Role of apoptosis in cardiovascular disease

Apoptosis

Volumn 14, Issue 4, 2009, Pages 536-548

  Lee, Youngil ^a   Gustafsson, Åsa B ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Bcl 2; Death receptors; Heart failure; Mitochondria

Indexed keywords

APOPTOSIS INDUCING FACTOR; CYTOCHROME C; DEATH RECEPTOR 4; DEATH RECEPTOR 5; ENDONUCLEASE G; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI; TUMOR NECROSIS FACTOR RECEPTOR 1;

APOPTOSIS; ATHEROSCLEROSIS; AUTOPHAGY; CARDIOMYOPATHY; CELL STRESS; CONGESTIVE HEART FAILURE; ENDOPLASMIC RETICULUM; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CARDIOVASCULAR DISEASES; CELL DEATH; HUMANS; MITOCHONDRIA, HEART; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, DEATH DOMAIN;

EID: 62449157200     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-008-0302-x     Document Type: Review

References (151)

1. F Reggiori DJ Klionsky 2005 Autophagosomes: biogenesis from scratch? Curr Opin Cell Biol 17 415 422 10.1016/j.ceb.2005.06.007
2. RN Kitsis CF Peng AM Cuervo 2007 Eat your heart out Nat Med 13 539 541 10.1038/nm0507-539
3. JU Schweichel HJ Merker 1973 The morphology of various types of cell death in prenatal tissues Teratology 7 253 266 10.1002/tera.1420070306
4. J Searle JF Kerr CJ Bishop 1982 Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance Pathol Annu 17 Pt 2 229 259
5. JF Kerr 1971 Shrinkage necrosis: a distinct mode of cellular death J Pathol 105 13 20 10.1002/path.1711050103
6. G Majno I Joris 1995 Apoptosis, oncosis, and necrosis. An overview of cell death Am J Pathol 146 3 15
7. T Rich CJ Watson A Wyllie 1999 Apoptosis: the germs of death Nat Cell Biol 1 E69 E71 10.1038/11038
8. J Savill V Fadok 2000 Corpse clearance defines the meaning of cell death Nature 407 784 788 10.1038/35037722
9. G Olivetti F Quaini R Sala 1996 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 28 2005 2016 10.1006/jmcc.1996.0193
10. A Saraste K Pulkki M Kallajoki K Henriksen M Parvinen LM Voipio-Pulkki 1997 Apoptosis in human acute myocardial infarction Circulation 95 320 323
11. J Narula N Haider R Virmani 1996 Apoptosis in myocytes in end-stage heart failure N Engl J Med 335 1182 1189 10.1056/NEJM199610173351603
12. S Aharinejad O Andrukhova T Lucas 2008 Programmed cell death in idiopathic dilated cardiomyopathy is mediated by suppression of the apoptosis inhibitor Apollon Ann Thorac Surg 86 109 114 10.1016/j.athoracsur.2008.03.057 discussion 114
13. W Cheng J Kajstura JA Nitahara 1996 Programmed myocyte cell death affects the viable myocardium after infarction in rats Exp Cell Res 226 316 327 10.1006/excr.1996.0232
14. RA Gottlieb KO Burleson RA Kloner BM Babior RL Engler 1994 Reperfusion injury induces apoptosis in rabbit cardiomyocytes J Clin Invest 94 1621 1628 10.1172/JCI117504
15. HK Gao Z Yin N Zhou XY Feng F Gao HC Wang 2008 Glycogen synthase kinase 3 inhibition protects the heart from acute ischemia-reperfusion injury via inhibition of inflammation and apoptosis J Cardiovasc Pharmacol 52 286 292 10.1097/FJC.0b013e318186a84d
16. T Kubota CF McTiernan CS Frye 1997 Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha Circ Res 81 627 635
17. D Bryant L Becker J Richardson 1998 Cardiac failure in transgenic mice with myocardial expression of tumor necrosis factor-alpha Circulation 97 1375 1381
18. MR Sayen AB Gustafsson MA Sussman JD Molkentin RA Gottlieb 2003 Calcineurin transgenic mice have mitochondrial dysfunction and elevated superoxide production Am J Physiol Cell Physiol 284 C562 C570
19. J Wang JP Silva CM Gustafsson P Rustin NG Larsson 2001 Increased in vivo apoptosis in cells lacking mitochondrial DNA gene expression Proc Natl Acad Sci USA 98 4038 4043 10.1073/pnas.061038798
20. MM Kockx GR De Meyer J Muhring W Jacob H Bult AG Herman 1998 Apoptosis and related proteins in different stages of human atherosclerotic plaques Circulation 97 2307 2315
21. MC Clarke TD Littlewood N Figg 2008 Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration Circ Res 102 1529 1538 10.1161/CIRCRESAHA.108.175976
22. K Matsumura RW Jeremy J Schaper LC Becker 1998 Progression of myocardial necrosis during reperfusion of ischemic myocardium Circulation 97 795 804
23. G Takemura M Ohno Y Hayakawa 1998 Role of apoptosis in the disappearance of infiltrated and proliferated interstitial cells after myocardial infarction Circ Res 82 1130 1138
24. WB Kannel M Hjortland WP Castelli 1974 Role of diabetes in congestive heart failure: the Framingham study Am J Cardiol 34 29 34 10.1016/0002-9149(74) 90089-7
25. L Cai W Li G Wang L Guo Y Jiang YJ Kang 2002 Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway Diabetes 51 1938 1948 10.2337/diabetes.51.6.1938
26. Z Li T Zhang H Dai 2007 Involvement of endoplasmic reticulum stress in myocardial apoptosis of streptozocin-induced diabetic rats J Clin Biochem Nutr 41 58 67 10.3164/jcbn.2007008
27. KJ Mukamal RW Nesto MC Cohen 2001 Impact of diabetes on long-term survival after acute myocardial infarction: comparability of risk with prior myocardial infarction Diabetes Care 24 1422 1427 10.2337/diacare.24.8.1422
28. T Backlund E Palojoki A Saraste 2004 Sustained cardiomyocyte apoptosis and left ventricular remodelling after myocardial infarction in experimental diabetes Diabetologia 47 325 330 10.1007/s00125-003-1311-5
29. F Kuethe HH Sigusch SR Bornstein K Hilbig V Kamvissi HR Figulla 2007 Apoptosis in patients with dilated cardiomyopathy and diabetes: a feature of diabetic cardiomyopathy? Horm Metab Res 39 672 676 10.1055/s-2007-985823
30. L Cai YJ Kang 2001 Oxidative stress and diabetic cardiomyopathy: a brief review Cardiovasc Toxicol 1 181 193 10.1385/CT:1:3:181
31. Y Song J Wang Y Li 2005 Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury Am J Pathol 167 17 26
32. G Ye NS Metreveli J Ren PN Epstein 2003 Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting reactive oxygen species production Diabetes 52 777 783 10.2337/diabetes.52.3.777
33. S Guerra A Leri X Wang 1999 Myocyte death in the failing human heart is gender dependent Circ Res 85 856 866
34. D Wencker M Chandra K Nguyen 2003 A mechanistic role for cardiac myocyte apoptosis in heart failure J Clin Invest 111 1497 1504
35. A Thorburn 2004 Death receptor-induced cell killing Cell Signal 16 139 144 10.1016/j.cellsig.2003.08.007
36. X Liao X Wang Y Gu Q Chen LY Chen 2005 Involvement of death receptor signaling in mechanical stretch-induced cardiomyocyte apoptosis Life Sci 77 160 174 10.1016/j.lfs.2004.11.029
37. B Levine J Kalman L Mayer HM Fillit M Packer 1990 Elevated circulating levels of tumor necrosis factor in severe chronic heart failure N Engl J Med 323 236 241
38. DP Dutka JS Elborn F Delamere DJ Shale GK Morris 1993 Tumour necrosis factor alpha in severe congestive cardiac failure Br Heart J 70 141 143 10.1136/hrt.70.2.141
39. R Ferrari T Bachetti R Confortini 1995 Tumor necrosis factor soluble receptors in patients with various degrees of congestive heart failure Circulation 92 1479 1486
40. M Testa M Yeh P Lee 1996 Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension J Am Coll Cardiol 28 964 971 10.1016/S0735-1097(96)00268-9
41. BP Giroir JH Johnson T Brown GL Allen B Beutler 1992 The tissue distribution of tumor necrosis factor biosynthesis during endotoxemia J Clin Invest 90 693 698 10.1172/JCI115939
42. S Kapadia J Lee G Torre-Amione HH Birdsall TS Ma DL Mann 1995 Tumor necrosis factor-alpha gene and protein expression in adult feline myocardium after endotoxin administration J Clin Invest 96 1042 1052 10.1172/JCI118090
43. I Jeremias C Kupatt A Martin-Villalba 2000 Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia Circulation 102 915 920
44. G Torre-Amione S Kapadia J Lee 1996 Tumor necrosis factor-alpha and tumor necrosis factor receptors in the failing human heart Circulation 93 704 711
45. K Doyama H Fujiwara M Fukumoto 1996 Tumour necrosis factor is expressed in cardiac tissues of patients with heart failure Int J Cardiol 54 217 225 10.1016/0167-5273(96)02607-1
46. S Gilles S Zahler U Welsch CP Sommerhoff BF Becker 2003 Release of TNF-alpha during myocardial reperfusion depends on oxidative stress and is prevented by mast cell stabilizers Cardiovasc Res 60 608 616 10.1016/j.cardiores.2003.08.016
47. M Tanaka H Ito S Adachi 1994 Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes Circ Res 75 426 433
48. DR Meldrum 1998 Tumor necrosis factor in the heart Am J Physiol 274 R577 R595
49. Y Seko N Kayagaki K Seino H Yagita K Okumura R Nagai 2002 Role of Fas/FasL pathway in the activation of infiltrating cells in murine acute myocarditis caused by Coxsackievirus B3 J Am Coll Cardiol 39 1399 1403 10.1016/S0735-1097(02)01776-X
50. P Lee M Sata DJ Lefer SM Factor K Walsh RN Kitsis 2003 Fas pathway is a critical mediator of cardiac myocyte death and MI during ischemia-reperfusion in vivo Am J Physiol Heart Circ Physiol 284 H456 H463
51. Y Li G Takemura K Kosai 2004 Critical roles for the Fas/Fas ligand system in postinfarction ventricular remodeling and heart failure Circ Res 95 627 636 10.1161/01.RES.0000141528.54850.bd
52. L Gomez N Chavanis L Argaud 2005 Fas-independent mitochondrial damage triggers cardiomyocyte death after ischemia-reperfusion Am J Physiol Heart Circ Physiol 289 H2153 H2158 10.1152/ajpheart.00165.2005
53. MS Bhuiyan Y Takada N Shioda S Moriguchi J Kasahara K Fukunaga 2008 Cardioprotective effect of vanadyl sulfate on ischemia/reperfusion-induced injury in rat heart in vivo is mediated by activation of protein kinase B and induction of FLICE-inhibitory protein Cardiovasc Ther 26 10 23
54. J Niu A Azfer MF Deucher PJ Goldschmidt-Clermont PE Kolattukudy 2006 Targeted cardiac expression of soluble FAS prevents the development of heart failure in mice with cardiac-specific expression of MCP-1 J Mol Cell Cardiol 40 810 820 10.1016/j.yjmcc.2006.03.010
55. TM Scarabelli A Stephanou E Pasini 2002 Different signaling pathways induce apoptosis in endothelial cells and cardiac myocytes during ischemia/reperfusion injury Circ Res 90 745 748 10.1161/01.RES.0000015224.07870. 9A
56. AB Gustafsson JG Tsai SE Logue MT Crow RA Gottlieb 2004 Apoptosis repressor with caspase recruitment domain protects against cell death by interfering with Bax activation J Biol Chem 279 21233 21238 10.1074/jbc. M400695200
57. M Chen DJ Won S Krajewski RA Gottlieb 2002 Calpain and mitochondria in ischemia/reperfusion injury J Biol Chem 277 29181 29186 10.1074/jbc.M204951200
58. A Hamacher-Brady NR Brady SE Logue 2007 Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy Cell Death Differ 14 146 157 10.1038/sj.cdd.4401936
59. EK Iliodromitis A Lazou DT Kremastinos 2007 Ischemic preconditioning: protection against myocardial necrosis and apoptosis Vasc Health Risk Manag 3 629 637
60. K Imahashi MD Schneider C Steenbergen E Murphy 2004 Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury Circ Res 95 734 741 10.1161/01.RES.0000143898.67182.4c
61. NN Danial SJ Korsmeyer 2004 Cell death: critical control points Cell 116 205 219 10.1016/S0092-8674(04)00046-7
62. DC Huang A Strasser 2000 BH3-Only proteins-essential initiators of apoptotic cell death Cell 103 839 842 10.1016/S0092-8674(00)00187-2
63. JL Reeve E Szegezdi SE Logue 2007 Distinct mechanisms of cardiomyocyte apoptosis induced by doxorubicin and hypoxia converge on mitochondria and are inhibited by Bcl-xL J Cell Mol Med 11 509 520 10.1111/j.1582-4934.2007.00042.x
64. LA Kirshenbaum D de Moissac 1997 The bcl-2 gene product prevents programmed cell death of ventricular myocytes Circulation 96 1580 1585
65. D Zhang JL Mott SW Chang M Stevens P Mikolajczak HP Zassenhaus 2005 Mitochondrial DNA mutations activate programmed cell survival in the mouse heart Am J Physiol Heart Circ Physiol 288 H2476 H2483 10.1152/ajpheart.00670.2004
66. V Brocheriou AA Hagege A Oubenaissa 2000 Cardiac functional improvement by a human Bcl-2 transgene in a mouse model of ischemia/reperfusion injury J Gene Med 2 326 333 10.1002/1521-2254(200009/10)2:5<326::AID-JGM133>3.0. CO;2-1
67. Z Chen CC Chua YS Ho RC Hamdy BH Chua 2001 Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice Am J Physiol Heart Circ Physiol 280 H2313 H2320
68. AB Gustafsson RA Gottlieb 2007 Bcl-2 family members and apoptosis, taken to heart Am J Physiol Cell Physiol 292 C45 C51
69. DJ Milner GE Taffet X Wang 1999 The absence of desmin leads to cardiomyocyte hypertrophy and cardiac dilation with compromised systolic function J Mol Cell Cardiol 31 2063 2076 10.1006/jmcc.1999.1037
70. N Weisleder GE Taffet Y Capetanaki 2004 Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy Proc Natl Acad Sci USA 101 769 774 10.1073/pnas.0303202101
71. M Karmazyn MP Moffat 1993 Role of Na+/H+ exchange in cardiac physiology and pathophysiology: mediation of myocardial reperfusion injury by the pH paradox Cardiovasc Res 27 915 924 10.1093/cvr/27.6.915
72. L Zhu Y Yu BH Chua YS Ho TH Kuo 2001 Regulation of sodium-calcium exchange and mitochondrial energetics by Bcl-2 in the heart of transgenic mice J Mol Cell Cardiol 33 2135 2144 10.1006/jmcc.2001.1476
73. W Rouslin JL Erickson RJ Solaro 1986 Effects of oligomycin and acidosis on rates of ATP depletion in ischemic heart muscle Am J Physiol 250 H503 H508
74. K Imahashi M Schneider C Steenbergen E Murphy 2004 BCL-2 reduces acidification and the fall in ATP during Ischaemia Cardiovasc J S Afr 15 S3
75. DA Kubli MN Quinsay C Huang Y Lee AB Gustafsson 2008 Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion Am J Physiol Heart Circ Physiol 295 5 H2025 H2031
76. J Zha H Harada E Yang J Jockel SJ Korsmeyer 1996 Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L) Cell 87 619 628 10.1016/S0092-8674(00)81382-3
77. MC Wei WX Zong EH Cheng 2001 Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 727 730 10.1126/science.1059108
78. DA Kubli JE Ycaza AB Gustafsson 2007 Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak Biochem J 405 407 415 10.1042/BJ20070319
79. WX Zong T Lindsten AJ Ross GR MacGregor CB Thompson 2001 BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak Genes Dev 15 1481 1486 10.1101/gad.897601
80. M Capano M Crompton 2006 Bax translocates to mitochondria of heart cells during simulated ischaemia: involvement of AMP-activated and p38 mitogen-activated protein kinases Biochem J 395 57 64 10.1042/BJ20051654
81. A Hamacher-Brady NR Brady RA Gottlieb 2006 Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes J Biol Chem 281 29776 29787 10.1074/jbc.M603783200
82. E Hochhauser S Kivity D Offen 2003 Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice Am J Physiol Heart Circ Physiol 284 H2351 H2359
83. A Diwan M Krenz FM Syed 2007 Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice J Clin Invest 117 2825 2833 10.1172/JCI32490
84. RK Bruick 2000 Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia Proc Natl Acad Sci USA 97 9082 9087 10.1073/pnas.97.16.9082
85. N Yurkova J Shaw K Blackie 2008 The cell cycle factor E2F-1 activates Bnip3 and the intrinsic death pathway in ventricular myocytes Circ Res 102 472 479 10.1161/CIRCRESAHA.107.164731
86. DP Frazier A Wilson RM Graham JW Thompson NH Bishopric KA Webster 2006 Acidosis regulates the stability, hydrophobicity, and activity of the BH3-only protein Bnip3 Antioxid Redox Signal 8 1625 1634 10.1089/ars.2006.8.1625
87. KM Regula K Ens LA Kirshenbaum 2002 Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes Circ Res 91 226 231 10.1161/01.RES.0000029232.42227.16
88. VC Vande J Cizeau D Dubik 2000 BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore Mol Cell Biol 20 5454 5468 10.1128/MCB.20.15.5454-5468.2000
89. A Diwan J Wansapura FM Syed SJ Matkovich JN Lorenz GW Dorn II 2008 Nix-mediated apoptosis links myocardial fibrosis, cardiac remodeling, and hypertrophy decompensation Circulation 117 396 404 10.1161/CIRCULATIONAHA.107. 727073
90. M Chen H He S Zhan S Krajewski JC Reed RA Gottlieb 2001 Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion J Biol Chem 276 30724 30728 10.1074/jbc.M103701200
91. CL Murriel E Churchill K Inagaki LI Szweda D Mochly-Rosen 2004 Protein kinase Cdelta activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria J Biol Chem 279 47985 47991 10.1074/jbc.M405071200
92. N Latif MA Khan E Birks 2000 Upregulation of the Bcl-2 family of proteins in end stage heart failure J Am Coll Cardiol 35 1769 1777 10.1016/S0735- 1097(00)00647-1
93. P Di Napoli AA Taccardi A Grilli 2003 Left ventricular wall stress as a direct correlate of cardiomyocyte apoptosis in patients with severe dilated cardiomyopathy Am Heart J 146 1105 1111 10.1016/S0002-8703(03)00445-9
94. A Baldi A Abbate R Bussani 2002 Apoptosis and post-infarction left ventricular remodeling J Mol Cell Cardiol 34 165 174 10.1006/jmcc.2001.1498
95. AK Sharma S Dhingra N Khaper PK Singal 2007 Activation of apoptotic processes during transition from hypertrophy to heart failure in guinea pigs Am J Physiol Heart Circ Physiol 293 H1384 H1390 10.1152/ajpheart.00553.2007
96. P Li D Nijhawan I Budihardjo 1997 Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 479 489 10.1016/S0092-8674(00)80434-1
97. D Acehan X Jiang DG Morgan JE Heuser X Wang CW Akey 2002 Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation Mol Cell 9 423 432 10.1016/S1097-2765(02) 00442-2
98. X Jiang X Wang 2000 Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1 J Biol Chem 275 31199 31203 10.1074/jbc.C000405200
99. P Pacher C Szabo 2007 Role of poly(ADP-ribose) polymerase 1 (PARP-1) in cardiovascular diseases: the therapeutic potential of PARP inhibitors Cardiovasc Drug Rev 25 235 260 10.1111/j.1527-3466.2007.00018.x
100. RA de Boer DJ van Veldhuisen J van der Wijk 2000 Additional use of immunostaining for active caspase 3 and cleaved actin and PARP fragments to detect apoptosis in patients with chronic heart failure J Card Fail 6 330 337 10.1054/jcaf.2000.20457
101. N Vahsen C Cande JJ Briere 2004 AIF deficiency compromises oxidative phosphorylation EMBO J 23 4679 4689 10.1038/sj.emboj.7600461
102. N Joza GY Oudit D Brown 2005 Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy Mol Cell Biol 25 10261 10272 10.1128/MCB.25.23.10261-10272.2005
103. VP van Empel AT Bertrand R van der Nagel 2005 Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation Circ Res 96 e92 e101 10.1161/01.RES.0000172081.30327.28
104. E Norberg V Gogvadze M Ott 2008 An increase in intracellular Ca(2+) is required for the activation of mitochondrial calpain to release AIF during cell death Cell Death Differ 15 12 1857 1864
105. E Daugas SA Susin N Zamzami 2000 Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis FASEB J 14 729 739
106. AP Halestrap 2006 Calcium, mitochondria and reperfusion injury: a pore way to die Biochem Soc Trans 34 232 237 10.1042/BST20060232
107. J Garcia-Rivas Gde K Carvajal F Correa C Zazueta 2006 Ru360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischaemic functional recovery in rats in vivo Br J Pharmacol 149 829 837 10.1038/sj.bjp.0706932
108. J Wang Z Zhang Y Hu 2007 SEA0400, a novel Na(+)/Ca(2+) exchanger inhibitor, reduces calcium overload induced by ischemia and reperfusion in mouse ventricular myocytes Physiol Res 56 17 23
109. GT Kim YS Chun JW Park MS Kim 2003 Role of apoptosis-inducing factor in myocardial cell death by ischemia-reperfusion Biochem Biophys Res Commun 309 619 624 10.1016/j.bbrc.2003.08.045
110. ZF Song XP Ji XX Li SJ Wang SH Wang Y Zhang 2008 Inhibition of the activity of poly (ADP-ribose) polymerase reduces heart ischaemia/reperfusion injury via suppressing JNK-mediated AIF translocation J Cell Mol Med 12 1220 1228 10.1111/j.1582-4934.2008.00183.x
111. N Roy QL Deveraux R Takahashi GS Salvesen JC Reed 1997 The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases EMBO J 16 6914 6925 10.1093/emboj/16.23.6914
112. QL Deveraux R Takahashi GS Salvesen JC Reed 1997 X-linked IAP is a direct inhibitor of cell-death proteases Nature 388 300 304 10.1038/40901
113. HR Liu E Gao A Hu 2005 Role of Omi/HtrA2 in apoptotic cell death after myocardial ischemia and reperfusion Circulation 111 90 96 10.1161/01.CIR. 0000151613.90994.17
114. MS Bhuiyan K Fukunaga 2007 Inhibition of HtrA2/Omi ameliorates heart dysfunction following ischemia/reperfusion injury in rat heart in vivo Eur J Pharmacol 557 168 177 10.1016/j.ejphar.2006.10.067
115. CC Chua J Gao YS Ho 2007 Overexpression of IAP-2 attenuates apoptosis and protects against myocardial ischemia/reperfusion injury in transgenic mice Biochim Biophys Acta 1773 577 583
116. S Ikeda K Ozaki 1997 Action of mitochondrial endonuclease G on DNA damaged by L-ascorbic acid, peplomycin, and cis-diamminedichloroplatinum (II) Biochem Biophys Res Commun 235 291 294 10.1006/bbrc.1997.6786
117. S Javadov A Choi V Rajapurohitam A Zeidan AG Basnakian M Karmazyn 2008 NHE-1 inhibition-induced cardioprotection against ischaemia/reperfusion is associated with attenuation of the mitochondrial permeability transition Cardiovasc Res 77 416 424 10.1093/cvr/cvm039
118. N Bahi J Zhang M Llovera M Ballester JX Comella D Sanchis 2006 Switch from caspase-dependent to caspase-independent death during heart development: essential role of endonuclease G in ischemia-induced DNA processing of differentiated cardiomyocytes J Biol Chem 281 22943 22952 10.1074/jbc.M601025200
119. E Szegezdi SE Logue AM Gorman A Samali 2006 Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 880 885 10.1038/sj.embor.7400779
120. C Xu B Bailly-Maitre JC Reed 2005 Endoplasmic reticulum stress: cell life and death decisions J Clin Invest 115 2656 2664 10.1172/JCI26373
121. K Okada T Minamino Y Tsukamoto 2004 Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis Circulation 110 705 712 10.1161/01.CIR.0000137836.95625.D4
122. E Szegezdi A Duffy ME O'Mahoney 2006 ER stress contributes to ischemia-induced cardiomyocyte apoptosis Biochem Biophys Res Commun 349 1406 1411 10.1016/j.bbrc.2006.09.009
123. DJ Thuerauf M Marcinko N Gude M Rubio MA Sussman CC Glembotski 2006 Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes Circ Res 99 275 282 10.1161/01.RES.0000233317.70421. 03
124. A Azfer J Niu LM Rogers FM Adamski PE Kolattukudy 2006 Activation of endoplasmic reticulum stress response during the development of ischemic heart disease Am J Physiol Heart Circ Physiol 291 H1411 H1420 10.1152/ajpheart.01378. 2005
125. CV Jackson GM McGrath AG Tahiliani RV Vadlamudi JH McNeill 1985 A functional and ultrastructural analysis of experimental diabetic rat myocardium.Manifestation of a cardiomyopathy Diabetes 34 876 883 10.2337/diabetes.34.9.876
126. H Hamada M Suzuki S Yuasa 2004 Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice Mol Cell Biol 24 8007 8017 10.1128/MCB.24.18.8007-8017.2004
127. DG Breckenridge M Germain JP Mathai M Nguyen GC Shore 2003 Regulation of apoptosis by endoplasmic reticulum pathways Oncogene 22 8608 8618 10.1038/sj.onc.1207108
128. X Qi A Vallentin E Churchill D Mochly-Rosen 2007 deltaPKC participates in the endoplasmic reticulum stress-induced response in cultured cardiac myocytes and ischemic heart J Mol Cell Cardiol 43 420 428 10.1016/j.yjmcc.2007.07.061
129. A Toth JR Jeffers P Nickson 2006 Targeted deletion of puma attenuates cardiomyocyte death and improves cardiac function during ischemia-reperfusion Am J Physiol Heart Circ Physiol 291 1 H52 H60
130. P Nickson A Toth P Erhardt 2007 PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress Cardiovasc Res 73 48 56 10.1016/j.cardiores.2006.10.001
131. L Scorrano SA Oakes JT Opferman 2003 BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis Science 300 135 139 10.1126/science.1081208
132. X Luo I Budihardjo H Zou C Slaughter X Wang 1998 Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors Cell 94 481 490 10.1016/S0092- 8674(00)81589-5
133. H Li H Zhu CJ Xu J Yuan 1998 Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis Cell 94 491 501 10.1016/S0092-8674(00)81590-1
134. T Date S Mochizuki AJ Belanger 2003 Differential effects of membrane and soluble Fas ligand on cardiomyocytes: role in ischemia/reperfusion injury J Mol Cell Cardiol 35 811 821 10.1016/S0022-2828(03)00139-1
135. SB Haudek GE Taffet MD Schneider DL Mann 2007 TNF provokes cardiomyocyte apoptosis and cardiac remodeling through activation of multiple cell death pathways J Clin Invest 117 2692 2701 10.1172/JCI29134
136. M Kalai M Lamkanfi G Denecker 2003 Regulation of the expression and processing of caspase-12 J Cell Biol 162 457 467 10.1083/jcb.200303157
137. G Bajaj RK Sharma 2006 TNF-alpha-mediated cardiomyocyte apoptosis involves caspase-12 and calpain Biochem Biophys Res Commun 345 1558 1564 10.1016/j.bbrc.2006.05.059
138. E Gyan E Frisan O Beyne-Rauzy 2008 Spontaneous and Fas-induced apoptosis of low-grade MDS erythroid precursors involves the endoplasmic reticulum Leukemia 22 1864 1873 10.1038/leu.2008.172
139. DG Breckenridge M Stojanovic RC Marcellus GC Shore 2003 Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol J Cell Biol 160 1115 1127 10.1083/jcb.200212059
140. JP Mathai M Germain GC Shore 2005 BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death J Biol Chem 280 23829 23836 10.1074/jbc.M500800200
141. A Nakai O Yamaguchi T Takeda 2007 The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress Nat Med 13 619 624 10.1038/nm1574
142. Y Matsui H Takagi X Qu 2007 Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy Circ Res 100 914 922 10.1161/01.RES.0000261924. 76669.36
143. H Zhu P Tannous JL Johnstone 2007 Cardiac autophagy is a maladaptive response to hemodynamic stress J Clin Invest 117 1782 1793 10.1172/JCI27523
144. L Yan DE Vatner SJ Kim 2005 Autophagy in chronically ischemic myocardium Proc Natl Acad Sci USA 102 13807 13812 10.1073/pnas.0506843102
145. S Yousefi R Perozzo I Schmid 2006 Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis Nat Cell Biol 8 1124 1132 10.1038/ncb1482
146. JO Pyo MH Jang YK Kwon 2005 Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death J Biol Chem 280 20722 20729 10.1074/jbc.M413934200
147. S Pattingre A Tassa X Qu 2005 Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy Cell 122 927 939 10.1016/j.cell.2005.07.002
148. MC Maiuri A Criollo E Tasdemir 2007 BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L) Autophagy 3 374 376
149. R Rashmi SG Pillai S Vijayalingam J Ryerse G Chinnadurai 2008 BH3-only protein BIK induces caspase-independent cell death with autophagic features in Bcl-2 null cells Oncogene 27 1366 1375 10.1038/sj.onc.1210783
150. U Akar A Chaves-Reyez M Barria 2008 Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells Autophagy 4 669 679
151. R Ray G Chen VC Vande 2000 BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites J Biol Chem 275 1439 1448 10.1074/jbc.275.2.1439