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
Martin SJ. Apoptosis: suicide, execution or murder? Trends Cell Biology 1993; 3: 141–144.
Martin SJ, Green DR, Cotter TG. Dicing with death: dissecting the components of the apoptosis machinery. Trends Biochem Sci 1994; 19: 26–30.
McConkey DJ, Orrenius S. Signal transduc-tion pathways to apoptosis. Trends Cell Biol 1994; 4: 370–375.
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.
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.
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.
Cummings MC. Increased p53 mRNA ex pression in liver and kidney apoptosis. Biochim Biophys Acta 1996; 1315:100–104.
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.
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.
Brugarolas J, Chandrasekaran C, Gordon JI et al. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995; 377: 552–557.
Hooper ML. The role of the p53 and Rb-1 genes in cancer, development and apoptosis. J Cell Sci 1994; 18: 13–17.
Donehower LA, Bradly A. The tumor sup pressor p53. Biochim Biophys Acta 1993; 1155: 181–205.
Montenarh M. Biochemical properties of the growth suppressor/oncoprotein p53. Onco-gene 1992; 7: 1673–1680.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Maki CG, Huibregtse JM, Howley PM. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 1996; 56: 2649–2654.
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.
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.
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.
Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell 1994; 79: 13–21.
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.
Richter C, Schweizer M, Cossarizza A et al. Control of apoptosis by the cellular ATP level. FEBS Lett 1996; 378: 107–110.
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.
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.
Mosser DD, Martin LH. Induced thermo tolerance to apoptosis in a human T lym phocyte cell line. J Cell Physiol 1992; 151: 561–570.
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.
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.
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.
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.
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.
Smeyne RJ, Vendrell M, Hayward M et al. Continuous c-fos expression precedes pro grammed cell death in vivo. Nature 1993; 363: 166–169.
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.
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.
Bonfoco E, Ceccatelli S, Manzo L et al. Colchicine induces apoptosis in cerebellar granule cells. Exp Cell Res 1995; 218: 189–200.
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.
Ireland CM, Pittman SM. Tubulin alter ations in taxol-induced apoptosis parallel those observed with other drugs. Biochem Pharmacol 1995; 49: 1491–1499.
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.
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.
Wei Y, Zhao X, Kariya Y et al. Induction of apoptosis by quercetin: Involvement of heat shock protein. Cancer Res 1994; 54: 4952–4957.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Umansky SR, Cuenco GM, Khutzian SS et al. Post-ischemic apoptotic death of rat neonatal cardiomyocytes. Cell Death Diff 1995; 2: 235–241.
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.
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.
Weil’ M, Jacobson MD, Coles HSR et al. Constitutive expression of the machinery for programmed cell death. J Cell Biol 1996; 133: 1053–1059.
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.
Raff MC. Social controls on cell survival and cell death. Nature 1992; 356: 397–400.
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.
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.
Rutherford SL, Zuker CS. Protein folding and the regulation of signaling pathways. Cell 1994; 79: 1129–1132.
Reed JC. Bcl-2 and the regulation of pro grammed cell death. J Cell Biol 1994; 124: 1–6.
Hockenbery DM. bcl-2 in cancer, develop ment and apoptosis. J Cell Sci 1994; 18: 51–55.
Chiou S-K, Rao L, White E. Bcl-2 blocks p53-dependent apoptosis. Mol Cell Biol 1994; 14: 2556–2563.
Schott AF, Apel IJ, Nunez G et al. Bcl-x(L) protects cancer cells from p53-mediated apoptosis. Oncogene 1995; 11: 1389–1394.
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.
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.
Shimizu S, Eguchi Y, Kamiike W et al. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene 1996; 12: 2251–2257.
Jacobson MD, Raff MC. Programmed cell death and Bcl-2 protection in very low oxygen. Nature 1995; 374: 814–816.
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
Distelhorst CW, Lam M, Mccormick TS. Bcl-2 inhibits hydrogen peroxide-induced ER Ca2+ pool depletion. Oncogene 1996; 12: 2051–2055.
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.
Tsujimoto Y. Stress-resistance conferred by high level of bcl-2 alpha protein in human B lymphoblastoid cell. Oncogene 1989; 4: 1331–1336.
Strasser A, Anderson RL. Bcl-2 and thermotolerance cooperate in cell survival. Cell Growth Diff 1995; 6: 799–805.
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.
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.
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.
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.
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.
Kroemer G, Petit P, Zamzami N et al. The biochemistry of programmed cell death. FASEB J 1995; 9: 1277–1287.
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.
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.
Kumar S, Harvey NL. Role of multiple cellular proteases in the execution of pro grammed cell death. FEBS Lell 1995; 375: 169–173.
Martin SJ, Green DR. Protease activation during apoptosis: Death by a thousand cuts? Cell 1995; 82: 349–352.
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.
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.
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.
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.
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.
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.
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.
Martin SJ, Obrien, Nishioka WK et al. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J Biol Chem 1995; 270: 6425–6428.
Squier MKT, Miller ACK, Malkinson AM et al. Calpain activation in apoptosis. J Cell Phys 1994; 159: 229–237.
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.
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.
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.
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.
Peitsch MC, Mannherz HG, Tschopp J. The apoptosis endonucleases: cleaning up after cell death? Trends Cell Biol 1994; 4: 37–41.
Kolber MA, Broschat KO, Landa-Gonzalez B. Cytochalasin B induces cellular DNA fragmentation. FASEB J 1990; 4: 3021–3027.
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
Samali A, Cotter TG. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 1996; 223: 163–170.
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.
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.
Shinohara K, Tomioka M, Nakano H et al. Apoptosis induction resulting from proteasome inhibition. Biochem J 1996; 317: 385–388.
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.
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.
Petit PX, Susin S-A, Zamzani N et al. Mitochondria and programmed cell death: back to the future. FEBS Lett 1996; 396: 7–13.
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.
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.
Mehlen P, Shulze-Osthoff K, Arrigo A-P. Small stress proteins as novel regulators of apoptosis. J Biol Chem 1996; 271: 16510–16514
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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
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