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European Heart Journal 1999 20(22):1619-1629; doi:10.1053/euhj.1999.1548
Copyright © 1999 by the European Society of Cardiology.
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Review

Cardiac myocyte apoptosis

S.A. Cookf1 and P.A. Poole-Wilson

National Heart and Lung Institute Division, Imperial College School of Medicine, Dovehouse Street, London, U.K.

Received December 1, 1998; accepted February 3, 1999

Key Words: Apoptosis, TUNEL, caspase, Bcl-2, mitogen-activated protein kinases.

f1 Correspondence: Dr Stuart Cook, NHLI Division (Cardiac Medicine), Imperial College School of Medicine, Dovehouse Street, London SW3 6LY, U.K.

References

  1. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer. 1971;26:239–257
  2. Wyllie AH, Duvall E. Cell injury and death. In: McGee JO’D, Isaacson PG, Wright NA, eds. Oxford Textbook of Pathology. Glasgow: William Collins & Sons & Co; 1992. p. 142–57
  3. Yuan J. Evolutionary conservation of genetic pathway of programmed cell death. J Cell Biochem. 1996;60:4–11[CrossRef][ISI][Medline]
  4. Allen RT, Hunter WJ, Agrawal DK. Morphological and biochemical characterisation and analysis of apoptosis. J Pharmacol Toxicol Methods. 1997;37:215–228[CrossRef][ISI][Medline]
  5. Vermes I, Haanen C, Steffens Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidyl-serine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods. 1995;184:39–51[CrossRef][ISI][Medline]
  6. Sgonc R, Boeck G, Dietrich H, Gruber J, Recheis H, Wick G. Simultaneous determination of cell surface antigens and apoptosis. Trends Genet. 1994;10:41–42[CrossRef][ISI][Medline]
  7. Chiu L, Cherwinski H, Ransom J, Dunne JF. Flow cytometric ratio analysis of the Hoescht 33342 emission spectrum: multiparametric characterisation of apoptotic lymphocytes. J Immunol Methods. 1996;189:157–171[CrossRef][ISI][Medline]
  8. Frey T. Nucleic acid dyes for detection of apoptosis in live cells. Cytometry. 1995;21:265–274[CrossRef][ISI][Medline]
  9. Gavrieli Y, Sherman Y, Ben Sasson SA. Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J Cell Biol. 1992;119:493–501[Abstract/Free Full Text]
  10. Negoescu A. TUNEL: Improvement and evaluation of the method for In Situ Apoptotic cell identification. Biochemica. 1997;2:12–17[Medline]
  11. Buja LM, Entman ML. Modes of myocardial cell injury and cell death in ischemic heart disease. Circulation. 1998;98:1355–1357[Free Full Text]
  12. Adams JM, Cory S. The Bcl-2 protein family: Arbiters of cell survival. Science. 1998;281:1322–1326[Abstract/Free Full Text]
  13. Cohen GM. Caspases: the executioners of apoptosis. Biochem J. 1998;326:1–16
  14. Sakahira H, Enari E, Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 1998;391:96–99[CrossRef][Medline]
  15. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 1995;270:1326–1331[Abstract/Free Full Text]
  16. Cleveland JL, Ihle JN. Contenders in Fas/TNF cell signalling. Cell. 1998;81:479–482
  17. Yue T-L, Wang C, Romanic A. Staurosporine-induced Apoptosis in Cardiomyocytes: A Potential role for Caspase-3. J Mol Cell Cardiol. 1998;30:495–507[CrossRef][ISI][Medline]
  18. Black SC, Huang JQ, Rezaiefar P. Co-localization of the cysteine protease caspase-3 with apoptotic myocytes after in vivo myocardial ischaemia and reperfusion in the rat. J Mol Cell Cardiol. 1998;30:733–742[CrossRef][ISI][Medline]
  19. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Attenuation of ischaemia/reperfusion injury in rats by a caspase inhibitor. Circulation. 1998;97:276–281[Abstract/Free Full Text]
  20. Meldrum DR. Tumour necrosis factor in the heart. Am J Physiol. 1998;274:R577–R595[ISI][Medline]
  21. Kuwana T, Smith JJ, Muzio M, Dixit V, Newmeyer DD, Kornbluth S. Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome- c. J Biol Chem. 1998;273:16589–16594[Abstract/Free Full Text]
  22. Hu Y, Benedict MA, Wu D, Inohara N, Nunez G. Bcl-Xlinteracts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci U S A. 1998;95:4386–4391[Abstract/Free Full Text]
  23. Cai J, Jones DP. Superoxide in Apoptosis. J Biol Chem. 1998;273:11401–11404[Abstract/Free Full Text]
  24. Stridh H, Kimland M, Jones DP, Orrenius S, Hampton MB. Cytochrome- c release and caspase activation in hydrogen peroxide- and tributylin-induced apoptosis. FEBS Lett. 1998;429:351–355[CrossRef][ISI][Medline]
  25. Kuida K, Haydar TF, Kuan C-Y. Reduced Apoptosis and Cytochrome- c Mediated Caspase Activation in Mice Lacking Caspase 9. Cell. 1998;94:325–337[CrossRef][ISI][Medline]
  26. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309–1312[Abstract/Free Full Text]
  27. Otter I, Conus S, Ravn U. The binding properties and the biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli. J Biol Chem. 1998;273:6110–6120[Abstract/Free Full Text]
  28. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO. 1998;17:3878–3885[CrossRef][ISI][Medline]
  29. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homologue, Bax, that accelerates programmed cell death. Cell. 1998;74:609–619
  30. Yang E, Zha J, Jockel J, Boise LH, Thompson CB. Bad, a heterodimeric partner for Bcl-xland Bcl-2, displaces Bax and promotes cell death. Cell. 1995;80:285–291[CrossRef][ISI][Medline]
  31. Maundrell K, Antonsson B, Magnenant E. BCL-2 undergoes phosphorylation by c-JUN N-terminal kinase/stress-activated protein kinases in the presence of the constitutively active GTP-binding protein Rac1. J Biol Chem. 1997;272:25238–25242[Abstract/Free Full Text]
  32. Horiuchi M, Hayashida W, Kambe T, Yamada T, Dzau VJ. Angiotensin Type 2 receptor dephosphorylates Bcl-2 by activating mitogen-activated protein kinase phosphatase-1 and induces apoptosis. J Biol Chem. 1997;272:19022–19026[Abstract/Free Full Text]
  33. Gajewski TF, Thompson CB. Apoptosis meets signal transduction. Elimination of a BAD Influence. Cell. 1996;87:589–592[CrossRef][ISI][Medline]
  34. Datta SR, Dudek H, Tao X. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231–241[CrossRef][ISI][Medline]
  35. Zhou H, Summers SA, Birnbaum JM, Pittman RN. Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J Biol Chem. 1998;273:16568–16575[Abstract/Free Full Text]
  36. Wang H, Rapp UR, Reed JC. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell. 1996;87:629–638[CrossRef][ISI][Medline]
  37. Scheid MP, Duronio V. Dissociation of cytokine-induced phosphorylation of Bad and the activation of PKB/akt: Involvement of MEK upstream of Bad phosphorylation. Proc Natl Acad Sci U S A. 1998;95:7439–7444[Abstract/Free Full Text]
  38. Kirshenbaum LA, de Moissac D. The bcl-2 gene product prevents programmed cell death of ventricular myocytes. Circulation. 1997;96:1580–1585[Abstract/Free Full Text]
  39. Olivetti G, Abbi R, Quaini F. Apoptosis in the failing human heart. N Engl J Med. 1997;336:1131–1141[Abstract/Free Full Text]
  40. Krown K, Page TP, Nguyen C. Tumour necrosis factor alpha-induced apoptosis in cardiac myocytes. J Clin Invest. 1996;98:2854–2865[ISI][Medline]
  41. Aikawa R, Komuro I, Yamazaki T. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest. 1997;100:1812–1813
  42. Wu C, Bishopric NH, Pratt RE. Atrial naturetic peptide induces apoptosis in neonatal rat cardiac myocytes. J Biol Chem. 1997;272:14860–14866[Abstract/Free Full Text]
  43. Tanaka M, Ito H, Adachi S. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ Res. 1994;75:426–433[Abstract/Free Full Text]
  44. Cheng W, Li B, Kajstura J. Stretch-induced programmed myocyte cell death. J Clin Invest. 1995;96:2247–2259[ISI][Medline]
  45. Robb MacLellan W, Schneider MD. Death by design. Circ Res. 1997;81:137–144[Abstract/Free Full Text]
  46. French L, Hahne M, Viard I. Fas and Fas ligand in embryos and adult mice : ligand expression in several immune-priviliged tissues and coexpression in adult tissues characterised by apoptotic cell turnover. J Cell Biol. 1998;133:335–343
  47. Schlegel J, Peters I, Orrenius S. CPP32/Apopain Is a Key Interleukin-1ß converting enzyme-like protease involved in Fas-mediated apoptosis. J Biol Chem. 1996;271:1841–1844[Abstract/Free Full Text]
  48. Martin DA, Siegel RM, Zheng L, Lenardo MJ. Membrane oligomerization and cleavage activates the Caspase-8 (FLICE/MACH{alpha}1) death signal. J Biol Chem. 1998;273:4345–4349[Abstract/Free Full Text]
  49. Granville DJ, Carthy CM, Hunt DWC, McManus BM. Apoptosis: molecular aspects of cell death and disease. Lab Invest. 1998;78:893–913[ISI][Medline]
  50. Irmler M, Thome M, Hahne M. Inhibition of death-receptor signals by cellular FLIP. Nature. 1997;388:190–195[CrossRef][Medline]
  51. Gotoh Y, Cooper JA. Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumour necrosis factor-{alpha} signal transduction. J Biol Chem. 1998;273:17477–17482[Abstract/Free Full Text]
  52. Dutka DP, Elborn JS, Delamere F, Shale DJ, Morris GK. Tumour necrosis factor alpha in severe congestive cardiac failure. Br Heart J. 1993;70:141–143[Abstract/Free Full Text]
  53. Toyozaki T, Hiroe M, Tanaka M, Nagata S, Ohwada H, Marumo F. Levels of soluble Fas ligand in myocarditis. Am J Cardiol. 1998;82:246–248[CrossRef][ISI][Medline]
  54. Nishigaki K, Minatoguchi S, Seishima M. Plasma Fas ligand, an inducer of apoptosis, and plasma soluble Fas, an inhibitor of apoptosis, in patients with chronic congestive heart failure. J Am Coll Cardiol. 1997;29:1214–1220[Abstract]
  55. Evan G, Littlewood T. A matter of life and cell death. Science. 1998;281:1317–1321[Abstract/Free Full Text]
  56. Bogoyevitch MA, Gillespie-Brown J, Ketterman AJ. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ Res. 1996;79:162–173[Abstract/Free Full Text]
  57. Cohen P. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trend Cell Biol. 1997;7:353–361[CrossRef][ISI][Medline]
  58. Sugden PH, Clerk A. ‘Stress-responsive’ mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ Res. 1998;83:345–352[Free Full Text]
  59. Palmero I, Pantoja C, Serrano M. p19ARFlinks tumour suppressor p53 to Ras. Nature. 1998;395:125–126[CrossRef][Medline]
  60. Pierzchalski P, Reiss K, Cheng W. p53 Induces Myocyte Apoptosis via the Activation of the Renin-Angiotensin System. Exp Cell Res. 1997;234:57–65[CrossRef][ISI][Medline]
  61. Bialik S, Geenen D, Sasson IE. Myocyte Apoptosis During Acute Myocardial Infarction in the Mouse Localises to Hypoxic Regions but Occurs Independently of p53. J Clin Invest. 1997;100:1363–1372[ISI][Medline]
  62. Sugden PH, Clerk A. Regulation of the ERK subgroup of MAP kinase cascades through G protein-coupled receptors. Cell Signalling. 1997;9:337–351[CrossRef][ISI][Medline]
  63. Wang X, Martindale JL, Liu Y, Holbrook NJ. The cellular response to oxidative stress: influences of the mitogen-activated protein kinase signalling pathways on cell survival. Biochem J. 1998;333:291–300[ISI][Medline]
  64. Guo Y-L, Baysal K, Kang B, Yang L-J, Williamson JR. Correlation between Sustained c-Jun N-terminal Protein Kinase Activation and Apoptosis Induced by Tumor Necrosis Factor-{alpha} in Rat Mesangial Cells. J Biol Chem. 1998;273:4027–4034[Abstract/Free Full Text]
  65. Li GW, Zaheer A, Coppey L, Oskarsson HJ. Activation of JNK in the remote myocardium after large myocardial infarction in rats. Biochem Biophys Res Commun. 1998;246:816–820[CrossRef][ISI][Medline]
  66. Ichijo H, Nishida E, Irie K. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signalling pathways. Science. 1998;275:90–94
  67. Schwenger P, Bellosta P, Vietor I, Basilico C, Skolnik EY, Vilcek J. Sodium salicylate induces apoptosis via p38 mitogen-activated protein kinase but inhibits tumor necrosis factor-induced c-Jun N-terminal kinase/stress-activated protein kinase activation. Proc Natl Acad Sci U S A. 1997;94:2869–2873[Abstract/Free Full Text]
  68. Nemoto S, Xiang J, Huang S, Lin A. Induction of apoptosis by SB202190 through inhibition of p38ß mitogen-activated protein kinase. J Biol Chem. 1998;273:16415–16420[Abstract/Free Full Text]
  69. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown J, Chien KR. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase dependent pathway. J Biol Chem. 1997;9:5783–5791
  70. Roulston A, Reinhard C, Amiri P, Williams LT. Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in the response to tumor necrosis Factor-{alpha}. J Biol Chem. 1998;273:10232–10239[Abstract/Free Full Text]
  71. Koseki T, Inohara N, Chen S, Nunez G. ARC, an inhibitor of apoptosis expressed in skeletal muscle and heart that interacts selectively with caspases. Proc Natl Acad Sci U S A. 1998;95:5156–5160[Abstract/Free Full Text]
  72. Deveraux QL, Roy N, Stennicke HR. IAPs block apoptotic events induced by caspase-8 and cytochrome- c by direct inhibition of distinct caspases. EMBO. 1998;17:2215–2223[CrossRef][ISI][Medline]
  73. Malinin NL, Boldin MP, Kovalenko AV, Wallach D. MAP3K-related kinase involved in NF-{kappa}B induction by TNF, CD-95 and IL-1. Nature. 1997;385:540–544[CrossRef][Medline]
  74. Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH, Ballard DW. Suppression of tumour necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-{kappa}B control. Proc Natl Acad Sci U S A. 1997;94:10057–10062[Abstract/Free Full Text]
  75. Narula J, Haider N, Virmani R. Apoptosis in myocytes in end-stage heart failure. N Engl J Med. 1996;335:1182–1189[Abstract/Free Full Text]
  76. Olivetti G, Quaini F, Sala R. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol. 1994;28:2005–2016[CrossRef]
  77. Saraste A, Pulkki K, Kallajoki M, Henriksen K, Parvinene M, Voipio-Pulkki L-M. Apoptosis in human acute myocardial infarction. Circulation. 1997;95:320–323[Abstract/Free Full Text]
  78. Mallat Z, Tedgui A, Fontaliran F, Frank R, Durigon M, Fontaine G. Evidence of apoptosis in arrhythmogenic right ventricular dysplasia. N Engl J Med. 1996;335:1224–1226[Free Full Text]
  79. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. Apaf-1 (CED-4 Homolog) Regulates Programmed Cell Death in Mammalian Development. Cell. 1998;94:727–737[CrossRef][ISI][Medline]
  80. Sharov VG, Sabbah HN, Shimoyama H, Goussev AV, Lesch M, Goldstein S. Evidence of cardiocyte apoptosis in myocardium of dogs with chronic heart failure. Am J Pathol. 1996;148:141–149[Abstract]
  81. Kajstura J, Zhang X, Liu Y. The cellular basis of pacing-induced dilated cardiomyopathy. Myocyte cell loss and myocyte cellular reactive hypertrophy. Circulation. 1995;92:2306–2317[Abstract/Free Full Text]
  82. Li Z, Bing OH, Long X, Robinson KG, Lakatta EG. Increased cardiomyocyte apoptosis during the transition to heart failure in the spontaneously hypertensive rat. Am J Physiol. 1997;272:H2313–H2319[ISI][Medline]
  83. Kajstura J, Cheng W, Reiss K. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest. 1996;74:86–107[ISI][Medline]
  84. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest. 1994;94:1621–1628[ISI][Medline]
  85. Ambrosio G, Zweier JL, Becker LC. Apoptosis is prevented by administration of superoxide dismutase in dogs with reperfused myocardium. Basic Res Cardiol. 1998;93:94–96[CrossRef][ISI][Medline]
  86. Piot CA, Padmanaban D, Ursell PC, Sievers RE, Wolfe CL. Ischaemic Preconditioning Decreases Apoptosis in Rat Hearts In Vivo. Circulation. 1997;96:1598–1604[Abstract/Free Full Text]
  87. Cohen MZ. Free radicals in ischaemic and reperfusion myocardial injury: is this the time for clinical trials? Annals of Internal Medicine. 1989;111:918–931[ISI][Medline]
  88. Mallat Z, Philip I, Lebret M, Chatel D, Maclouf J, Tedgui A. Elevated Levels of 8-iso-Prostaglandin F2{alpha}in Pericardial Fluid of Patients With Heart Failure. Circulation. 1998;97:1536–1539[Abstract/Free Full Text]
  89. Feuerstein G, Bril A, Ruffolo R. Protective effects of carvedilol in the myocardium. Am J Cardiol. 1997;80:41L–45L[CrossRef][Medline]
  90. Doughty RN, Rodgers A, Sharpe N, MacMahon S. Effects of beta-blocker therapy on mortality in patients with heart failure. Eur Heart J. 1997;18:560–565[Abstract/Free Full Text]

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