The morphology of apoptosis

Cell and Tissue Research

Volumn 301, Issue 1, 2000, Pages 5-17

  Häcker, Georg ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Apoptosis; Caspases; Morphology

Indexed keywords

CASPASE;

ANIMAL CELL; APOPTOSIS; BIOCHEMISTRY; CELL COMMUNICATION; CELL DEATH; CELL FUNCTION; CELL STRUCTURE; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

EID: 0033942431     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410000193     Document Type: Review

References (116)

1. Arends MJ, Morris RG, Wyllie AH (1990) Apoptosis. The role of the endonuclease. Am J Pathol 136:593-608
2. Ballard KJ, Holt SJ (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
3. Bannerman DD, Sathyamoorthy M, Goldblum SE (1998) Bacterial lipopolysaccharide disrupts endothelial monolayer integrity and survival signaling events through caspase cleavage of adherens junction proteins. J Biol Chem 273:35371-35380
4. Bardon S, Vignon F, Montcourrier P, Rochefort H (1987) Steroid receptor-mediated cytotoxicity of an antiestrogen and an antiprogestin in breast cancer cells. Cancer Res 47:1441-1448
5. Belloni AS, Vassanelli P, Robba C, Rebuffat P, Mazzocchi G, Nussdorfer GG (1982) Ultrastructural observations on the regeneration of adrenocortical autotransplants in the rat spleen. J Anat 135:245-253
6. Borner C, Monney L (1999) Apoptosis without caspases: an inefficient molecular guillotine? Cell Death Differ 6:497-507
7. Bowen ID, Mullarkey K, Morgan SM (1996) Programmed cell death during metamorphosis in the blow-fly Calliphora vomitoria. Microsc Res Tech 34:202-217
8. Brancolini C, Benedetti M, Schneider C (1995) Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICE-like proteases. EMBO J 14:5179-5190
9. Bursch W, Taper HS, Lauer B, Schulte-Hermann R (1985) Quantitative histological and histochemical studies on the occurrence and stages of controlled cell death (apoptosis) during regression of rat liver hyperplasia. Virchows Arch B Cell Pathol Incl Mol Pathol 50:153-166
10. Chautan M, Chazal G, Cecconi F, Gruss P, Golstein P (1999) Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 9:967-970
11. Cikala M, Wilm B, Hobmayer E, Bottger A, David CN (1999) Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol 9:959-962
12. Clarke PG, Clarke S (1996) Nineteenth century research on naturally occurring cell death and related phenomena. Anat Embryol (Berl) 193:81-99
13. Cohen JJ, Duke RC (1984) Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132:38-42
14. Colussi PA, Harvey NL, Kumar S (1998) Prodomain-dependent nuclear localization of the caspase-2 (Nedd2) precursor. A novel function for a caspase prodomain. J Biol Chem 273: 24535-24542
15. Cosulich SC, Horiuchi H, Zerial M, Clarke PR, Woodman PG (1997) Cleavage of Rabaptin-5 blocks endosome fusion during apoptosis. EMBO J 16:6182-6191
16. Cotter TG, Lennon SV, Glynn JM, Green DR (1992) Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res 52: 997-1005
17. Dai JD, Gilbert LI (1999) An in vitro analysis of ecdysteroid-elicited cell death in the prothoracic gland of Manduca sexta. Cell Tissue Res 297:319-327
18. Dunn WA Jr (1994) Autophagy and related mechanisms of lysosomal-mediated protein degradation. Trends Cell Biol 4:139-143
19. Ellis RE, Jacobson DM, Horvitz HR (1991a) Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129:79-94
20. Ellis RE, Yuan JY, Horvitz HR (1991b) Mechanisms and functions of cell death. Annu Rev Cell Biol 7:663-698
21. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43-50
22. Fadok VA, Henson PM (1998) Apoptosis: getting rid of the bodies. Curr Biol 8:R6930-R695
23. Fearnhead HO, Dinsdale D, Cohen GM (1995) An interleukin-1 beta-converting enzyme-like protease is a common mediator of apoptosis in thymocytes. FEBS Lett 375:283-288
24. Ferguson DJ, Anderson TJ (1981) Ultrastructural observations on cell death by apoptosis in the "resting" human breast. Virchows Arch Pathol Anat Histopathol 393:193-203
25. Fernandez-Segura E, Garcia JM, Campos A (1990) Scanning electron microscopic study of natural killer cell-mediated cytotoxicity. Histol Histopathol 5:305-310
26. Franc NC, Dimarcq JL, Lagueux M, Hoffmann J, Ezekowitz RA (1996) Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4: 431-443
27. Fraser AG, McCarthy NJ, Evan GI (1997) drICE is an essential caspase required for apoptotic activity in Drosophila cells. EMBO J 16:6192-6199
28. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501
29. Gohring F, Schwab BL, Nicotera P, Leist M, Fackelmayer FO (1997) The novel SAR-binding domain of scaffold attachment factor A (SAF-A) is a target in apoptotic nuclear breakdown. EMBO J 16:7361-7371
30. Granville DJ, Carthy CM, Jiang H, Shore GC, McManus BM, Hunt DW (1998) Rapid cytochrome c release, activation of caspases 3, 6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated with photodynamic therapy. FEBS Lett 437:5-10
31. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309-1312
32. Halaby R, Zakeri Z, Lockshin RA (1994) Metabolic events during programmed cell death in insect labial glands. Biochem Cell Biol 72:597-601
33. Hammond EM, Brunet CL, Johnson GD, Parkhill J, Milner AE, Brady G, Gregory CD, Grand RJ (1998) Homology between a human apoptosis specific protein and the product of APG5, a gene involved in autophagy in yeast. FEBS Lett 425:391-395
34. Henics T, Wheatley DN (1999) Cytoplasmic vacuolation, adaptation and cell death: a view on new perspectives and features. Biol Cell 91:485-498
35. Hirata H, Takahashi A, Kobayashi S, Yonehara S, Sawai H, Okazaki T, Yamamoto K, Sasada M (1998) Caspases are activated in a branched protease cascade and control distinct downstream processes in Fas-induced apoptosis. J Exp Med 187:587-600
36. Huot J, Houle F, Rousseau S, Deschesnes RG, Shah GM, Landry J (1998) SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J Cell Biol 143:1361-1373
37. Inohara N, Koseki T, Chen S, Wu X, Nunez G (1998) CIDE, a novel family of cell death activators with homology to the 45 kDa subunit of the DNA fragmentation factor. EMBO J 17:2526-2533
38. Jacobson MD, Burne JF, Raff MC (1994) Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J 13:1899-1910
39. Janicke RU, Ng P, Sprengart ML, Porter AG (1998a) Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem 273:15540-15545
40. Janicke RU, Sprengart ML, Wati MR, Porter AG (1998b) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273:9357-9360
41. Kawabata Y, Hirokawa M, Kitabayashi A, Horiuchi T, Kuroki J, Miura AB (1999) Defective apoptotic signal transduction pathway downstream of caspase-3 in human B-lymphoma cells: a novel mechanism of nuclear apoptosis resistance. Blood 94:3523-3530
42. Kerr JF (1965) A histochemical study of hypertrophy and ischaemic injury of rat liver with special reference to changes in lysosomes. J Pathol Bacteriol 90:419-435
43. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basis biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257
44. Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E, Goldberg M, Allen T, Barber MJ, Green DR, Newmeyer DD (1999) The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147:809-822
45. Kondo T, Takeuchi K, Doi Y, Yonemura S, Nagata S, Tsukita S (1997) ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis. J Cell Biol 139:749-758
46. Kothakota S, Azuma T, Reinhard C, Klippel A, Tang J, Chu K, McGarry TJ, Kirschner MW, Koths K, Kwiatkowski DJ, Williams LT (1997) Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278: 294-298
47. Lagasse E, Weissman IL (1994) Bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J Exp Med 179:1047-1052
48. Lapointe J, Bergeron D, Dufour M, Dube D, Govindan MV, Lambert RD (1993) Biochemical and morphological characterizations of DU-145 cell mortality in rabbit embryo-fetal fluid. Cell Prolif 26:125-138
49. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346-347
50. Lazebnik YA, Takahashi A, Moir RD, Goldman RD, Poirier GG, Kaufmann SH, Earnshaw WC (1995a) Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci USA 92:9042-9046
51. Lazebnik YA, Takahashi A, Poirier GG, Kaufmann SH, Earnshaw WC (1995b) Characterisation of the execution phase of apoptosis in vitro using extracts from condemned-phase cells. J Cell Sci 19:41-49
52. Lee N, MacDonald H, Reinhard C, Halenbeck R, Roulston A, Shi T, Williams LT (1997) Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc Natl Acad Sci USA 94:13642-13647
53. Levkau B, Herren B, Koyama H, Ross R, Raines EW (1998) Caspase-mediated cleavage of focal adhesion kinase pp125FAK and disassembly of focal adhesions in human endothelial cell apoptosis. J Exp Med 187:579-586
54. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489
55. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676
56. Liu X, Zou H, Slaughter C, Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175-184
57. Liu X, Li P, Widlak P, Zou H, Luo X, Garrard WT, Wang X (1998) The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci U S A 95:8461-8466
58. Liu X, Zou H, Widlak P, Garrard W, Wang X (1999) Activation of the apoptotic endonuclease DFF40 (caspase-activated DNase or nuclease). Oligomerization and direct interaction with histone H1. J Biol Chem 274:13836-13840
59. Ludewig B, Graf D, Gelderblom HR, Becker Y, Kroczek RA, Pauli G (1995) Spontaneous apoptosis of dendritic cells is efficiently inhibited by TRAP (CD40-ligand) and TNF-alpha, but strongly enhanced by interleukin-10. Eur J Immunol 25:1943-1950
60. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3-15
61. Martin SJ, Green DR (1995a) Protease activation during apoptosis: death by a thousand cuts? Cell 82:349-352
62. Martin SJ, O'Brien GA, Nishioka WK, McGahon AJ, Mahboubi A, Saido TC, Green DR (1995b) Proteolysis of fodrin (nonerythroid spectrin) during apoptosis. J Biol Chem 270:6425-6428
63. Mashima T, Naito M, Fujita N, Noguchi K, Tsuruo T (1995) Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis. Biochem Biophys Res Commun 217:1185-1192
64. McCarthy NJ, Whyte MK, Gilbert CS, Evan GI (1997) Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J Cell Biol 136:215-227
65. Mills JC, Lee VM, Pittman RN (1998a) Activation of a PP2A-like phosphatase and dephosphorylation of tau protein characterize onset of the execution phase of apoptosis. J Cell Sci 111:625-636
66. Mills JC, Stone NL, Erhardt J, Pittman RN (1998b) Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol 140:627-636
67. Mills JC, Stone NL, Pittman RN (1999) Extranuclear apoptosis. The role of the cytoplasm in the execution phase. J Cell Biol 146:703-708
68. Moir RD, Goldman RD (1993) Lamin dynamics. Curr Opin Cell Biol 5:408-411
69. Nagata S (1996) Fas-mediated apoptosis. Adv Exp Med Biol 406:119-124
70. Nakagawara A, Nakamura Y, Ikeda H, Hiwasa T, Kuida K, Su MS, Zhao H, Cnaan A, Sakiyama S (1997) High levels of expression and nuclear localization of interleukin-1 beta converting enzyme (ICE) and CPP32 in favorable human neuroblastomas. Cancer Res 57:4578-4584
71. Ng FW, Shore GC (1998) Bcl-XL cooperatively associates with the Bap31 complex in the endoplasmic reticulum, dependent on procaspase-8 and Ced-4 adaptor. J Biol Chem 273:3140-3143
72. Ng FW, Nguyen M, Kwan T, Branton PE, Nicholson DW, Cromlish JA, Shore GC (1997) p28 Bap31, a Bc1-2/Bc1-XL-and procaspase-8-associated protein in the endoplasmic reticulum. J Cell Biol 139:327-338
73. Odaka C, Mizuochi T (1999) Role of macrophage lysosomal enzymes in the degradation of nucleosomes of apoptotic cells. J Immunol 163:5346-5352
74. Ohsawa Y, Isahara K, Kanamori S, Shibata M, Kametaka S, Gotow T, Watanabe T, Kominami E, Uchiyama Y (1998) An ultrastructural and immunohistochemical study of PC12 cells during apoptosis induced by serum deprivation with special reference to autophagy and lysosomal cathepsins. Arch Histol Cytol 61:395-403
75. Ohtsu M, Sakai N, Fujita H, Kashiwagi M, Gasa S, Shimizu S, Eguchi Y, Tsujimoto Y, Sakiyama Y, Kobayashi K, Kuzumaki N (1997) Inhibition of apoptosis by the actin-regulatory protein gelsolin. EMBO J 16:4650-4656
76. Pipan N, Sterle M (1979) Cytochemical analysis of organelle degradation in phagosomes and apoptotic cells of the mucoid epithelium of mice. Histochemistry 59:225-232
77. Pollard JW, Pacey J, Cheng SV, Jordan EG (1987) Estrogens and cell death in murine uterine luminal epithelium. Cell Tissue Res 249:533-540
78. Qi XM, He H, Zhong H, Distelhorst CW (1997) Baculovirus p35 and Z-VAD-fmk inhibit thapsigargin-induced apoptosis of breast cancer cells. Oncogene 15:1207-1212
79. Rao L, Perez D, White E (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135:1441-1455
80. Rotello RJ, Fernandez PA, Yuan J (1994) Anti-apogens and anti-engulfens: monoclonal antibodies reveal specific antigens on apoptotic and engulfment cells during chicken embryonic development. Development 120:1421-1431
81. Rudel T, Bokoch GM (1997) Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276:1571-1574
82. Russell SW, Rosenau W, Lee JC (1972) Cytolysis induced by human lymphotoxin. Am J Pathol 69:103-118
83. Sabourin LA, Seale P, Wagner J, Rudnicki MA (2000) Caspase 3 cleavage of the Ste20-related kinase SLK releases and activates an apoptosis-inducing kinase domain and an actin-disassembling region. Mol Cell Biol 20:684-696
84. Sahara S, Aoto M, Eguchi Y, Imamoto N, Yoneda Y, Tsujimoto Y (1999) Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature 401:168-173
85. Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391:96-99
86. Sakahira H, Enari M, Ohsawa Y, Uchiyama Y, Nagata S (1999) Apoptotic nuclear morphological change without DNA fragmentation. Curr Biol 9:543-546
87. Samali A, Zhivotovsky B, Jones D, Nagata S, Orrenius S (1999) Apoptosis: cell death defined by caspase activation. Cell Death Differ 6:495-496
88. Samejima K, Earnshaw WC (1998a) ICAD/DFF regulator of apoptotic nuclease is nuclear. Exp Cell Res 243:453-459
89. Samejima K, Tone S, Kottke TJ, Enari M, Sakahira H, Cooke CA, Durrieu F, Martins LM, Nagata S, Kaufmann SH, Earnshaw WC (1998b) Transition from caspase-dependent to caspase-independent mechanisms at the onset of apoptotic execution. J Cell Biol 143:225-239
90. Samms M, Philp D, Emanus F, Osuji O, Pezzano M, Guyden JC (1999) Lysosomal-mediated degradation of apoptotic thymocytes within thymic nurse cells. Cell Immunol 197:108-115
91. Savill J (1996) Phagocyte recognition of apoptotic cells. Biochem Soc Trans 24:1065-1069
92. Schulze-Osthoff K, Walczak H, Droge W, Krammer PH (1994) Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 127:15-20
93. Sheridan JW, Bishop CJ, Sinimons RJ (1981) Biophysical and morphological correlates of kinetic change and death in a starved human melanoma cell line. J Cell Sci 49:119-137
94. Strasser A (1999) Dr. Josef Steiner Cancer Research Prize Lecture: the role of physiological cell death in neoplastic transformation and in anti-cancer therapy. Int J Cancer 81:505-511
95. Sun DY, Jiang S, Zheng LM, Ojcius DM, Young JD (1994) Separate metabolic pathways leading to DNA fragmentation and apoptotic chromatin condensation. J Exp Med 179:559-568
96. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G (1996) Bc1-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184:1331-1341
97. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446
98. Tang D, Kidd VJ (1998) Cleavage of DFF-45/ICAD by multiple caspases is essential for its function during apoptosis. J Biol Chem 273:28549-28552
99. Tata JR (1966) Requirement for RNA and protein synthesis for induced regression of the tadpole tail in organ culture. Dev Biol 13:77-94
100. Toh SY, Wang X, Li P (1998) Identification of the nuclear factor HMG2 as an activator for DFF nuclease activity. Biochem Biophys Res Commun 250:598-601
101. Tomei LD, Shapiro JP, Cope FO (1993) Apoptosis in C3H/10T1/2 mouse embryonic cells: evidence for internucleosomal DNA modification in the absence of double-strand cleavage. Proc Natl Acad Sci U S A 90:853-857
102. Torgerson RR, McNiven MA (1998) The actin-myosin cytoskeleton mediates reversible agonist-induced membrane blebbing. J Cell Sci 111:2911-2922
103. Ucker DS, Obermiller PS, Eckhart W, Apgar JR, Berger NA, Meyers J (1992) Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol Cell Biol 12:3060-3069
104. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB (1997) Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91:627-637
105. Vaux DL, Hacker G (1995) Hypothesis: apoptosis caused by cytotoxins represents a defensive response that evolved to combat intracellular pathogens. Clin Exp Pharmacol Physiol 22:861-863
106. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P (1998) Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187: 1477-1485
107. Vogt C (1842) Untersuchungen über die Entwicklungsbiologie der Geburtshelferkröte (Alytes obstetricans). Jent und Gassmann, Solothurn, Switzerland
108. Wen LP, Fahrni JA, Troie S, Guan JL, Orth K, Rosen GD (1997) Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem 272:26056-26061
109. Wilhelm S, Häcker G (1999) Proteolytic specificity of caspases is required to signal the appearance of apoptotic morphology. Eur J Cell Biol 78:127-133
110. Wohrl W, Häcker G (1999) Extent and limitation of the control of nuclear apoptosis by DNA-fragmenting factor. Biochem Biophys Res Commun 254:552-558
111. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556
112. Xiang J, Chao DT, Korsmeyer SJ (1996) BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc Natl Acad Sci U S A 93:14559-14563
113. Zhang J, Liu X, Scherer DC, van Kaer L, Wang X, Xu M (1998) Resistance to DNA fragmentation and chromatin condensation in mice lacking the DNA fragmentation factor 45. Proc Natl Acad Sci U S A 95:12480-12485
114. Zheng TS, Schlosser SF, Dao T, Hingorani R, Crispe IN, Boyer JL, Flavell RA (1998) Caspase-3 controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc Natl Acad Sci U S A 95:13618-13623
115. Zhivotovsky B, Samali A, Gahm A, Orrenius S (1999) Caspases: their intracellular localization and translocation during apoptosis. Cell Death Differ 6:644-651
116. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982-995