Mechanisms and inhibitors of apoptosis in cardiovascular diseases

Current Pharmaceutical Design

Volumn 17, Issue 18, 2011, Pages 1783-1793

  Singh, Sylvia S ^a   Kang, Peter M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anti apoptotic interventions; Apoptosis; Caspase inhibitors; Endogenous inhibitors; Heart failure

Indexed keywords

ALLOPURINOL; ALPHA TOCOPHEROL; APROTININ; ASCORBIC ACID; AURINTRICARBOXYLIC ACID; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BETA CAROTENE; CALPAIN; CARBOBENZOXYVALYLALANYLASPARTYLNMETHYL FLUOROMETHYLKETONE; CARVEDILOL; CASPASE INHIBITOR; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; ERYTHROPOIETIN; GRANULOCYTE COLONY STIMULATING FACTOR; INHIBITOR OF APOPTOSIS PROTEIN; INSULIN; METOPROLOL; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OXIPURINOL; PROBUCOL; QUINAPRIL; RAMIPRIL; SNJ 1945; SOMATOMEDIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; XANTHINE OXIDASE INHIBITOR;

APOPTOSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL DEATH; DOWN REGULATION; HEART FAILURE; HEART INFARCTION; HUMAN; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW;

APOPTOSIS; CARDIOVASCULAR AGENTS; GENE EXPRESSION REGULATION; HEART DISEASES; HUMANS;

EID: 79960329587     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161211796390994     Document Type: Review

References (154)

1. Garg S, Narula J, Chandrashekhar Y. Apoptosis and heart failure: clinical relevance and therapeutic target. J Mol Cell Cardiol 2005; 38: 73-79.
2. van Empel VP, Bertrand AT, Hofstra L, Crijns HJ, Doevendans PA, de Windt LJ. Myocyte apoptosis in heart failure. Cardiovasc Res 2005; 67: 21-29.
3. Ottaviani G, Lavezzi AM, Rossi L, Matturri L. Proliferating cell nuclear antigen (PCNA) and apoptosis in hyperacute and acute myocardial infarction. Eur J Histochem 1999; 43: 7-14.
4. Olivetti G, Quaini F, Sala R, et al. 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 1996; 28: 2005-2016.
5. Sabbah HN, Sharov VG. Apoptosis in heart failure. Prog Cardiovasc Dis 1998; 40: 549-562.
6. Kang PM, Haunstetter A, Aoki H, Usheva A, Izumo S. Morphological and molecular characterization of adult cardiomyocyte apoptosis during hypoxia and reoxygenation. Circ Res 2000; 87: 118-125.
7. Knaapen MW, Davies MJ, De Bie M, Haven AJ, Martinet W, Kockx MM. Apoptotic versus autophagic cell death in heart failure. Cardiovasc Res 2001; 51: 304-312.
8. Khoynezhad A, Jalali Z, Tortolani AJ. A synopsis of research in cardiac apoptosis and its application to congestive heart failure. Tex Heart Inst J 2007; 34: 352-359.
9. Abraham MC, Shaham S. Death without caspases, caspases without death. Trends Cell Biol 2004; 14: 184-193.
10. Haunstetter A, Izumo S. Apoptosis: basic mechanisms and implications for cardiovascular disease. Circ Res 1998; 82: 1111-1129.
11. Kang PM, Izumo S. Apoptosis and heart failure: A critical review of the literature. Circ Res 2000; 86: 1107-1113.
12. Kang PM, Izumo S. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med 2003; 9: 177-182.
13. Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005; 11: 725-730.
14. Slee EA, Harte MT, Kluck RM, et al. Ordering the cytochrome cinitiated caspase cascade: hierarchical activation of caspases-2, -3, - 6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999; 144: 281-292.
15. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
16. Chowdhury I, Tharakan B, Bhat GK. Caspases - an update. Comp Biochem Physiol B Biochem Mol Biol 2008; 151: 10-27.
17. Kim NH, Kang PM. Apoptosis in cardiovascular diseases: mechanism and clinical implications. Korean Circ J; 40: 299-305.
18. Brunet CL, Gunby RH, Benson RS, Hickman JA, Watson AJ, Brady G. Commitment to cell death measured by loss of clonogenicity is separable from the appearance of apoptotic markers. Cell Death Differ 1998; 5: 107-115.
19. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996; 86: 147-157.
20. Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATP dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91: 479-489.
21. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90: 405-413.
22. Chen G, Goeddel DV. TNF-R1 signaling: a beautiful pathway. Science 2002; 296: 1634-1635.
23. Engel D, Peshock R, Armstong RC, Sivasubramanian N, Mann DL. Cardiac myocyte apoptosis provokes adverse cardiac remodeling in transgenic mice with targeted TNF overexpression. Am J Physiol Heart Circ Physiol 2004; 287: 1303-1311.
24. Roncon-Albuquerque R, Jr., Vasconcelos M, Lourenco AP, et al. Acute changes of biventricular gene expression in volume and right ventricular pressure overload. Life Sci 2006; 78: 2633-2642.
25. Baumgarten G, Knuefermann P, Kalra D, et al. Load-dependent and -independent regulation of proinflammatory cytokine and cytokine receptor gene expression in the adult mammalian heart. Circulation 2002; 105: 2192-2197.
26. Meldrum DR, Cleveland JC, Jr., Cain BS, Meng X, Harken AH. Increased myocardial tumor necrosis factor-alpha in a crystalloidperfused model of cardiac ischemia-reperfusion injury. Ann Thorac Surg 1998; 65: 439-443.
27. Higuchi Y, McTiernan CF, Frye CB, McGowan BS, Chan TO, Feldman AM. Tumor necrosis factor receptors 1 and 2 differentially regulate survival, cardiac dysfunction, and remodeling in transgenic mice with tumor necrosis factor-alphainduced cardiomyopathy. Circulation 2004; 109: 1892-1897.
28. Hedayat M, Mahmoudi MJ, Rose NR, Rezaei N. Proinflammatory cytokines in heart failure: double-edged swords. Heart Fail Rev 2010; 15: 543-562.
29. Ishiyama S, Hiroe M, Nishikawa T, et al. The Fas/Fas ligand system is involved in the pathogenesis of autoimmune myocarditis in rats. J Immunol 1998; 161: 4695-4701.
30. Liao X, Wang X, Gu Y, Chen Q, Chen LY. Involvement of death receptor signaling in mechanical stretch-induced cardiomyocyte apoptosis. Life Sci 2005; 77: 160-174.
31. Twu C, Liu NQ, Popik W, et al. Cardiomyocytes undergo apoptosis in human immunodeficiency virus cardiomyopathy through mitochondrion- and death receptor-controlled pathways. Proc Natl Acad Sci USA 2002; 99: 14386-14391.
32. Yeh WC, Pompa JL, McCurrach ME, et al. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 1998; 279: 1954-1958.
33. Rychli K, Niessner A, Hohensinner PJ, et al. Prognostic value of pigment epithelium-derived factor in patients with advanced heart failure. Chest 2010; 138: 656-664.
34. Chen L, Zhang SS, Barnstable CJ, Tombran-Tink J. PEDF induces apoptosis in human endothelial cells by activating p38 MAP kinase dependent cleavage of multiple caspases. Biochem Biophys Res Commun 2006; 348: 1288-1295.
35. Volpert OV, Zaichuk T, Zhou W, et al. Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat Med 2002; 8: 349-357.
36. Abbate A, Biondi-Zoccai GG, Bussani R, et al. Increased myocardial apoptosis in patients with unfavorable left ventricular remodeling and early symptomatic post-infarction heart failure. J Am Coll Cardiol 2003; 41: 753-760.
37. Rossig L, Fichtlscherer S, Heeschen C, Berger J, Dimmeler S, Zeiher AM. The pro-apoptotic serum activity is an independent mortality predictor of patients with heart failure. Eur Heart J 2004; 25: 1620-1625.
38. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 2004; 95: 957-970.
39. Chen Z, Chua CC, Ho YS, Hamdy RC, Chua BH. Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice. Am J Physiol Heart Circ Physiol 2001; 280: H2313-H2320.
40. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94: 491-501.
41. Bartling B, Milting H, Schumann H, et al. Myocardial gene expression of regulators of myocyte apoptosis and myocyte calcium homeostasis during hemodynamic unloading by ventricular assist devices in patients with end-stage heart failure. Circulation 1999; 100: II216-II223.
42. Hochhauser E, Cheporko Y, Yasovich N, et al. Bax deficiency reduces infarct size and improves long-term function after myocardial infarction. Cell Biochem Biophys 2007; 47: 11-20.
43. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Attenuation of ischemia/reperfusion injury in rats by a caspase inhibitor. Circulation 1998; 97: 276-281.
44. Doi R, Masuyama T, Yamamoto K, et al. Development of different phenotypes of hypertensive heart failure: systolic versus diastolic failure in Dahl salt-sensitive rats. J Hypertens 2000; 18: 111-120.
45. Laugwitz KL, Moretti A, Weig HJ, et al. Blocking caspaseactivated apoptosis improves contractility in failing myocardium. Hum Gene Ther 2001; 12: 2051-2063.
46. Lorenzo HK, Susin SA, Penninger J, Kroemer G. Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death Differ 1999; 6: 516-524.
47. Bae S, Siu PM, Choudhury S, et al. Delayed activation of caspaseindependent apoptosis during heart failure in transgenic mice overexpressing caspase inhibitor CrmA. Am J Physiol Heart Circ Physiol 2010; 299: H1374-H1381.
48. Cande C, Cecconi F, Dessen P, Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 2002; 115: 4727-4734.
49. Choudhury S, Bae S, Kumar SR, et al. Role of AIF in cardiac apoptosis in hypertrophic cardiomyocytes from Dahl salt-sensitive rats. Cardiovasc Res 2010; 85: 28-37.
50. Cregan SP, Dawson VL, Slack RS. Role of AIF in caspasedependent and caspase-independent cell death. Oncogene 2004; 23: 2785-2796.
51. Joseph B, Marchetti P, Formstecher P, Kroemer G, Lewensohn R, Zhivotovsky B. Mitochondrial dysfunction is an essential step for killing of non-small cell lung carcinomas resistant to conventional treatment. Oncogene 2002; 21: 65-77.
52. Penninger JM, Kroemer G. Mitochondria, AIF and caspases--rivaling for cell death execution. Nat Cell Biol 2003; 5: 97-99.
53. Modjtahedi N, Giordanetto F, Madeo F, Kroemer G. Apoptosisinducing factor: vital and lethal. Trends Cell Biol 2006; 16: 264-272.
54. Porter AG, Urbano AG. Does apoptosis-inducing factor (AIF) have both life and death functions in cells? Bioessays 2006; 28: 834-843.
55. Joza N, Susin SA, Daugas E, et al. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 2001; 410: 549-554.
56. Klein JA, Longo-Guess CM, Rossmann MP, et al. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002; 419: 367-374.
57. van Empel VP, Bertrand AT, van der Nagel R, et al. 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 2005; 96: e92-e101.
58. Joza N, Oudit GY, Brown D, et al. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol Cell Biol 2005; 25: 10261-10272.
59. Cheung EC, Joza N, Steenaart NA, et al. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. EMBO J 2006; 25: 4061-4073.
60. Bae S, Yalamarti B, Kang PM. Role of caspase-independent apoptosis in cardiovascular diseases. Front Biosci 2008; 13: 2495-2503.
61. Siu PM, Bae S, Bodyak N, Rigor DL, Kang PM. Response of caspase-independent apoptotic factors to high salt diet-induced heart failure. J Mol Cell Cardiol 2007; 42: 678-686.
62. Chen M, Zsengeller Z, Xiao CY, Szabo C. Mitochondrial-tonuclear translocation of apoptosis-inducing factor in cardiac myocytes during oxidant stress: potential role of poly(ADP-ribose) polymerase-1. Cardiovasc Res 2004; 63: 682-688.
63. Yu SW, Wang H, Poitras MF, et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002; 297: 259-263.
64. Virag L, Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 2002; 54: 375-429.
65. Sharp TV, Wang HW, Koumi A, et al. K15 protein of Kaposi's sarcoma-associated herpesvirus is latently expressed and binds to HAX-1, a protein with antiapoptotic function. J Virol 2002; 76: 802-816.
66. Alonso M, Tamasdan C, Miller DC, Newcomb EW. Flavopiridol induces apoptosis in glioma cell lines independent of retinoblastoma and p53 tumor suppressor pathway alterations by a caspase-independent pathway. Mol Cancer Ther 2003; 2: 139-150.
67. Pieper AA, Brat DJ, Krug DK, et al. Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocininduced diabetes. Proc Natl Acad Sci USA 1999; 96: 3059-3064.
68. Xiao CY, Chen M, Zsengeller Z, et al. Poly(ADP-Ribose) polymerase promotes cardiac remodeling, contractile failure, and translocation of apoptosis-inducing factor in a murine experimental model of aortic banding and heart failure. J Pharmacol Exp Ther 2005; 312: 891-898.
69. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001; 412: 95-99.
70. Varecha M, Zimmermann M, Amrichova J, Ulman V, Matula P, Kozubek M. Prediction of localization and interactions of apoptotic proteins. J Biomed Sci 2009; 16: 59.
71. Ishihara Y, Shimamoto N. Involvement of endonuclease G in nucleosomal DNA fragmentation under sustained endogenous oxidative stress. J Biol Chem 2006; 281: 6726-6733.
72. van Loo G, Schotte P, van Gurp M, et al. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ 2001; 8: 1136-1142.
73. Bahi N, Zhang J, Llovera M, Ballester M, Comella JX, Sanchis D. 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 2006; 281: 22943-22952.
74. David KK, Sasaki M, Yu SW, Dawson TM, Dawson VL. EndoG is dispensable in embryogenesis and apoptosis. Cell Death Differ 2006; 13: 1147-1155.
75. Irvine RA, Adachi N, Shibata DK, et al. Generation and characterization of endonuclease G null mice. Mol Cell Biol 2005; 25: 294-302.
76. Balakrishnan MP, Cilenti L, Mashak Z, Popat P, Alnemri ES, Zervos AS. THAP5 is a human cardiac-specific inhibitor of cell cycle that is cleaved by the proapoptotic Omi/HtrA2 protease during cell death. Am J Physiol Heart Circ Physiol 2009; 297: H643-H653.
77. Vande Walle L, Lamkanfi M, Vandenabeele P. The mitochondrial serine protease HtrA2/Omi: an overview. Cell Death Differ 2008; 15: 453-460.
78. Cilenti L, Lee Y, Hess S, et al. Characterization of a novel and specific inhibitor for the pro-apoptotic protease Omi/HtrA2. J Biol Chem 2003; 278: 11489-11494.
79. Liu HR, Gao E, Hu A, et al. Role of Omi/HtrA2 in apoptotic cell death after myocardial ischemia and reperfusion. Circulation 2005; 111: 90-96.
80. Bhuiyan MS, Fukunaga K. Inhibition of HtrA2/Omi ameliorates heart dysfunction following ischemia/reperfusion injury in rat heart in vivo. Eur J Pharmacol 2007; 557: 168-177.
81. Regula KM, Ens K, Kirshenbaum LA. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 2002; 91: 226-231.
82. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 2002; 99: 12825-12830.
83. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997; 388: 190-195.
84. Rasper DM, Vaillancourt JP, Hadano S, et al. Cell death attenuation by 'Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ 1998; 5: 271-288.
85. Salvesen GS, Dixit VM. Caspase activation: the induced-proximity model. Proc Natl Acad Sci USA 1999; 96: 10964-10967.
86. Deveraux QL, Roy N, Stennicke HR, et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 1998; 17: 2215-2223.
87. Holly TA, Drincic A, Byun Y, et al. Caspase inhibition reduces myocyte cell death induced by myocardial ischemia and reperfusion in vivo. J Mol Cell Cardiol 1999; 31: 1709-1715.
88. Huang JQ, Radinovic S, Rezaiefar P, Black SC. In vivo myocardial infarct size reduction by a caspase inhibitor administered after the onset of ischemia. Eur J Pharmacol 2000; 402: 139-142.
89. Sun CK, Chang LT, Sheu JJ, et al. Losartan preserves integrity of cardiac gap junctions and PGC-1 alpha gene expression and prevents cellular apoptosis in remote area of left ventricular myocardium following acute myocardial infarction. Int Heart J 2007; 48: 533-546.
90. Chua CC, Gao J, Ho YS, et al. Overexpression of IAP-2 attenuates apoptosis and protects against myocardial ischemia/reperfusion injury in transgenic mice. Biochim Biophys Acta 2007; 1773: 577-583.
91. Han Y, Chen YS, Liu Z, et al. Overexpression of HAX-1 protects cardiac myocytes from apoptosis through caspase-9 inhibition. Circ Res 2006; 99: 415-423.
92. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
93. Verhagen AM, Ekert PG, Pakusch M, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000; 102: 43-53.
94. Ludwig-Galezowska AH, Flanagan L, Rehm M. Apoptosis repressor with caspase recruitment domain, a multifunctional modulator of cell death. J Cell Mol Med 2010.
95. Donath S, Li P, Willenbockel C, et al. Apoptosis repressor with caspase recruitment domain is required for cardio protection in response to biomechanical and ischemic stress. Circulation 2006; 113: 1203-1212.
96. Ekhterae D, Lin Z, Lundberg MS, Crow MT, Brosius FC, 3rd, Nunez G. ARC inhibits cytochrome c release from mitochondria and protects against hypoxia-induced apoptosis in heart-derived H9c2 cells. Circ Res 1999; 85: e70-e77.
97. Chatterjee S, Bish LT, Jayasankar V, et al. Blocking the development of postischemic cardiomyopathy with viral gene transfer of the apoptosis repressor with caspase recruitment domain. J Thorac Cardiovasc Surg 2003; 125: 1461-1469.
98. Gustafsson AB, Sayen MR, Williams SD, Crow MT, Gottlieb RA. TAT protein transduction into isolated perfused hearts: TATapoptosis repressor with caspase recruitment domain is cardioprotective. Circulation 2002; 106: 735-739.
99. Cancel LM, Tarbell JM. The role of apoptosis in LDL transport through cultured endothelial cell monolayers. Atherosclerosis 2010; 208: 335-341.
100. Uetani T, Nakayama H, Okayama H, et al. Insufficiency of proheparin-binding epidermal growth factor-like growth factor shedding enhances hypoxic cell death in H9c2 cardiomyoblasts via the activation of caspase-3 and c-Jun N-terminal kinase. J Biol Chem 2009; 284: 12399-12409.
101. Chandrashekhar Y, Sen S, Anway R, Shuros A, Anand I. Longterm caspase inhibition ameliorates apoptosis, reduces myocardial troponin-I cleavage, protects left ventricular function, and attenuates remodeling in rats with myocardial infarction. J Am Coll Cardiol 2004; 43: 295-301.
102. Hayakawa Y, Chandra M, Miao W, et al. Inhibition of cardiac myocyte apoptosis improves cardiac function and abolishes mortality in the peripartum cardiomyopathy of Galpha(q) transgenic mice. Circulation 2003; 108: 3036-3041.
103. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Apoptosis in relevant clinical situations: contribution of apoptosis in myocardial infarction. Cardiovasc Res 2000; 45: 630-641.
104. Jagtap P, Soriano FG, Virag L, et al. Novel phenanthridinone inhibitors of poly (adenosine 5'-diphosphate-ribose) synthetase: potent cytoprotective and antishock agents. Crit Care Med 2002; 30: 1071-1082.
105. Fiorillo C, Ponziani V, Giannini L, et al. Protective effects of the PARP-1 inhibitor PJ34 in hypoxic-reoxygenated cardiomyoblasts. Cell Mol Life Sci 2006; 63: 3061-3071.
106. Faro R, Toyoda Y, McCully JD, et al. Myocardial protection by PJ34, a novel potent poly (ADP-ribose) synthetase inhibitor. Ann Thorac Surg 2002; 73: 575-581.
107. Szenczi O, Kemecsei P, Holthuijsen MF, et al. Poly(ADP-ribose) polymerase regulates myocardial calcium handling in doxorubicininduced heart failure. Biochem Pharmacol 2005; 69: 725-732.
108. Szabo G, Bahrle S, Stumpf N, et al. Poly(ADP-Ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ Res 2002; 90: 100-106.
109. Szabo G, Buhmann V, Andrasi T, et al. Poly-ADP-ribose polymerase inhibition protects against myocardial and endothelial reperfusion injury after hypothermic cardiac arrest. J Thorac Cardiovasc Surg 2003; 126: 651-658.
110. Andrasi TB, Blazovics A, Szabo G, Vahl CF, Hagl S. Poly(ADPribose) polymerase inhibitor PJ-34 reduces mesenteric vascular injury induced by experimental cardiopulmonary bypass with cardiac arrest. Am J Physiol Heart Circ Physiol 2005; 288: H2972-H2978.
111. Pacher P, Liaudet L, Mabley J, Komjati K, Szabo C. Pharmacologic inhibition of poly(adenosine diphosphate-ribose) polymerase may represent a novel therapeutic approach in chronic heart failure. J Am Coll Cardiol 2002; 40: 1006-1016.
112. Andrew DJ, Hay AW, Evans SW. Aurintricarboxylic acid inhibits apoptosis and supports proliferation in a haemopoietic growthfactor dependent myeloid cell line. Immunopharmacology 1999; 41: 1-10.
113. Heiduschka P, Thanos S. Aurintricarboxylic acid promotes survival and regeneration of axotomised retinal ganglion cells in vivo. Neuropharmacology 2000; 39: 889-902.
114. Beery R, Haimsohn M, Wertheim N, et al. Activation of the insulin-like growth factor 1 signaling pathway by the antiapoptotic agents aurintricarboxylic acid and evans blue. Endocrinology 2001; 142: 3098-3107.
115. Lam TT, Fu J, Hrynewycz M, Tso MO. The effect of aurintricarboxylic acid, an endonuclease inhibitor, on ischemia/reperfusion damage in rat retina. J Ocul Pharmacol Ther 1995; 11: 253-259.
116. Mesner PW, Jr., Bible KC, Martins LM, et al. Characterization of caspase processing and activation in HL-60 cell cytosol under cellfree conditions. Nucleotide requirement and inhibitor profile. J Biol Chem 1999; 274: 22635-22645.
117. Zhao ZQ, Morris CD, Budde JM, et al. Inhibition of myocardial apoptosis reduces infarct size and improves regional contractile dysfunction during reperfusion. Cardiovasc Res 2003; 59: 132-142.
118. Pruefer D, Buerke U, Khalil M, et al. Cardioprotective effects of the serine protease inhibitor aprotinin after regional ischemia and reperfusion on the beating heart. J Thorac Cardiovasc Surg 2002; 124: 942-949.
119. Iwamoto H, Miura T, Okamura T, et al. Calpain inhibitor-1 reduces infarct size and DNA fragmentation of myocardium in ischemic/reperfused rat heart. J Cardiovasc Pharmacol 1999; 33: 580-586.
120. Yaoita H, Maruyama Y. Intervention for apoptosis in cardiomyopathy. Heart Fail Rev 2008; 13: 181-191.
121. Keith M, Geranmayegan A, Sole MJ, et al. Increased oxidative stress in patients with congestive heart failure. J Am Coll Cardiol 1998; 31: 1352-1356.
122. Dhalla NS, Elmoselhi AB, Hata T, Makino N. Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res 2000; 47: 446-456.
123. Zhao ZQ, Nakamura M, Wang NP, et al. Reperfusion induces myocardial apoptotic cell death. Cardiovasc Res 2000; 45: 651-660.
124. Oskarsson HJ, Coppey L, Weiss RM, Li WG. Antioxidants attenuate myocyte apoptosis in the remote non-infarcted myocardium following large myocardial infarction. Cardiovasc Res 2000; 45: 679-687.
125. Qin F, Shite J, Liang CS. Antioxidants attenuate myocyte apoptosis and improve cardiac function in CHF: association with changes in MAPK pathways. Am J Physiol Heart Circ Physiol 2003; 285: H822-H832.
126. Gavin AD, Struthers AD. Allopurinol reduces B-type natriuretic peptide concentrations and haemoglobin but does not alter exercise capacity in chronic heart failure. Heart 2005; 91: 749-753.
127. Reyes AJ, Leary WP. Allopurinol or oxypurinol in heart failure therapy - a promising new development or end of story? Cardiovasc Drugs Ther 2005; 19: 311-313.
128. Jialal I, Devaraj S. Scientific evidence to support a vitamin E and heart disease health claim: research needs. J Nutr 2005; 135: 348-353.
129. Wu BJ, Di Girolamo N, Beck K, et al. Probucol [4,4'-[(1- methylethylidene)bis(thio)]bis-[2,6-bis(1,1-dimethylethyl)phenol ]] inhibits compensatory remodeling and promotes lumen loss associated with atherosclerosis in apolipoprotein E-deficient mice. J Pharmacol Exp Ther 2007; 321: 477-484.
130. Sam F, Kerstetter DL, Pimental DR, et al. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J Card Fail 2005; 11: 473-480.
131. Humphreys RA, Haist JV, Chakrabarti S, Feng Q, Arnold JM, Karmazyn M. Orally administered NHE1 inhibitor cariporide reduces acute responses to coronary occlusion and reperfusion. Am J Physiol 1999; 276: H749-H757.
132. Massoudy P, Zahler S, Kupatt C, Reder E, Becker BF, Gerlach E. Cardioprotection by cyclosporine A in experimental ischemia and reperfusion--evidence for a nitric oxide-dependent mechanism mediated by endothelin. J Mol Cell Cardiol 1997; 29: 535-544.
133. Maulik N, Engelman RM, Rousou JA, Flack JE, 3rd, Deaton D, Das DK. Ischemic preconditioning reduces apoptosis by upregulating anti-death gene Bcl-2. Circulation 1999; 100: II369-II375.
134. Baines CP, Molkentin JD. STRESS signaling pathways that modulate cardiac myocyte apoptosis. J Mol Cell Cardiol 2005; 38: 47-62.
135. Li Q, Li B, Wang X, et al. Over expression of insulin-like growth factor-1 in mice protects from myocyte death after infarction, attenuating ventricular dilation, wall stress, and cardiac hypertrophy. J Clin Invest 1997; 100: 1991-1999.
136. Lee WL, Chen JW, Ting CT, et al. Insulin-like growth factor I improves cardiovascular function and suppresses apoptosis of cardiomyocytes in dilated cardiomyopathy. Endocrinology 1999; 140: 4831-4840.
137. Abbate A, Biondi-Zoccai GG, Baldi A. Pathophysiologic role of myocardial apoptosis in post-infarction left ventricular remodeling. J Cell Physiol 2002; 193: 145-153.
138. Smith CG, Vane JR. The discovery of captopril. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 2003; 17: 788-789.
139. Yusuf S, Sleight P, Pogue J, Bosch J, Davies R, Dagenais G. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. The New England journal of medicine 2000; 342: 145-153.
140. Kobara M, Tatsumi T, Kambayashi D, et al. Effects of ACE inhibition on myocardial apoptosis in an ischemia-reperfusion rat heart model. Journal of cardiovascular pharmacology 2003; 41: 880-889.
141. Kajstura J, Cigola E, Malhotra A, et al. Angiotensin II induces apoptosis of adult ventricular myocytes in vitro. J Mol Cell Cardiol 1997; 29: 859-870.
142. Pitt B, Gheorghiade M, Zannad F, et al. Evaluation of eplerenone in the subgroup of EPHESUS patients with baseline left ventricular ejection fraction
143. Veliotes DG, Norton GR, Correia RJ, et al. Impact of aldosterone receptor blockade on the deleterious cardiac effects of adrenergic activation in hypertensive rats. Journal of cardiovascular pharmacology 2010; 56: 203-211.
144. Sabbah HN, Sharov VG, Gupta RC, Todor A, Singh V, Goldstein S. Chronic therapy with metoprolol attenuates cardiomyocyte apoptosis in dogs with heart failure. J Am Coll Cardiol 2000; 36: 1698-705.
145. Communal C, Singh K, Pimentel DR, Colucci WS. Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the beta-adrenergic pathway. Circulation 1998; 98: 1329-1334.
146. Kawai K, Qin F, Shite J, Mao W, Fukuoka S, Liang CS. Importance of antioxidant and antiapoptotic effects of beta-receptor blockers in heart failure therapy. Am J Physiol Heart Circ Physiol 2004; 287: H1003-H1012.
147. Balsam LB, Kofidis T, Robbins RC. Caspase-3 inhibition preserves myocardial geometry and long-term function after infarction. The Journal of surgical research 2005; 124: 194-200.
148. Yoshikawa Y, Hagihara H, Ohga Y, et al. Calpain inhibitor-1 protects the rat heart from ischemia-reperfusion injury: analysis by mechanical work and energetics. American journal of physiology Heart and circulatory physiology 2005; 288: H1690-H1698.
149. Wang L, Ma W, Markovich R, Chen JW, Wang PH. Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I. Circ Res 1998; 83: 516-522.
150. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nature medicine 2001; 7: 430-436.
151. Jayasankar V, Woo YJ, Pirolli TJ, et al. Induction of angiogenesis and inhibition of apoptosis by hepatocyte growth factor effectively treats postischemic heart failure. Journal of cardiac surgery 2005; 20: 93-101.
152. Moon C, Krawczyk M, Ahn D, et al. Erythropoietin reduces myocardial infarction and left ventricular functional decline after coronary artery ligation in rats. Proceedings of the National Academy of Sciences of the United States of America 2003; 100: 11612-11617.
153. Moon C, Krawczyk M, Paik D, et al. Erythropoietin, modified to not stimulate red blood cell production, retains its cardioprotective properties. The Journal of pharmacology and experimental therapeutics 2006; 316: 999-1005.
154. Gao F, Tao L, Yan W, et al. Early anti-apoptosis treatment reduces myocardial infarct size after a prolonged reperfusion. Apoptosis: an international journal on programmed cell death 2004; 9: 553-559.