals in immature T cells. Implications for selection and tolerance. J. Immunol. 142: 3006-12
68. Smith, C. A., Williams, G. T., Kingston, R., Jenkinson, E. J., Owen, J. J. T. 1989. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 337: 181-84
69. Shi, Y. F., Bissonnette, R. P., Parfrey, N., Szalay, M., Kubo, R. T., Green, D. R. 1991. In vivo administration of monoclonal antibodies to the CD3 T cell receptor complex induces cell death (apoptosis) in immature thymocytes. J. Immunol. 146: 3340-46
70. Ashwell, J. D., Cunningham, R. E., Noguchi, P. D., Hernandez, D. 1987. Cell growth cycle block of T cell hybridomas upon activation with antigen. J. Exp. Med. 165: 173-94
71. Mercep, M., Bluestone, J. A., Noguchi, P. D., Ashwell, J. D. 1988. Inhibition of transformed T cell growth in vitro by monoclonal antibodies directed against distinct activating molecules. J. Immunol. 140: 324-35
72. Ucker, D. S., Ashwell, J. D., Nickas, G. 1989. Activation-driven T cell death. I. Requirements for de novo transcription and translation and association with genome fragmentation. J. Immunol. 143: 3461-69
73. Mercep, M., Weissman, A. M., Frank, S. J., Klausner, R. D., Ashwell, J. D. 1989. Activation-driven programmed cell death and T cell receptor zeta eta expression. Science 246: 1162-65
74. + thymocytes in suspension culture by extrathymic antigen-presenting cells. Nature 351: 150-53
75. lo thymocytes in vivo. Science 250: 1720-23
76. Hiramine, C., Hojo, K., Koseto, M., Nakagawa, T., Mukasa, A. 1990. Establishment of a murine thymic epithelial cell line capable of inducing both thymic nurse cell formation and thymocyte apoptosis. Lab. Invest. 62: 41-54
77. Nakashima, M., Mori, K., Maeda, K., Kishi, H., Hirata, K., Kawabuchi, M., Watanabe, T. 1990. Selective elimination of double-positive immature thymocytes by a thymic epithelial cell line. Eur. J. Immunol. 20: 47-53
78. Miller, J. F. A. P., Morahan, G., Allison, J., Bhathal, P. S., Cox, K. O. 1989. T cell tolerance in transgenic mice expressing major histocompatibility class I molecules in defined tissues. Immunol. Rev. 107: 109-23
79. Lo, D., Burkly, G., Wildera, C., Cowing, C., Flavell, R. D., Palmiter, R. D., Brinster, R. L. 1988. Diabetes and tolerance in transgenic mice expressing class II molecules in pancreatic beta cells. Cell 53: 159-68
80. Quill, H., Schwartz, R. H. 1987. Stimulation of normal inducer T cell clones with antigen presented by purified Ia molecules in planar lipid membranes: specific induction of a long-lived state of proliferative nonresponsiveness. J. Immunol. 138: 3704-12
81. Jenkins, M. K., Schwartz, R. H. 1987. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165: 302-19
82. Newell, M. K., Haughn, L. J., Maroun, C. R., Julius, M. H. 1990. Death of mature T cells by separate ligation of CD4 and the T-cell receptor for antigen. Nature 347: 286-89
83. Ameisen, J. C., Capron, A. 1991. Cell dysfunction and depletion in AIDS: the programmed cell death hypothesis. Immunol. Today 12: 102-5
84. Cohen, J. J. 1992. Glucocorticoids. In Encyclopedia of Immunology, ed. I. M. Roitt, P. J. Delves, pp. 616-17. London: Saunders
85. Owens, G. P., Hahn, W. E., Cohen, J. J. 1991. Identification of mRNAs associated with programmed cell death in immature thymocytes. Mol. Cell. Biol. 11: 4177-88
86. Gillis, S., Ferm, M. M., Ou, W., Smith, K. A. 1978. T cell growth factor: parameters of production and a quantitative microassay for activity. J. Immunol. 120: 2027-32
87. Bishop, C. J., Moss, D. J., Ryan, J. M., Burrows, S. R. 1985. T lymphocytes in infectious mononucleosis. II. Response in vitro to interleukin-2 and establishment of T cell lines. Clin. Exp. Immunol. 60: 70-77
88. Cohen, J. J., Duke, R. C., Chervenak, R., Sellins, K. S., Olson, L. K. 1985. DNA fragmentation in targets of CTL: an example of programmed cell death in the immune system. Adv. Exp. Med. Biol. 184: 493-506
89. Duke, R. C., Cohen, J. J. 1986. IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells. Lymphokine Res. 5: 289-99
90. Malynn, B. A., Blackwell, T. K., Fulop, G. M., Rathbun, G. A., Furley, A. J. W., Ferrier, P., Heinke, L. B., Phillips, R. A., Yancopoulos, G. D., Alt, F. W. 1988. The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell 54: 453-60
91. Nossal, G. J. V. 1983. Cellular mechanisms of immunologic tolerance. Annu. Rev. Immunol. 1: 33-62
92. Nemazee, D. A., Buerki, K. 1989. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337: 562-66
93. Nemazee, D. A., Buerki, K. 1989. Clonal deletion of autoreactive B lymphocytes in bone marrow chimeras. Proc. Natl. Acad. Sci. USA 86: 8039-43
94. Benhamou, L. E., Cazenave, P. A., Sarthou, P. 1990. Anti-immunoglobulins induce death by apoptosis in WEHI-231 B lymphoma cells. Eur. J. Immunol. 20: 1405-7
95. Monroe, J. G., Seyfert, V. L., Owen, C. S., Sykes, N. 1989. Isolation and characterization of a B lymphocyte mutant with altered signal transduction through its antigen receptor. J. Exp. Med. 169: 1059-70
96. Trowell, O. A. 1952. The sensitivity of lymphocytes to ionizing radiation. J. Path. Bact. 64: 687-704
97. Okada, S. 1970. Radiation-induced death. In Radiation Biochemistry, Vol. 1: Cells, ed. C. Kent, S. Mann, pp. 247-307. New York: Academic
98. Cole, L. J., Ellis, M. E. 1957. Radiation-induced changes in tissue nucleic acids: release of soluble deoxypoly-nucleotides in the spleen. Rad. Res. 7: 508-17
99. Shalka, M., Matyasova, J., Cejkova, M. 1976. DNA in chromatin of irradiated lymphoid tissues degrades in vivo into regular fragments. FEBS Lett. 72: 271-74
100. Zhivotovsky, B. D., Zvonareva, N. B., Hanson, K. P. 1981. Characteristics of rat thymus chromatin degradation products after whole-body X-irradiation. Int. J. Radiat. Biol. 39: 437-40
101. Yamada, T., Ohyama, H., Kinjo, Y., Watanabe, M. 1981. Evidence for the internucleosomal breakage of chromatin in rat thymocytes irradiated in vitro. Radiat. Res. 85: 544-53
102. Umansky, S. R., Korol, B. A., Nelipovich, P. A. 1981. In vivo DNA degradation in thymocytes of gamma-irradiated or hydrocortisone-treated rats. Biochim. Biophys. Acta 655: 9-17
103. Nikonova, L. V., Nelipovich, P. A., Umansky, S. R. 1982. The involvement of nuclear nucleases in rat thymocyte DNA fragmentation after gamma-irradiation. Biochim. Biophys. Acta 699: 281-89
104. Matyasova, J., Skalka, M., Cejkova, M. 1984. On the degradation of chromatin to nucleosomes in the thymocytes of X-irradiated mice. Fol. Biol. (Praha) 30: 123-36
105. Sellins, K. S., Cohen, J. J. 1987. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J. Immunol. 139: 3199-3206
106. Yamada, T., Ohyama, H. 1988. Radiation-induced interphase death of rat thymocytes is internally programmed (apoptosis). Int. J. Radiat. Biol. 53: 65-75
107. Domashenko, A. D., Nazarova, L. F., Umansky, S. R. 1990. Comparison of the spectra of proteins synthesized in mouse thymocytes after irradiation or hydrocortisone treatment. Int. J. Rad. Biol. 57: 315-29
108. Prasad, K. N. 1984. CRC Handbook of Radiobiology. Boca Raton: CRC
109. Anderson, R. E., Warner, N. L. 1976. Ionizing radiation and the immune response. Adv. Immunol. 24: 215-335
110. Warters, R. L., Roti Roti, J. L. 1982. Hyperthermia and the cell nucleus. Radiat. Res. 92: 458-62
111. Roti Roti, J. L., Laszlo, A. 1988. The effects of hyperthermia on cellular macromolecules. In Hyperthermia and Oncology, ed. M. Urano, E. Douple, 1: 13-56. Amsterdam: VSP BV
112. Roti Roti, J. L. 1982. Heat-induced cell death and radiosensitization: Molecular mechanisms. Natl. Cancer Inst. Monogr. 61: 3-10
113. Dewey, W. C. 1989. The search for critical cellular targets damaged by heat. Radiat. Res. 120: 191-204
114. Buckley, I. K. 1972. A light and electron microscopic study of thermally injured cultured cells. Lab. Invest. 26: 201-9
115. Wanner, R. A., Edwards, M. J., Wright, R. G. 1976. The effects of hyperthermia on the neuro-epithelium of the 21-day guinea-pig foetus: histologic and ultrastructural study. J. Pathol. 118: 235-44
116. Allan, D. J., 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. Scan. Electron. Microsc. 3: 1121-33
117. Allan, D. J., Harmon, B. V., Kerr, J. F. R. 1987. Cell death in spermatogenesis. In Perspectives on Mammalian Cell Death, ed. C. S. Potten, pp. 229-59. Oxford: Oxford Univ. Press
118. Dyson, J. E., Simmons, D. M., Daniel, J., McLaughlin, J. M., Quirke, P., Bird, C. C. 1986. Kinetic and physical studies of cell death induced by chemotherapeutic agents or hyperthermia. Cell Tissue Kinet. 19: 311-24
119. Harmon, B. V., Corder, A. M., Collins, R. J., Gobe, G. C., Allen, J., Allan, D. J., Kerr, J. F. R. 1990. Cell death induced in murine mastocytoma by 42-47°C heating in vitro: evidence that the form of death changes from apoptosis to necrosis above a critical heat load. Int. J. Radiat. Biol. 58: 845-58
120. Harmon, B. V., Takano, Y. S., Winterford, C. M., Gobe, G. C. 1991. The role of apoptosis in the response of cells and tumours to mild hyperthermia. Int. J. Radiat. Biol. 59: 489-501
121. Deleted in proof
122. Sanderson, C. J., Thomas, J. A. 1977. The mechanism of T-cell mediated cytolysis. II. Characteristics of the effector cell and morphological changes in the target cell. Proc. R. Soc. London Ser. B 197: 417-24
123. Bishop, C. J., Whiting, V. A. 1983. The role of natural killer cells in the intravascular death of intravenously injected murine tumor cells. Br. J. Cancer 48: 441-44
124. Stacey, N. H., Bishop, C. J., Halliday, J. W., Halliday, W. J., Cooksley, W. G. E., Powell, L. W., Kerr, J. F. R. 1985. Appptosis as the mode of cell death in antibody-dependent lymphocytotoxicity. J. Cell Sci. 74: 169-79
125. Duke, R. C., Cohen, J. J., Chervenak, R. 1986. Differences in target cell DNA fragmentation induced by mouse cytotoxic T lymphocytes and natural killer cells. J. Immunol. 137: 1442-47
126. Zychlinsky, A., Zheng, L. M., Liu, C. C., Young, J. D. 1991. Cytolytic lymphocytes induce both apoptosis and necrosis in target cells. J. Immunol. 146: 393-400
127. Henkart, P. A. 1985. Mechanism of lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 3: 31-58
128. Podack, E. R. 1985. The molecular mechanism of lymphocyte-mediated tumor cell lysis. Immunol. Today 6: 21-23
129. Young, J. D.-E., Cohn, Z. A. 1986. Cell-mediated killing: a common mechanism? Cell 46: 641-42
130. Henkart, P. A., Millard, P. J., Reynolds, C. W., Henkart, M. P. 1984. Cytolytic activity of purified cytoplasmic granules from cytotoxic rat LGL tumors. J. Exp. Med. 160: 75-93
131. Podack, E. R., Konigsberg, P. J., Acha-Orbea, H., Pircher, H., Hengartner, H. 1985. Cytolytic T-cell granules: biochemical properties and functional specificity. Adv. Exp. Med. Biol. 184: 99-117
132. Podack, E. R., Young, J. D.-E., Cohn, Z. A. 1985. Isolation and biochemical and functional characterization of perform 1 from cytolytic T cell granules. Proc. Natl. Acad. Sci. USA 82: 8629-33
133. Pasternak, M. S., Eisen, H. N. 1985. A novel serine esterase expressed by CTL. Nature 314: 743-45
134. Masson, D., Corthesy, P., Nabholz, M., Tschopp, J. 1985. Appearance of cytolytic granules upon induction of cytolytic activity in CTL-hybrids. EMBO J. 4: 2533-38
135. Battersby, C., Egerton, W. S., Balderson, G., Kerr, J. F. R., Burnett, W. 1974. Another look at rejection of pig liver homografts. Surgery 76: 617-23
136. Slavin, R. E., Woodruff, J. M. 1974. The pathology of bone marrow transplantation. Pathol. Ann. 9: 291-344
137. Don, M. M., Ablett, G., Bishop, C. J., Bundesin, P. G., Donald, K. J., Searle, J., Kerr, J. F. R. 1977. Death of cells by apoptosis following attachment of specifically allergized lymphocytes in vitro. Aust. J. Exp. Biol. Med. Sci. 55: 407-17
138. Sanderson, C. J., Glauert, A. M. 1977. The mechanism of T-cell mediated cytolysis. V. Morphological studies by electron microscopy. Proc. R. Soc. London Ser. B 198: 315-23
139. Searle, J., Kerr, J. F. R., Battersby, C., Egerton, W. S., Balderson, G., Burnett, W. 1977. An electron microscopic study of the mode of donor cell death in unmodified rejection of pig liver allografts. Aust. J. Exp. Biol. Med. Sci. 55: 401-6
140. Matter, A. 1979. Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes. Immunology 36: 179-90
141. Russell, J. H., Dobos, C. B. 1980. Mechanisms of immune lysis 2. CTL-induced disintegration of the target begins within minutes of cell contact. J. Immunol. 125: 1256-61
142. Russell, J. H., Masakowski, V. R., Rucinsky, T., Phillips, G. 1982. Mechanisms of immune lysis 3. Characterization of the nature and kinetics of the cytotoxic T lymphocyte-induced nuclear lesion in the target. J. Immunol. 128: 2087-94
143. Duke, R. C., Chervenak, R., Cohen, J. J. 1983. Endogenous endonuclease-induced DNA fragmentation: An early event in cell-mediated cytolysis. Proc. Natl. Acad. Sci. USA 80: 6361-65
144. Duke, R. C., Cohen, J. J. 1988. The role of nuclear damage in lysis of target cells by cytotoxic T lymphocytes. In Cytolytic Lymphocytes and Complement: Effectors of the Immune System, ed. E. R. Podack, pp. 35-57. Boca Raton: CRC Press
145. Young, J. D.-E., Clark, W. R., Liu, C.-C., Cohn, Z. A. 1987. A calcium-and perforin-independent pathway of killing mediated by murine cytolytic lymphocytes. J. Exp. Med. 166: 1894-99
146. Ostergaard, H. L., Clark, W. R. 1989. Evidence for multiple lytic pathways used by cytotoxic T lymphocytes. J. Immunol. 143: 2120-26
147. Ju, S.-T., Ruddle, N. H., Struck, P., Dorf, M. E., DeKruyff, R. H. 1990. Expression of two distinct cytolytic mechanisms among murine CD4 subsets. J. Immunol. 144: 23-31
148. Duke, R. C., Sellins, K. S., Cohen, J. J. 1988. Cytotoxic lymphocyte-derived lytic granules do not induce DNA fragmentation in target cells. J. Immunol. 141: 2191-94
149. Gromkowski, S. H., Brown, T. C., Masson, D., Tschopp, J. 1988. Lack of DNA degradation in target cells lysed by granules derived from cytolytic T lymphocytes. J. Immunol. 141: 774-78
150. Duke, R. C., Persechini, P. M., Chang, S., Liu, C.-C., Cohen, J. J., Young, D.-E. 1989. Purified perform induces target cell lysis but not DNA fragmentation. J. Exp. Med. 170: 1451-56
151. Munger, W. E., Reynolds, C. W., Henkart, P. A. 1985. DNase activity in cytoplasmic granules of cytotoxic lymphocytes. Fed. Proc. 44: 1284 (Abs.)
152. Konigsberg, P. J., Podack, E. R. 1985. Target cell DNA fragmentation induced by cytolytic T-cell granules. J. Leukocyte Biol. 38: 109 (Abs.)
153. Munger, W. E., Berrebi, G. A., Henkart, P. A. 1988. Possible involvement of CTL granule proteases in target cell DNA breakdown. Immunol. Rev. 103: 99-109
154. Hameed, A., Olsen, K. J., Lee, M.-K., Lichtenheld, M. G., Podack, E. R. 1989. Cytolysis by Ca-permeable transmembrane channels. Pore formation causes extensive DNA degradation and cell lysis. J. Exp. Med. 169: 765-77
155. Laster, S. M., Wood, J. G., Gooding, L. R. 1988. Tumor necrosis factor can induce both apoptotic and necrotic forms of cell lysis. J. Immunol. 141: 2629-34
156. Schmid, D. S., Tite, J. P., Ruddle, N. H. 1986. DNA fragmentation: Manifestation of target cell destruction mediated by cytotoxic T-cell lines, lymphotoxin-containing supernatant. Proc. Natl. Acad. Sci. USA 83: 1881-85
157. Liu, C.-C., Steffen, M., King, F., Young, J. D.-E. 1987. Identification, isolation, and characterization of a novel cytotoxin in murine cytolytic lymphocytes. Cell 51: 393-403
158. Shi, Y. F., Kraut, R. P., Greenberg, A. H. 1991. Partial purification of NK cell granule nucleolytic factor. FASEB J. 5: A601
159. Ostergaard, H. L., Kane, K. P., Mescher, M. F., Clark, W. R. 1987. Cytotoxic T lymphocyte mediated lysis without release of serine esterase. Nature 330: 71-72
160. Trenn, G., Takayama, H., Sitkovski, M. V. 1987. Exocytosis of cytolytic granules may not be required for target cell lysis by cytotoxic T-lymphocytes. Nature 330: 72-74
161. Takayama, H., Trenn, G., Sitkovsky, M. V. 1988. Locus of inhibitory action of cAMP-dependent protein kinase in the antigen receptor-triggered cytotoxic T lymphocyte activation pathway. J. Biol. Chem. 263: 2330-36
162. Trenn, G., Taffs, R., Hohman, R., Kincaid, R., Shevach, E. M., Sitkovsky, M. 1989. Biochemical characterization of the inhibitory effect of cyclosporin A on cytolytic T lymphocyte effector functions. J. Immunol. 142: 3796-3802
163. Nash, P. B., Duke, R. C. 1991. Certain requirements for delivery of the lethal hit can be overcome by "triggering" the effector cells prior to interaction with their targets. FASEB J. 5: A600
164. Felgar, R., Hiserodt, J. 1990. A novel cytotoxic activity isolated from the plasma membrane of highly purified lymphokine activated killer cells and the LGL tumor CRNK-16. FASEB J. 4: A1900
165. 2+ increase in the target. FASEB J. 4: 2661-64
166. Henkart, P., Henkart, M., Millard, P., Frederikse, P., Bluestone, J., Blumenthal, R., Yue, C., Reynolds, C. 1984. The role of cytoplasmic granules in cytotoxicity by large granular lymphocytes and cytotoxic T lymphocytes. Adv. Exp. Med. Biol. 184: 121-34
167. Martz, E., Howell, D. M. 1989. CTL: virus control cells first and cytolytic cells second? DNA fragmentation, apoptosis and the prelytic halt hypothesis. Immunol. Today 10: 79-86
168. Christiaansen, J. E., Sears, D. W. 1985. Lack of lymphocyte-induced DNA fragmentation in human targets during lysis represents a species-specific difference between human and murine cells. Proc. Natl. Acad. Sci. USA 82: 4482-85
169. Gromkowski, S. H., Brown, T. C., Cerutti, P. A., Cerottini, J. C. 1986. DNA of human Raji target cells is damaged upon lymphocyte-mediated lysis. J. Immunol. 136: 752-56
170. Howell, D. M., Martz, E. 1987. The degree of CTL-induced DNA solubilization is not determined by the human vs mouse origin of the target cell. J. Immunol. 138: 3695-98
171. Sellins, K. S., Duke, R. C., Cohen, J. J. 1988. All target cells undergo DNA damage during cytotoxic T cell-mediated lysis. FASEB J. 2: A468
172. Martin, S. J., Lennon, S. V., Bonham, A. M., 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: 1859-67
173. McCall, C. A., Cohen, J. J. 1991. Programmed cell death in terminally differentiating keratinocytes: role of endogenous endonuclease. J. Invest. Dermatol. 97: 111-14
174. Martin, J. B. 1982. Huntington's disease: genetically programmed cell death in the human central nervous system. Nature 299: 205-6