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Mechanisms of HSP-Mediated Protection from Ischemia-Induced Apoptosis

  • Chapter
Heat Shock Proteins and Cytoprotection

Abstract

Apoptosis can be divided into the three following phases: induction (or triggering), transduction of signal, and execution (see refs. 1-3 for review). Theoretically, HSPs may modulate any of these apoptotic phases with the same final result, namely rescue of the cells. Below we consider what is presently known about ischemia-induced apoptosis and speculate how HSPs may affect its distinct phases.

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References

  1. Martin SJ. Apoptosis: suicide, execution or murder? Trends Cell Biology 1993; 3: 141–144.

    Article  Google Scholar 

  2. Martin SJ, Green DR, Cotter TG. Dicing with death: dissecting the components of the apoptosis machinery. Trends Biochem Sci 1994; 19: 26–30.

    Article  Google Scholar 

  3. McConkey DJ, Orrenius S. Signal transduc-tion pathways to apoptosis. Trends Cell Biol 1994; 4: 370–375.

    Article  Google Scholar 

  4. Price BD, Calderwood SK. Gadd45 and Gadd 153 messenger RNA levels are in creased during hypoxia and after exposure of cells to agents which elevate the levels of the glucose-regulated proteins. Cancer Res 1992; 52: 3814–3817.

    Google Scholar 

  5. Graeber TG, Peterson JF, Tsai M et al. Hypoxia induces accumulation of p5 3 pro tein, but activation of a G1-phase check point by low-oxygen conditions is indepen dent of p53 status. Mol Cell Biol 1994; 14: 6264–6277.

    Article  Google Scholar 

  6. Graeber TG, Osmanian C, Jacks T et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996; 379: 88–91.

    Article  Google Scholar 

  7. Cummings MC. Increased p53 mRNA ex pression in liver and kidney apoptosis. Biochim Biophys Acta 1996; 1315:100–104.

    Article  Google Scholar 

  8. Didenko VV, Wang XD, Yang LQ et al. Expression of p21 (WAF1/CIP1/SDI1) and p53 in apoptotic cells in the adrenal cortex and induction by ischemia reperfusion in jury. J Clin Invest 1996; 97: 1723–1731.

    Article  Google Scholar 

  9. Kuerbitz SJ, Plunkett BS, Walsh WV et al. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl Acad Sci USA 1992; 89: 7491–7495.

    Article  Google Scholar 

  10. Brugarolas J, Chandrasekaran C, Gordon JI et al. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995; 377: 552–557.

    Article  Google Scholar 

  11. Hooper ML. The role of the p53 and Rb-1 genes in cancer, development and apoptosis. J Cell Sci 1994; 18: 13–17.

    Google Scholar 

  12. Donehower LA, Bradly A. The tumor sup pressor p53. Biochim Biophys Acta 1993; 1155: 181–205.

    Google Scholar 

  13. Montenarh M. Biochemical properties of the growth suppressor/oncoprotein p53. Onco-gene 1992; 7: 1673–1680.

    Google Scholar 

  14. Sugano T, Nitta M, Ohmori H et al. Nuclear accumulation of p53 in normal human fibroblasts is induced by various cellular stresses which evoke the heat shock response, independently of the cell cycle. Jap J Cancer Res 1995; 86: 415–418.

    Article  Google Scholar 

  15. Lennon SV, Martin SJ, Cotter TG. Induc tion of apoptosis (programmed cell death) in tumor cell lines by widely diverging stimuli. Biochem Soc Trans 1990; 18: 343–345.

    Google Scholar 

  16. Ghibelli L, Nosseri C, Oliverio S et al. Cycloheximide can rescue heat-shocked L cells from death by blocking stress-induced apoptosis. Exp Cell Res 1992; 201: 436–443.

    Article  Google Scholar 

  17. Migliorati G, Nicoletti I, Crocicchio F et al. Heat shock induces apoptosis in mouse thymocytes and protects them from gluco-corticoid-induced cell death. Cell Immunol 1992; 143: 348–356.

    Article  Google Scholar 

  18. Lee YJ, Kim JH, Ryu S et al. Mechanisms of mild hyperthermia-induced cytotoxicity in human prostatic carcinoma cells: Perturba tion of cell cycle progression and DNA frag mentation. J Therm Biol 1994; 19: 305–313.

    Article  Google Scholar 

  19. Dypbukt JM, Ankarcrona M, Burkitt M et al. Different prooxidant levels stimulate growth, trigger apoptosis, or produce ne crosis of insulin-secreting RINm5F cells. J Biol Chem 1994; 269: 30553–30560.

    Google Scholar 

  20. Sakaguchi Y, Stephens LC, Makino M et al. Apoptosis in tumor and normal tissues induced by whole body hyperthermia in rats. Cancer Res 1995; 55: 5459–5464.

    Google Scholar 

  21. Cummings M. Increased c-fos expression associated with hyperthermia-induced apoptosis of a Burkitt lymphoma cell line. Int J Radiat Biol 1995; 68: 687–692.

    Article  Google Scholar 

  22. Troiano L, Monti D, Cossarizza A et al. Involvement of CD45 in dexamethasone-and heat shock-induced apoptosis of rat thymocytes. Biochem Biophys Res Com munic 1995; 214: 941–948.

    Article  Google Scholar 

  23. Gabai VL, Kabakov AE, Makarova YuM et al. DNA fragmentation in Ehrlich ascites carcinoma under exposures cai]sing cyto skeletal protein aggregation. Biochemistry (Moscow) 1994; 59: 399–404.

    Google Scholar 

  24. Chowdary DR, Dermody JJ, Jha KK et al. Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol Cell Biol 1994; 14: 1997–2003.

    Google Scholar 

  25. Maki CG, Huibregtse JM, Howley PM. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 1996; 56: 2649–2654.

    Google Scholar 

  26. Molinari M, Milner J. p53 in complex with DNA is resistant to ubiquitin-dependent proteolysis in the presence of HPV-16 E6. Oncogene 1995; 10: 1849–1854.

    Google Scholar 

  27. Parag HA, Raboy B, Kulka RG. Effect of heat shock on protein degradation in mam malian cells: involvement of the ubiquitin system. EMBO J 1987; 6: 55–61.

    Google Scholar 

  28. Carlson N, Rogers S, Rechsteiner M. Mi croinjection of ubiquitin: changes in pro tein degradation in HeLa cells subjected to heat-shock. J Cell Biol 1987; 104: 547–555.

    Article  Google Scholar 

  29. Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell 1994; 79: 13–21.

    Article  Google Scholar 

  30. Chou CC, Lam CY, Yung BYM. Intracel lular ATP is required for actinomycin D induced apoptotic cell death in HeLa cells. Cancer Lett 1995; 96: 181–187.

    Article  Google Scholar 

  31. Richter C, Schweizer M, Cossarizza A et al. Control of apoptosis by the cellular ATP level. FEBS Lett 1996; 378: 107–110.

    Article  Google Scholar 

  32. Matsumoto H, Shimura M, Omatsu T et al. p53 proteins accumulated by heat stress associate with heat shock proteins HSP72/ HSC73 in human glioblastoma cell lines. Cancer Lett 1994; 87: 39–46.

    Article  Google Scholar 

  33. Ohnishi T, Wang XJ, Ohnishi K et al. p53-dependent induction of WAF1 by heat treat ment in human glioblastoma cells. J Biol Chem 1996; 271: 14510–14513.

    Article  Google Scholar 

  34. Mosser DD, Martin LH. Induced thermo tolerance to apoptosis in a human T lym phocyte cell line. J Cell Physiol 1992; 151: 561–570.

    Article  Google Scholar 

  35. Mosser DD, Duchaine J, Bourget L et al. Changes in heat shock protein synthesis and heat sensitivity during mouse thymocyte development. Developmental Genetics 1993; 14: 148–158.

    Article  Google Scholar 

  36. Blake MJ, Buckley AR, Zhang MY et al. A novel heat shock response in prolactin-de-pendent Nb2 node lymphoma cells. J Biol Chem 1995; 270: 29614–29620.

    Article  Google Scholar 

  37. Gabai VL, Zamulaeva IV, Mosin AF et al. Resistance of Ehrlich tumor cells to apoptosis can be due to accumulation of heat shock proteins. FEBS Lett 1995; 375: 21–26.

    Article  Google Scholar 

  38. Li WX, Chen CH, Ling CC et al. Apoptosis in heat-induced cell killing: The protective role of hsp-70 and the sensitization effect of the c-myc gene. Radiat Res 1996; 145: 324–330.

    Article  Google Scholar 

  39. Bukh A, Martinez-Valdez H, Freedman SJ et al. The expression of c-fos, c-jun, and c myc genes is regulated by heat shock in human lymphoid cells. J Immunol 1990; 144: 4835–4840.

    Google Scholar 

  40. Smeyne RJ, Vendrell M, Hayward M et al. Continuous c-fos expression precedes pro grammed cell death in vivo. Nature 1993; 363: 166–169.

    Article  Google Scholar 

  41. Tsurumi C, Ishida N, Tamura T et al. Degradation of c-fos by the 26S proteasome is accelerated by c-jun and multiple protein kinases. Mol Cell Biol 1995; 15: 5682–5687.

    Google Scholar 

  42. Tishler RB, Lamppu DM, Park S et al. Microtubule-active drugs taxol, vinblastine, and nocodazole increase the levels of tran scriptionally active p53. Cancer Res 1995; 55:6021–6025.

    Google Scholar 

  43. Bonfoco E, Ceccatelli S, Manzo L et al. Colchicine induces apoptosis in cerebellar granule cells. Exp Cell Res 1995; 218: 189–200.

    Article  Google Scholar 

  44. Sherwood SW, Sheridan JP, Schimke RT. Induction of apoptosis by the anti-tubulin drug colcemid: Relationship of mitotic checkpoint control to the induction of apoptosis in HeLa S3 cells. Exp Cell Res 1994; 215: 373–379.

    Article  Google Scholar 

  45. Ireland CM, Pittman SM. Tubulin alter ations in taxol-induced apoptosis parallel those observed with other drugs. Biochem Pharmacol 1995; 49: 1491–1499.

    Article  Google Scholar 

  46. Lee WC, Lin KY, Chen KD et al. Induc tion of HSP70 is associated with vincristine resistance in heat-shocked 9L rat brain tu mor cells. Br J Cancer 1992; 66: 653–659.

    Article  Google Scholar 

  47. Wiegant FAC, van Bergen en Henegouwen PMP, van Dongen G al. Stress-induced thermotolerance of the cytoskeleton of mouse neuroblastoma N2A cells and rat reuber H35 hepatoma cells. Cancer Res 1987; 47: 1674–1680.

    Google Scholar 

  48. Wei Y, Zhao X, Kariya Y et al. Induction of apoptosis by quercetin: Involvement of heat shock protein. Cancer Res 1994; 54: 4952–4957.

    Google Scholar 

  49. Wei Y, Zhao X, Kariya Y et al. Inhibition of proliferation and induction of apoptosis by abrogation of heat-shock protein (HSP) 70 expression in tumor cellś. Cancer Immunol Immunother 1995; 40: 73–78.

    Article  Google Scholar 

  50. Perezsala D, Mollinedo F. Inhibition of N linked glycosylation induces early apoptosis in human promyelocytic HL-60 cells. J Cell Physiol 1995; 163: 523–531.

    Article  Google Scholar 

  51. Vai]x DL, Hacker G. Hypothesis: Apoptosis cai]sed by cytotoxins represents a defensive response that evolved to combat intracellu lar pathogens. Clin Exp Pharm Physiol 1995; 22: 861–863.

    Article  Google Scholar 

  52. Zhan O, Fan S, Bae I et al. Induction of bax by genotoxic stress in human cells corre lates with normal p53 status and apoptosis. Oncogene 1994; 9: 3743–3751.

    Google Scholar 

  53. Owen-Schai]b LB, Zhang W, Cusack JC et al. Wild-type human p53 and a tempera ture-sensitive mutant induce Fas/APOl expression. Mol Cell Biol 1995; 15: 3032–3040.

    Google Scholar 

  54. Tanaka M, Ito H, Adachi S et al. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ Res 1994; 75: 426–433.

    Article  Google Scholar 

  55. Caelles C, Helmberg A, Karin M. p53-de pendent apoptosis in the absense of tran scriptional activation of p53-target genes. Nature 1994; 370: 220–223.

    Article  Google Scholar 

  56. Rowan S, Ludwig RL, Hai]pt Y et al. Spe cific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant. EMBO J 1996; 15: 827–838.

    Google Scholar 

  57. Gottlieb E, Lindner S, Oren M. Relation ship of sequence-specific transactivation and p53-regulated apoptosis in interleukin 3-dependent hematopoietic cells. Cell Growth Diff 1996; 7: 301–310.

    Google Scholar 

  58. Umansky SR, Cuenco GM, Khutzian SS et al. Post-ischemic apoptotic death of rat neonatal cardiomyocytes. Cell Death Diff 1995; 2: 235–241.

    Google Scholar 

  59. Gabai VL, Mosina VA, Makarova, YuM et al. Serum withdrawal induces thymocytes apoptosis not requiring protein synthesis or ATP generation. Biochemistry (Moscow) 1995; 60: 907–912.

    Google Scholar 

  60. Ishizaki Y, Cheng L, Mudge AW et al. Programmed cell death by defai]lt in em bryonic cells, fibroblasts, and cancer cells. Mol Biol Cell 1995; 6: 1443–1458.

    Google Scholar 

  61. Weil’ M, Jacobson MD, Coles HSR et al. Constitutive expression of the machinery for programmed cell death. J Cell Biol 1996; 133: 1053–1059.

    Article  Google Scholar 

  62. Jacobson MD, Burne JF, Raff MC. Pro grammed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J 1994; 13: 1899–1910.

    Google Scholar 

  63. Raff MC. Social controls on cell survival and cell death. Nature 1992; 356: 397–400.

    Article  Google Scholar 

  64. Buerke M, Murohara T, Skurk C et al. Cardioprotective effect of insulin-like growth factor I in myocardial ischemia fol lowed by reperfusion. Proc Natl Acad Sci USA 1995; 92: 8031–8035.

    Article  Google Scholar 

  65. Sakaki T, Yamada K, Otsuki H et al. Brief exposure to hypoxia induces bFGF mRNA and protein and protects rat cortical neu rons from prolonged hypoxic stress. Neurosci Res 1995; 23: 289–296.

    Article  Google Scholar 

  66. Rutherford SL, Zuker CS. Protein folding and the regulation of signaling pathways. Cell 1994; 79: 1129–1132.

    Article  Google Scholar 

  67. Reed JC. Bcl-2 and the regulation of pro grammed cell death. J Cell Biol 1994; 124: 1–6.

    Article  Google Scholar 

  68. Hockenbery DM. bcl-2 in cancer, develop ment and apoptosis. J Cell Sci 1994; 18: 51–55.

    Google Scholar 

  69. Chiou S-K, Rao L, White E. Bcl-2 blocks p53-dependent apoptosis. Mol Cell Biol 1994; 14: 2556–2563.

    Article  Google Scholar 

  70. Schott AF, Apel IJ, Nunez G et al. Bcl-x(L) protects cancer cells from p53-mediated apoptosis. Oncogene 1995; 11: 1389–1394.

    Google Scholar 

  71. Shimizu S, Eguchi Y, Kamiike W et al. Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-X(L). Cancer Res 1996; 56: 2161–2166.

    Google Scholar 

  72. Shimizu S, Eguchi Y, Kamiike W et al. Retardation of chemical hypoxia-induced necrotic cell death by Bcl-2 and ICE inhibi tors: Possible involvement of common me diators in apoptotic and necrotic signal trans ductions. Oncogene 1996; 12: 2045–2050.

    Google Scholar 

  73. Shimizu S, Eguchi Y, Kamiike W et al. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene 1996; 12: 2251–2257.

    Google Scholar 

  74. Jacobson MD, Raff MC. Programmed cell death and Bcl-2 protection in very low oxygen. Nature 1995; 374: 814–816.

    Article  Google Scholar 

  75. Zornig M, Busch G, Beneke R et al. Survival and death of prelymphomatous B-cells from N-myc/bcl-2 double transgenic mice correlates with the regulation of intracellu-lar Ca2+ fluxes. Oncogene 1995; 11: 2165–2

    Google Scholar 

  76. Distelhorst CW, Lam M, Mccormick TS. Bcl-2 inhibits hydrogen peroxide-induced ER Ca2+ pool depletion. Oncogene 1996; 12: 2051–2055.

    Google Scholar 

  77. Marin MC, Fernandez A, Bick RJ et al. Apoptosis suppression by bcl-2 is correlated with the regulation of nuclear and cytosolic Ca2+. Oncogene 1996; 12: 2259–2266.

    Google Scholar 

  78. Tsujimoto Y. Stress-resistance conferred by high level of bcl-2 alpha protein in human B lymphoblastoid cell. Oncogene 1989; 4: 1331–1336.

    Google Scholar 

  79. Strasser A, Anderson RL. Bcl-2 and thermotolerance cooperate in cell survival. Cell Growth Diff 1995; 6: 799–805.

    Google Scholar 

  80. Cuende E, Ales-Martinez JE, Ding L et al. Programmed cell death by bel-2-dependent and independent mechanisms in B lym-phoma cells. EMBOJ 1993; 12: 1555–1560.

    Google Scholar 

  81. Vai]x DL, Whitney D, Weissman IL. Acti vation of physiological cell death mecha nisms by a necrosis-cai]sing agent. Micros copy Res Technique 1996; 34: 259–266.

    Article  Google Scholar 

  82. Jaattela M, Benedict M, Tewari M et al. Bcl-x and bcl-2 inhibit TNF and Fas-in duced apoptosis and activation of phospho lipase A2 in breast carcinoma cells. Oncogene 1995; 10: 2297–2305.

    Google Scholar 

  83. Jaattela M. Overexpression of major heat shock protein hsp70 inhibits tumor necro sis factor-induced activation of phospholi-pase A2. J Immunol 1993; 151: 4286–4294.

    Google Scholar 

  84. Macewan DJ. Elevated cPLA2 levels as a mechanism by which the p70 TNF and p75 NGF receptors enhance apoptosis. FEBS Lett 1996; 379: 77–81.

    Article  Google Scholar 

  85. Kroemer G, Petit P, Zamzami N et al. The biochemistry of programmed cell death. FASEB J 1995; 9: 1277–1287.

    Google Scholar 

  86. Vayssiere JL, Petite PX, Risler Y et al. Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immor talized with simian virus 40. Proc Natl Acad Sci USA 1994; 91: 11752–11756.

    Article  Google Scholar 

  87. Saks VA, Kuznetsov AV, Khuchua ZA et al. Control of cellular respiration in vivo by mitochondrial outer membrane and by cre atine kinase. A new speculative hypothesis: possible involvement of mitochondrial cytoskeleton interactions. J Mol Cell Cardiol 1995 27: 625–645.

    Article  Google Scholar 

  88. Kumar S, Harvey NL. Role of multiple cellular proteases in the execution of pro grammed cell death. FEBS Lell 1995; 375: 169–173.

    Article  Google Scholar 

  89. Martin SJ, Green DR. Protease activation during apoptosis: Death by a thousand cuts? Cell 1995; 82: 349–352.

    Article  Google Scholar 

  90. Boulakia CA, Chen G, Ng FWH et al. Bcl-2 and adenovirus E1B 19 kDa protein pre vent ElA-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene 1996; 12: 529–535.

    Google Scholar 

  91. Chinnaiyan AM, Orth K, Orourke K et al. Molecular ordering of the cell death path way—Bcl-2 and Bcl-x (L) function upstream of the CED-3-like apoptotic proteases. J Biol Chem 1996; 271: 4573–4576.

    Article  Google Scholar 

  92. Monney L, Otter I, Olivier R et al. Bcl-2 overexpression blocks activation of the death protease CPP32/Yama/apopain. Biochem Biophys Res Comm 1996; 221: 340–345.

    Article  Google Scholar 

  93. Gottlieb RA, Gruol DL, Zhu JY et al. Preconditioning in rabbit cardiomyocytes—Role of pH, vacuolar proton ATPase, and apoptosis. J Clin Invest 1996; 97: 2391–2398.

    Article  Google Scholar 

  94. Mashima T, Naito M, Fujita N et al. 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 Comm 1995; 217: 1185–1192.

    Article  Google Scholar 

  95. Kayalar C, Ord T, Testa MP et al. Cleavage of actin by interleukin 1 beta-converting enzyme to reverse DNase I inhibition. Proc Natl Acad Sei USA 1996; 93: 2234–2238.

    Article  Google Scholar 

  96. Brancolini C, Benedetti M, Schneider C. Microfilament reorganization during apoptosis: The role of Gas2, a possible substrate for ICE-like proteases. EMBO J 1995; 14: 5179–5190.

    Google Scholar 

  97. Martin SJ, Obrien, Nishioka WK et al. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J Biol Chem 1995; 270: 6425–6428.

    Article  Google Scholar 

  98. Squier MKT, Miller ACK, Malkinson AM et al. Calpain activation in apoptosis. J Cell Phys 1994; 159: 229–237.

    Article  Google Scholar 

  99. Laster SM, Mackenzie JM. Bleb formation and F-actin distribution during mitosis and tumor necrosis factor-induced apoptosis. Microscopy Res Technique 1996; 34: 272–280.

    Article  Google Scholar 

  100. Miyoshi H, Umeshita K, Sakon M et al. Calpain activation in plasma membrane bleb formation during tertbutyl hydroperoxide-induced rat hepatocyte injury. Gastroenter-ology 1996; 110: 1897–1904.

    Article  Google Scholar 

  101. Ucker DS, Obermiller PS, Eckhart W et al. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol Cell Biol 1992; 12: 3060–3069.

    Google Scholar 

  102. Peitsch MC, Polzar B, Stephan H et al. Characterization of the endogenous deox-yribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J 1993; 12: 371–377.

    Google Scholar 

  103. Peitsch MC, Mannherz HG, Tschopp J. The apoptosis endonucleases: cleaning up after cell death? Trends Cell Biol 1994; 4: 37–41.

    Article  Google Scholar 

  104. Kolber MA, Broschat KO, Landa-Gonzalez B. Cytochalasin B induces cellular DNA fragmentation. FASEB J 1990; 4: 3021–3027.

    Google Scholar 

  105. Sai]man I, Berry SJ. Cytochalasin-D treatment triggers premature apoptosis of insect ovarian follicle and nurse cells. Int J Dev Biol 1993; 37: 441–450

    Google Scholar 

  106. Samali A, Cotter TG. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 1996; 223: 163–170.

    Article  Google Scholar 

  107. Endresen PC, Prytz PS, Aarbakke J. A new flow cytometric method for discrimination of apoptotic cells and detection of their cell cycle specificity through staining of F-actin and DNA. Cytometry 1995; 20: 162–171.

    Article  Google Scholar 

  108. Radford NB, Fina M, Benjamin IJ et al. Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc Natl Acad Sei USA 1996; 93: 2339–2342.

    Article  Google Scholar 

  109. Shinohara K, Tomioka M, Nakano H et al. Apoptosis induction resulting from proteasome inhibition. Biochem J 1996; 317: 385–388.

    Google Scholar 

  110. Cheng W, Kajstura J, Nitahara J et al. Programmed myocyte cell death affects the viable myocardium after infarction in rats. Exp Cell Res 1996; 226: 316–327.

    Article  Google Scholar 

  111. Misao J, Hayakawa Y, Ohno M et al. Ex pression of Bcl-2 protein, an inhibitor of apoptosis, and bax, an accelerator of apoptosis, in ventricular myocytes of hu man hearts with myocardial infarction. Circulation 1996; 94: 1502–1512.

    Article  Google Scholar 

  112. Petit PX, Susin S-A, Zamzani N et al. Mitochondria and programmed cell death: back to the future. FEBS Lett 1996; 396: 7–13.

    Article  Google Scholar 

  113. Susin SA, Zamzani N, Castedo M et al. Bcl 2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 1996; 184: 1331–1341.

    Article  Google Scholar 

  114. Asoh S, Mori T, Hayashi J-I, Ohta S. Ex pression of the apoptosis mediator Fas is enhanced by dysfunctional mitochondria. J Biochem 1996; 120: 600–607.

    Article  Google Scholar 

  115. Mehlen P, Shulze-Osthoff K, Arrigo A-P. Small stress proteins as novel regulators of apoptosis. J Biol Chem 1996; 271: 16510–16514

    Article  Google Scholar 

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Kabakov, A.E., Gabai, V.L. (1997). Mechanisms of HSP-Mediated Protection from Ischemia-Induced Apoptosis. In: Heat Shock Proteins and Cytoprotection. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6007-4_8

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  • DOI: https://doi.org/10.1007/978-1-4615-6007-4_8

  • Publisher Name: Springer, Boston, MA

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