Programmed necrosis, not apoptosis, in the heart

Circulation Research

Volumn 108, Issue 8, 2011, Pages 1017-1036

  Kung, Gloria ^a   Konstantinidis, Klitos ^a   Kitsis, Richard N ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

apoptosis; cell death; heart failure; myocardial infarction; necrosis

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE; CYCLOPHILIN D; DEATH RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; LIPOXYGENASE; NECROSTATIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATE TRANSPORTER; PHOSPHOLIPASE; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTEIN KINASE PIM 1; PROTEINASE; REACTIVE OXYGEN METABOLITE; RECEPTOR INTERACTING PROTEIN 1; RECEPTOR INTERACTING PROTEIN 140; RECEPTOR INTERACTING PROTEIN 3; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

APOPTOSIS; CAENORHABDITIS ELEGANS; CELL DEATH; CELL MEMBRANE; CELL PERMEABILIZATION; CELL STRUCTURE; ENDOPLASMIC RETICULUM; HEART DISEASE; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; INFLAMMATION; LYSOSOME; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NECROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; APOPTOSIS; CELL DEATH; HEART; HUMANS; MYOCYTES, CARDIAC; NECROSIS;

EID: 79954606808     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.225730     Document Type: Review

References (179)

1. Ellis RE, Yuan JY, Horvitz HR. Mechanisms and functions of cell death. Annu Rev Cell Biol. 1991;7:663-698.
2. Shaham S, Horvitz HR. Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev. 1996;10:578-591. (Pubitemid 26091769)
3. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116:205-219. (Pubitemid 38167313)
4. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 2007;14:1237-1243. (Pubitemid 46969863)
5. Xu K, Tavernarakis N, Driscoll M. Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca(2) release from the endoplasmic reticulum. Neuron. 2001;31:957-971. (Pubitemid 32925282)
6. Syntichaki P, Xu K, Driscoll M, Tavernarakis N. Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature. 2002;419:939-944. (Pubitemid 35339629)
7. Bianchi L, Gerstbrein B, Frokjaer-Jensen C, Royal DC, Mukherjee G, Royal MA, Xue J, Schafer WR, Driscoll M. The neurotoxic MEC-4(d) DEG/ENac sodium channel conducts calcium: implications for necrosis initiation. Nat Neurosci. 2004;7:1337-1344. (Pubitemid 41057756)
8. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell. 2003;114:181-190. (Pubitemid 36936912)
9. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434: 658-662. (Pubitemid 40488559)
10. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005;434:652-658. (Pubitemid 40488558)
11. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA. 2005;102:12005-12010. (Pubitemid 41291119)
12. Kitsis RN, Molkentin JD. Apoptotic cell death "Nixed" by an ER-mitochondrial necrotic pathway. Proc Natl Acad Sci USA. 2010; 107:9031-9032.
13. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, Jaleel N, Chua BH, Hewett TE, Robbins J, Houser SR, Molkentin JD. Ca2- and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J Clin Invest. 2007;117:2431-2444. (Pubitemid 47494345)
14. Du H, Guo L, Fang F, Chen D, Sosunov AA, McKhann GM, Yan Y, Wang C, Zhang H, Molkentin JD, Gunn-Moore FJ, Vonsattel JP, Arancio O, Chen JX, Yan SD. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med. 2008;14:1097-1105.
15. Esposito E, Cuzzocrea S. New therapeutic strategy for Parkinson's and Alzheimer's disease. Curr Med Chem. 2010;17:2764-2774.
16. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137:1112-1123.
17. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med. 2008;14:442-447. (Pubitemid 351499389)
18. Fujimoto K, Chen Y, Polonsky KS, Dorn GW II. Targeting cyclophilin D and the mitochondrial permeability transition enhances beta-cell survival and prevents diabetes in Pdx1 deficiency. Proc Natl Acad Sci USA. 2010;107:10214-10219.
19. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 2009;137:1100-1111.
20. Whelan RS, Kaplinskiy V, Kitsis RN. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol. 2010; 72:19-44.
21. Balkwill F. Tumour necrosis factor and cancer. Nat Rev Cancer. 2009; 9:361-371.
22. Fiers W, Beyaert R, Boone E, Cornelis S, Declercq W, Decoster E, Denecker G, Depuydt B, De Valck D, De Wilde G, Goossens V, Grooten J, Haegeman G, Heyninck K, Penning L, Plaisance S, Vancompernolle K, Van Criekinge W, Vandenabeele P, Vanden Berghe W, Van de Craen M, Vandevoorde V, Vercammen D. TNF-induced intracellular signaling leading to gene induction or to cytotoxicity by necrosis or by apoptosis. J Inflamm. 1995;47:67-75.
23. Meylan E, Tschopp J. The RIP kinases: crucial integrators of cellular stress. Trends Biochem Sci. 2005;30:151-159. (Pubitemid 40332531)
24. Stanger BZ, Leder P, Lee TH, Kim E, Seed B. RIP: a novel protein containing a death domain that interacts with Fas/Apo-1 (CD95) in yeast and causes cell death. Cell. 1995;81:513-523.
25. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ. 2007;14:400-410.
26. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1:489-495.
27. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, Hedrick SM, Gerber SA, Lugovskoy A, Yuan J. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol. 2008;4:313-321. (Pubitemid 351550892)
28. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005;1:112-119.
29. Smith CC, Davidson SM, Lim SY, Simpkin JC, Hothersall JS, Yellon DM. Necrostatin: a potentially novel cardioprotective agent? Cardiovasc Drugs Ther. 2007;21:227-233. (Pubitemid 47387468)
30. Sun X, Yin J, Starovasnik MA, Fairbrother WJ, Dixit VM. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J Biol Chem. 2002;277: 9505-9511. (Pubitemid 34953039)
31. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 1998;17:2215-2223. (Pubitemid 28171907)
32. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell. 2008;30:689-700. (Pubitemid 351818251)
33. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell. 2006;22:245-257.
34. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C, Enwere E, Arora V, Mak TW, Lacasse EC, Waring J, Korneluk RG. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc Natl Acad Sci USA. 2008;105:11778-11783.
35. Wong WW, Gentle IE, Nachbur U, Anderton H, Vaux DL, Silke J. RIPK1 is not essential for TNFR1-induced activation of NF-kappaB. Cell Death Differ. 2010;17:482-487.
36. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature. 2004;430:694-699. (Pubitemid 39061687)
37. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell. 2008;135:1311-1323.
38. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell. 2008;133:693-703. (Pubitemid 351636305)
39. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM, Ricci JE, Edris WA, Sutherlin DP, Green DR, Salvesen GS. A unified model for apical caspase activation. Mol Cell. 2003;11:529-541. (Pubitemid 36293843)
40. Lin Y, Devin A, Rodriguez Y, Liu ZG. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 1999;13:2514-2526. (Pubitemid 29489643)
41. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med. 1998;187:1477-1485. (Pubitemid 28215406)
42. Ermolaeva MA, Michallet MC, Papadopoulou N, Utermohlen O, Kranidioti K, Kollias G, Tschopp J, Pasparakis M. Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat Immunol. 2008;9:1037-1046.
43. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science. 2009;325:332-336.
44. Goossens V, De Vos K, Vercammen D, Steemans M, Vancompernolle K, Fiers W, Vandenabeele P, Grooten J. Redox regulation of TNF signaling. Biofactors. 1999;10:145-156. (Pubitemid 29533823)
45. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, Tran JH, Nedospasov SA, Liu ZG. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem. 2004;279: 10822-10828. (Pubitemid 38372695)
46. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem. 1992;267:5317-5323.
47. Kim YS, Morgan MJ, Choksi S, Liu ZG. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol Cell. 2007;26:675-687. (Pubitemid 46856240)
48. Saelens X, Festjens N, Parthoens E, Vanoverberghe I, Kalai M, Van Kuppeveld F, Vandenabeele P. Protein synthesis persists during necrotic cell death. J Cell Biol. 2005;168:545-551. (Pubitemid 40271019)
49. Sun XM, Butterworth M, MacFarlane M, Dubiel W, Ciechanover A, Cohen GM. Caspase activation inhibits proteasome function during apoptosis. Mol Cell. 2004;14:81-93. (Pubitemid 38469911)
50. Soldani C, Scovassi AI. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis. 2002;7:321-328. (Pubitemid 34832256)
51. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997;185:1481-1486. (Pubitemid 27187604)
52. Kraus WL. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol. 2008;20:294-302.
53. Bogan KL, Brenner C. Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD- precursor vitamins in human nutrition. Annu Rev Nutr. 2008;28:115-130.
54. Los M, Mozoluk M, Ferrari D, Stepczynska A, Stroh C, Renz A, Herceg Z, Wang ZQ, Schulze-Osthoff K. Activation and caspase-mediated inhibition of PARP: a molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell. 2002;13:978-988. (Pubitemid 34250359)
55. Eliasson MJ, Sampei K, Mandir AS, Hurn PD, Traystman RJ, Bao J, Pieper A, Wang ZQ, Dawson TM, Snyder SH, Dawson VL. Poly(ADPribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med. 1997;3:1089-1095. (Pubitemid 27444449)
56. Zingarelli B, Hake PW, O'Connor M, Denenberg A, Kong S, Aronow BJ. Absence of poly(ADP-ribose)polymerase-1 alters nuclear factor-kappa B activation and gene expression of apoptosis regulators after reperfusion injury. Mol Med. 2003;9:143-153. (Pubitemid 37310951)
57. Zhou HZ, Swanson RA, Simonis U, Ma X, Cecchini G, Gray MO. Poly(ADP-ribose) polymerase-1 hyperactivation and impairment of mitochondrial respiratory chain complex I function in reperfused mouse hearts. Am J Physiol Heart Circ Physiol. 2006;291:H714-H723. (Pubitemid 44175077)
58. Lai Y, Chen Y, Watkins SC, Nathaniel PD, Guo F, Kochanek PM, Jenkins LW, Szabo C, Clark RS. Identification of poly-ADP-ribosylated mitochondrial proteins after traumatic brain injury. J Neurochem. 2008; 104:1700-1711. (Pubitemid 351316774)
59. Pankotai E, Lacza Z, Muranyi M, Szabo C. Intra-mitochondrial poly- (ADP-ribosyl)ation: potential role for alpha-ketoglutarate dehydrogenase. Mitochondrion. 2009;9:159-164.
60. Xu Y, Huang S, Liu ZG, Han J. Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/Traf2- mediated Jnk1 activation. J Biol Chem. 2006;281:8788-8795. (Pubitemid 43847985)
61. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 2002;297:259-263. (Pubitemid 34761289)
62. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA. 2006; 103:18314-18319. (Pubitemid 44871655)
63. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, Menissier-de Murcia J, Susin SA. Sequential activation of poly(ADPribose) polymerase 1, calpains, and Bax is essential in apoptosisinducing factor-mediated programmed necrosis. Mol Cell Biol. 2007;27: 4844-4862. (Pubitemid 47016136)
64. Artus C, Boujrad H, Bouharrour A, Brunelle MN, Hoos S, Yuste VJ, Lenormand P, Rousselle JC, Namane A, England P, Lorenzo HK, Susin SA. AIF promotes chromatinolysis and caspase-independent pro- grammed necrosis by interacting with histone H2AX. EMBO J. 2010; 29:1585-1599.
65. Temkin V, Huang Q, Liu H, Osada H, Pope RM. Inhibition of ADP/ATP exchange in receptor-interacting protein-mediated necrosis. Mol Cell Biol. 2006;26:2215-2225. (Pubitemid 43346922)
66. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007;87:99-163. (Pubitemid 46209992)
67. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11:700-714.
68. Berghe TV, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, Guerin CJ, Brunk UT, Declercq W, Vandenabeele P. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 2010;17:922-930.
69. Goossens V, Stange G, Moens K, Pipeleers D, Grooten J. Regulation of tumor necrosis factor-induced, mitochondria- and reactive oxygen species-dependent cell death by the electron flux through the electron transport chain complex I. Antioxid Redox Signal. 1999;1:285-295. (Pubitemid 129622799)
70. Wang KK. Calpain and caspase: can you tell the difference? Trends Neurosci. 2000;23:20-26. (Pubitemid 30100309)
71. Bano D, Young KW, Guerin CJ, Lefeuvre R, Rothwell NJ, Naldini L, Rizzuto R, Carafoli E, Nicotera P. Cleavage of the plasma membrane Na/Ca2 exchanger in excitotoxicity. Cell. 2005;120:275-285. (Pubitemid 40174769)
72. Kar P, Chakraborti T, Samanta K, Chakraborti S. Mu-calpain mediated cleavage of the Na/Ca2 exchanger in isolated mitochondria under A23187 induced Ca2 stimulation. Arch Biochem Biophys. 2009;482: 66-76.
73. Spencer MJ, Croall DE, Tidball JG. Calpains are activated in necrotic fibers from Mdx dystrophic mice. J Biol Chem. 1995;270:10909-10914.
74. Harwood SM, Allen DA, Raftery MJ, Yaqoob MM. High glucose initiates calpain-induced necrosis before apoptosis in LLC-PK1 cells. Kidney Int. 2007;71:655-663. (Pubitemid 46494560)
75. Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, Kominami E. Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus. 2003;13:791-800. (Pubitemid 37407965)
76. Oikawa S, Yamada T, Minohata T, Kobayashi H, Furukawa A, Tada- Oikawa S, Hiraku Y, Murata M, Kikuchi M, Yamashima T. Proteomic identification of carbonylated proteins in the monkey hippocampus after ischemia-reperfusion. Free Radic Biol Med. 2009;46:1472-1477.
77. Doulias PT, Kotoglou P, Tenopoulou M, Keramisanou D, Tzavaras T, Brunk U, Galaris D, Angelidis C. Involvement of heat shock protein-70 in the mechanism of hydrogen peroxide-induced DNA damage: the role of lysosomes and iron. Free Radic Biol Med. 2007;42:567-577. (Pubitemid 46162124)
78. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Hoyer-Hansen M, Weber E, Multhoff G, Rohde M, Jaattela M. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med. 2004;200:425-435. (Pubitemid 39121900)
79. Van Herreweghe F, Festjens N, Declercq W, Vandenabeele P. Tumor necrosis factor-mediated cell death: to break or to burst, that's the question. Cell Mol Life Sci. 2010;67:1567-1579.
80. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene. 2008;27:6434-6451.
81. Syntichaki P, Samara C, Tavernarakis N. The vacuolar H-ATPase mediates intracellular acidification required for neurodegeneration in C. elegans. Curr Biol. 2005;15:1249-1254. (Pubitemid 40950525)
82. Zhao M, Antunes F, Eaton JW, Brunk UT. Lysosomal enzymes promote mitochondrial oxidant production, cytochrome c release and apoptosis. Eur J Biochem. 2003;270:3778-3786. (Pubitemid 37123249)
83. Kurz T, Terman A, Gustafsson B, Brunk UT. Lysosomes in iron metabolism, ageing and apoptosis. Histochem Cell Biol. 2008;129: 389-406.
84. Xie C, Zhang N, Zhou H, Li J, Li Q, Zarubin T, Lin SC, Han J. Distinct roles of basal steady-state and induced H-ferritin in tumor necrosis factor-induced death in L929 cells. Mol Cell Biol. 2005;25:6673-6681. (Pubitemid 41023240)
85. Yamashima T, Kohda Y, Tsuchiya K, Ueno T, Yamashita J, Yoshioka T, Kominami E. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis'. Eur J Neurosci. 1998;10:1723-1733.
86. Schnitzer E, Pinchuk I, Lichtenberg D. Peroxidation of liposomal lipids. Eur Biophys J. 2007;36:499-515. (Pubitemid 46626218)
87. Kim C, Kim JY, Kim JH. Cytosolic phospholipase A(2), lipoxygenase metabolites, and reactive oxygen species. BMB Rep. 2008;41:555-559.
88. Burke JE, Dennis EA. Phospholipase A2 biochemistry. Cardiovasc Drugs Ther. 2009;23:49-59.
89. Suffys P, Beyaert R, De Valck D, Vanhaesebroeck B, Van Roy F, Fiers W. Tumour-necrosis-factor-mediated cytotoxicity is correlated with phospholipase-A2 activity, but not with arachidonic acid release perse. Eur J Biochem. 1991;195:465-475.
90. Won JS, Singh I. Sphingolipid signaling and redox regulation. Free Radic Biol Med. 2006;40:1875-1888. (Pubitemid 43728861)
91. Poppe M, Reimertz C, Munstermann G, Kogel D, Prehn JH. Ceramideinduced apoptosis of D283 medulloblastoma cells requires mitochondrial respiratory chain activity but occurs independently of caspases and is not sensitive to Bcl-xL overexpression. J Neurochem. 2002;82: 482-494. (Pubitemid 34831489)
92. Jayadev S, Hayter HL, Andrieu N, Gamard CJ, Liu B, Balu R, Hayakawa M, Ito F, Hannun YA. Phospholipase A2 is necessary for tumor necrosis factor alpha-induced ceramide generation in L929 cells. J Biol Chem. 1997;272:17196-17203. (Pubitemid 27289833)
93. Strelow A, Bernardo K, Adam-Klages S, Linke T, Sandhoff K, Kronke M, Adam D. Overexpression of acid ceramidase protects from tumor necrosis factor-induced cell death. J Exp Med. 2000;192:601-612.
94. Thon L, Mohlig H, Mathieu S, Lange A, Bulanova E, Winoto-Morbach S, Schutze S, Bulfone-Paus S, Adam D. Ceramide mediates caspaseindependent programmed cell death. FASEB J. 2005;19:1945-1956. (Pubitemid 41759740)
95. Antignani A, Youle RJ. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr Opin Cell Biol. 2006;18: 685-689. (Pubitemid 44692478)
96. O'Rourke B. Mitochondrial ion channels. Annu Rev Physiol. 2007;69: 19-49. (Pubitemid 46457634)
97. Crompton M, Costi A, Hayat L. Evidence for the presence of a reversible Ca2-dependent pore activated by oxidative stress in heart mitochondria. Biochem J. 1987;245:915-918.
98. Crompton M, Ellinger H, Costi A. Inhibition by cyclosporin A of a Ca2-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J. 1988;255:357-360.
99. Halestrap AP. Calcium-dependent opening of a non-specific pore in the mitochondrial inner membrane is inhibited at pH values below 7. Implications for the protective effect of low pH against chemical and hypoxic cell damage. Biochem J. 1991;278(Pt 3):715-719.
100. Griffiths EJ, Halestrap AP. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J. 1995;307(Pt 1):93-98.
101. Hunter FE Jr, Ford L. Inactivation of oxidative and phosphorylative systems in mitochondria by preincubation with phosphate and other ions. J Biol Chem. 1955;216:357-369.
102. Chappell JB, Crofts AR. Calcium ion accumulation and volume changes of isolated liver mitochondria. Calcium ion-induced swelling. Biochem J. 1965;95:378-386.
103. Haworth RA, Hunter DR. The Ca2-induced membrane transition in mitochondria. II. Nature of the Ca2 trigger site. Arch Biochem Biophys. 1979;195:460-467. (Pubitemid 9235078)
104. Halestrap AP, Woodfield KY, Connern CP. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J Biol Chem. 1997;272:3346-3354.
105. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trezeguet V, Lauquin GJ, Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature. 2003;426:39-44. (Pubitemid 37432535)
106. McStay GP, Clarke SJ, Halestrap AP. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem J. 2002;367: 541-548. (Pubitemid 35216831)
107. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, MacGregor GR, Wallace DC. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature. 2004;427:461-465. (Pubitemid 38168501)
108. Rodic N, Oka M, Hamazaki T, Murawski MR, Jorgensen M, Maatouk DM, Resnick JL, Li E, Terada N. DNA methylation is required for silencing of ANT4, an adenine nucleotide translocase selectively expressed in mouse embryonic stem cells and germ cells. Stem Cells. 2005;23:1314-1323. (Pubitemid 41504919)
109. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH. Isolation of the mitochondrial benzodiazepine receptor: association with the voltagedependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA. 1992;89:3170-3174.
110. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltagedependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol. 2007;9:550-555. (Pubitemid 46696536)
111. Krauskopf A, Eriksson O, Craigen WJ, Forte MA, Bernardi P. Properties of the permeability transition in VDAC1(-/-) mitochondria. Biochim Biophys Acta. 2006;1757:590-595. (Pubitemid 43993836)
112. Halestrap AP, Davidson AM. Inhibition of Ca(2)-induced largeamplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J. 1990;268:153-160. (Pubitemid 20166664)
113. Connern CP, Halestrap AP. Purification and N-terminal sequencing of peptidyl-prolyl cis-trans-isomerase from rat liver mitochondrial matrix reveals the existence of a distinct mitochondrial cyclophilin. Biochem J. 1992;284(Pt 2):381-385.
114. Elrod JW, Wong R, Mishra S, Vagnozzi RJ, Sakthievel B, Goonasekera SA, Karch J, Gabel S, Farber J, Force T, Brown JH, Murphy E, Molkentin JD. Cyclophilin D controls mitochondrial pore-dependent Ca(2) exchange, metabolic flexibility, and propensity for heart failure in mice. J Clin Invest. 2010;120:3680-3687.
115. Leung AW, Varanyuwatana P, Halestrap AP. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J Biol Chem. 2008;283:26312-26323.
116. Griffiths EJ, Halestrap AP. Further evidence that cyclosporin A protects mitochondria from calcium overload by inhibiting a matrix peptidylprolyl cis-trans isomerase. Implications for the immunosuppressive and toxic effects of cyclosporin. Biochem J. 1991;274(Pt 2):611-614.
117. Basso E, Petronilli V, Forte MA, Bernardi P. Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation. J Biol Chem. 2008;283: 26307-26311.
118. Clarke SJ, McStay GP, Halestrap AP. Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem. 2002;277:34793-34799.
119. Halestrap AP. A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochem Soc Trans. 2010;38:841-860.
120. McNeil PL, Khakee R. Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage. Am J Pathol. 1992;140:1097-1109.
121. Campbell KP. Three muscular dystrophies: loss of cytoskeletonextracellular matrix linkage. Cell. 1995;80:675-679.
122. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP. Defective membrane repair in dysferlindeficient muscular dystrophy. Nature. 2003;423:168-172. (Pubitemid 36569539)
123. Han R, Bansal D, Miyake K, Muniz VP, Weiss RM, McNeil PL, Campbell KP. Dysferlin-mediated membrane repair protects the heart from stress-induced left ventricular injury. J Clin Invest. 2007;117: 1805-1813. (Pubitemid 47036314)
124. Cai C, Masumiya H, Weisleder N, Matsuda N, Nishi M, Hwang M, Ko JK, Lin P, Thornton A, Zhao X, Pan Z, Komazaki S, Brotto M, Takeshima H, Ma J. Mg53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol. 2009;11:56-64.
125. Cai C, Masumiya H, Weisleder N, Pan Z, Nishi M, Komazaki S, Takeshima H, Ma J. MG53 regulates membrane budding and exocytosis in muscle cells. J Biol Chem. 2009;284:3314-3322.
126. Cai C, Weisleder N, Ko JK, Komazaki S, Sunada Y, Nishi M, Takeshima H, Ma J. Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3, and dysferlin. J Biol Chem. 2009;284:15894-15902.
127. Weisleder N, Takeshima H, Ma J. Mitsugumin 53 (MG53) facilitates vesicle trafficking in striated muscle to contribute to cell membrane repair. Commun Integr Biol. 2009;2:225-226.
128. Turner PR, Westwood T, Regen CM, Steinhardt RA. Increased protein degradation results from elevated free calcium levels found in muscle from Mdx mice. Nature. 1988;335:735-738.
129. Toyo-Oka T, Kawada T, Nakata J, Xie H, Urabe M, Masui F, Ebisawa T, Tezuka A, Iwasawa K, Nakajima T, Uehara Y, Kumagai H, Kostin S, Schaper J, Nakazawa M, Ozawa K. Translocation and cleavage of myocardial dystrophin as a common pathway to advanced heart failure: a scheme for the progression of cardiac dysfunction. Proc Natl Acad Sci USA. 2004;101:7381-7385. (Pubitemid 38638041)
130. Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell. 2010;140:798-804.
131. Munoz LE, Peter C, Herrmann M, Wesselborg S, Lauber K. Scent of dying cells: the role of attraction signals in the clearance of apoptotic cells and its immunological consequences. Autoimmun Rev. 2010;9: 425-430.
132. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, Van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med. 1995;182:1545-1556.
133. Krysko O, De Ridder L, Cornelissen M. Phosphatidylserine exposure during early primary necrosis (oncosis) in JB6 cells as evidenced by immunogold labeling technique. Apoptosis. 2004;9:495-500. (Pubitemid 38987586)
134. Brouckaert G, Kalai M, Krysko DV, Saelens X, Vercammen D, Ndlovu M, Haegeman G, D'Herde K, Vandenabeele P. Phagocytosis of necrotic cells by macrophages is phosphatidylserine dependent and does not induce inflammatory cytokine production. Mol Biol Cell. 2004;15: 1089-1100. (Pubitemid 38316218)
135. Miyamoto S, Murphy AN, Brown JH. Akt mediated mitochondrial protection in the heart: metabolic and survival pathways to the rescue. J Bioenerg Biomembr. 2009;41:169-180.
136. Miyamoto S, Murphy AN, Brown JH. Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ. 2008;15:521-529. (Pubitemid 351267303)
137. Muraski JA, Rota M, Misao Y, Fransioli J, Cottage C, Gude N, Esposito G, Delucchi F, Arcarese M, Alvarez R, Siddiqi S, Emmanuel GN, Wu W, Fischer K, Martindale JJ, Glembotski CC, Leri A, Kajstura J, Magnuson N, Berns A, Beretta RM, Houser SR, Schaefer EM, Anversa P, Sussman MA. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat Med. 2007;13:1467-1475. (Pubitemid 350224243)
138. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res. 2003;92:873-880. (Pubitemid 36542528)
139. Ogbi M, Johnson JA. Protein kinase Cepsilon interacts with cytochrome c oxidase subunit IV and enhances cytochrome c oxidase activity in neonatal cardiac myocyte preconditioning. Biochem J. 2006;393: 191-199. (Pubitemid 43049315)
140. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML, Heidenreich KA. Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci. 2004;24:9993-10002. (Pubitemid 39463581)
141. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW, Ziman BD, Wang S, Ytrehus K, Antos CL, Olson EN, Sollott SJ. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest. 2004;113:1535-1549. (Pubitemid 39071677)
142. Rasola A, Sciacovelli M, Chiara F, Pantic B, Brusilow WS, Bernardi P. Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc Natl Acad Sci USA. 2010;107:726-731.
143. Lim SY, Davidson SM, Mocanu MM, Yellon DM, Smith CC. The cardioprotective effect of necrostatin requires the cyclophilin-D component of the mitochondrial permeability transition pore. Cardiovasc Drugs Ther. 2007;21:467-469. (Pubitemid 350231514)
144. Puthalakath H, Villunger A, O'Reilly LA, Beaumont JG, Coultas L, Cheney RE, Huang DC, Strasser A. BMF: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science. 2001;293:1829-1832. (Pubitemid 32845780)
145. Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell. 1999;3:159-167. (Pubitemid 29292617)
146. Ricci JE, Munoz-Pinedo C, Fitzgerald P, Bailly-Maitre B, Perkins GA, Yadava N, Scheffler IE, Ellisman MH, Green DR. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell. 2004;117:773-786. (Pubitemid 38748893)
147. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ. Bax and Bak regulation of endoplasmic reticulum Ca2: a control point for apoptosis. Science. 2003;300:135-139. (Pubitemid 36423046)
148. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, Pozzan T, Korsmeyer SJ. Proapoptotic Bax and Bak regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci USA. 2005;102:105-110. (Pubitemid 40094436)
149. Palmer AE, Jin C, Reed JC, Tsien RY. Bcl-2-mediated alterations in endoplasmic reticulum Ca2 analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA. 2004;101: 17404-17409. (Pubitemid 39657417)
150. Ray R, Chen G, Vande Velde C, Cizeau J, Park JH, Reed JC, Gietz RD, Greenberg AH. 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. 2000;275: 1439-1448. (Pubitemid 30051204)
151. Yussman MG, Toyokawa T, Odley A, Lynch RA, Wu G, Colbert MC, Aronow BJ, Lorenz JN, Dorn GW II. Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy. Nat Med. 2002;8:725-730. (Pubitemid 34778726)
152. Diwan A, Krenz M, Syed FM, Wansapura J, Ren X, Koesters AG, Li H, Kirshenbaum LA, Hahn HS, Robbins J, Jones WK, Dorn GW. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of BNip3 restrains postinfarction remodeling in mice. J Clin Invest. 2007;117: 2825-2833. (Pubitemid 47529613)
153. Diwan A, Wansapura J, Syed FM, Matkovich SJ, Lorenz JN, Dorn GW II. Nix-mediated apoptosis links myocardial fibrosis, cardiac remodeling, and hypertrophy decompensation. Circulation. 2008;117: 396-404.
154. Diwan A, Matkovich SJ, Yuan Q, Zhao W, Yatani A, Brown JH, Molkentin JD, Kranias EG, Dorn GW II. Endoplasmic reticulummitochondria crosstalk in Nix-mediated murine cell death. J Clin Invest. 2009;119:203-212.
155. Chen Y, Lewis W, Diwan A, Cheng EH, Matkovich SJ, Dorn GW II. Dual autonomous mitochondrial cell death pathways are activated by Nix/BNip3L and induce cardiomyopathy. Proc Natl Acad Sci USA. 2010;107:9035-9042.
156. Klee M, Pallauf K, Alcala S, Fleischer A, Pimentel-Muinos FX. Mitochondrial apoptosis induced by BH3-only molecules in the exclusive presence of endoplasmic reticular Bak. EMBO J. 2009;28:1757-1768.
157. Kajstura J, Cheng W, Reiss K, Clark WA, Sonnenblick EH, Krajewski S, Reed JC, Olivetti G, Anversa P. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest. 1996;74:86-107. (Pubitemid 26041012)
158. Wencker D, Chandra M, Nguyen K, Miao W, Garantziotis S, Factor SM, Shirani J, Armstrong RC, Kitsis RN. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest. 2003;111:1497-1504. (Pubitemid 38063282)
159. Christofferson DE, Yuan J. Cyclophilin A release as a biomarker of necrotic cell death. Cell Death Differ. 2010;17:1942-1943.
160. Caulfield J, Klionsky B. Myocardial ischemia and early infarction: an electron microscopic study. Am J Pathol. 1959;35:489-523.
161. Lee P, Sata M, Lefer DJ, Factor SM, Walsh K, Kitsis RN. Fas pathway is a critical mediator of cardiac myocyte death and MI during ischemiareperfusion in vivo. Am J Physiol Heart Circ Physiol. 2003;284: H456-H463. (Pubitemid 36142871)
162. Jeremias I, Kupatt C, Martin-Villalba A, Habazettl H, Schenkel J, Boekstegers P, Debatin KM. Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia. Circulation. 2000;102:915-920.
163. Kurrelmeyer KM, Michael LH, Baumgarten G, Taffet GE, Peschon JJ, Sivasubramanian N, Entman ML, Mann DL. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemicinduced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci USA. 2000;97:5456-5461. (Pubitemid 30313740)
164. Burchfield JS, Dong JW, Sakata Y, Gao F, Tzeng HP, Topkara VK, Entman ML, Sivasubramanian N, Mann DL. The cytoprotective effects of tumor necrosis factor are conveyed through tumor necrosis factor receptor-associated factor 2 in the heart. Circ Heart Fail. 2010;3: 157-164.
165. Brocheriou V, Hagege AA, Oubenaissa A, Lambert M, Mallet VO, Duriez M, Wassef M, Kahn A, Menasche P, Gilgenkrantz H. Cardiac functional improvement by a human Bcl-2 transgene in a mouse model of ischemia/reperfusion injury. J Gene Med. 2000;2:326-333.
166. 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.
167. Hochhauser E, Kivity S, Offen D, Maulik N, Otani H, Barhum Y, Pannet H, Shneyvays V, Shainberg A, Goldshtaub V, Tobar A, Vidne BA. Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol Heart Circ Physiol. 2003;284: H2351-H2359. (Pubitemid 36622451)
168. Nazareth W, Yafei N, Crompton M. Inhibition of anoxia-induced injury in heart myocytes by cyclosporin A. J Mol Cell Cardiol. 1991;23: 1351-1354.
169. Griffiths EJ, Halestrap AP. Protection by cyclosporin A of ischemia/ reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol. 1993;25:1461-1469. (Pubitemid 24049454)
170. Hausenloy DJ, Duchen MR, Yellon DM. Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury. Cardiovasc Res. 2003;60:617-625. (Pubitemid 37501119)
171. Argaud L, Gateau-Roesch O, Muntean D, Chalabreysse L, Loufouat J, Robert D, Ovize M. Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. J Mol Cell Cardiol. 2005;38:367-374. (Pubitemid 40215206)
172. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, Macia C, Raczka F, Sportouch C, Gahide G, Finet G, Andre-Fouet X, Revel D, Kirkorian G, Monassier JP, Derumeaux G, Ovize M. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med. 2008;359:473-481.
173. Mewton N, Croisille P, Gahide G, Rioufol G, Bonnefoy E, Sanchez I, Cung TT, Sportouch C, Angoulvant D, Finet G, Andre-Fouet X, Derumeaux G, Piot C, Vernhet H, Revel D, Ovize M. Effect of cyclosporine on left ventricular remodeling after reperfused myocardial infarction. J Am Coll Cardiol. 2010;55:1200-1205.
174. Guerra S, Leri A, Wang X, Finato N, Di Loreto C, Beltrami CA, Kajstura J, Anversa P. Myocyte death in the failing human heart is gender dependent. Circ Res. 1999;85:856-866. (Pubitemid 29504161)
175. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA, Quaini E, Di Loreto C, Beltrami CA, Krajewski S, Reed JC, Anversa P. Apoptosis in the failing human heart. N Engl J Med. 1997;336: 1131-1141.
176. Saraste A, Pulkki K, Kallajoki M, Heikkila P, Laine P, Mattila S, Nieminen MS, Parvinen M, Voipio-Pulkki LM. Cardiomyocyte apoptosis and progression of heart failure to transplantation. Eur J Clin Invest. 1999;29:380-386. (Pubitemid 29209759)
177. Pacher P, Szabo C. Role of poly(ADP-ribose) polymerase 1 (PARP-1) in cardiovascular diseases: the therapeutic potential of PARP inhibitors. Cardiovasc Drug Rev. 2007;25:235-260. (Pubitemid 47547464)
178. Khalil PN, Neuhof C, Huss R, Pollhammer M, Khalil MN, Neuhof H, Fritz H, Siebeck M. Calpain inhibition reduces infarct size and improves global hemodynamics and left ventricular contractility in a porcine myocardial ischemia/reperfusion model. Eur J Pharmacol. 2005;528: 124-131. (Pubitemid 41773662)
179. Townsend D, Turner I, Yasuda S, Martindale J, Davis J, Shillingford M, Kornegay JN, Metzger JM. Chronic administration of membrane sealant prevents severe cardiac injury and ventricular dilatation in dystrophic dogs. J Clin Invest. 2010;120:1140-1150.