Mitochondrial membrane permeabilization and cell death during myocardial infarction: Roles of calcium and reactive oxygen species

Future Cardiology

Volumn 8, Issue 6, 2012, Pages 863-884

  Webster, Keith A ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; Bcl 2; caspase; ischemia reperfusion; necrosis; oxidative stress

Indexed keywords

2 AMINO 6 BROMO 4 (1 CYANO 2 ETHOXY 2 OXOETHYL) 4H CHROMENE 3 CARBOXYLIC ACID ETHYL ESTER; BH3 PROTEIN; CALCIUM; CALPASTATIN; CYCLOPHILIN D; CYTOCHROME C; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; FLAVINE ADENINE NUCLEOTIDE; LIPOCORTIN 5; LITHIUM; MITOFUSIN 1; MITOFUSIN 2; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SODIUM CHANNEL; SODIUM ION; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UBIDECARENONE; VOLTAGE DEPENDENT ANION CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

ACUTE HEART INFARCTION; APOPTOSIS; AUTOPHAGY; CALCIUM TRANSPORT; CELL DEATH; CELL HYPOXIA; CELL PHAGOCYTOSIS; CHROMATIN CONDENSATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE NECROSIS; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NICK END LABELING; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DEGRADATION; REPERFUSION INJURY; RESPIRATORY CHAIN; REVIEW;

APOPTOSIS; CALCIUM; CELL DEATH; CYTOSOL; HUMANS; MITOCHONDRIAL MEMBRANES; MYOCARDIAL INFARCTION; PERMEABILITY; REACTIVE OXYGEN SPECIES;

EID: 84870278725     PISSN: 14796678     EISSN: 17448298     Source Type: Journal    
DOI: 10.2217/fca.12.58     Document Type: Review

References (186)

1. Adams JM, Cory S. The Bcl-2-regulated apoptosis switch: mechanism and therapeutic potential. Curr. Opin. Immunol. 19(5), 488-496 (2007). (Pubitemid 47487452)
2. Konstantinidis K, Whelan RS, Kitsis RN. Mechanisms of cell death in heart disease. Arterioscler. Thromb. Vasc. Biol. 32(7), 1552-1562 (2012).
3. Oerlemans MI, Koudstaal S, Chamuleau SA, De Kleijn DP, Doevendans PA, Sluijter JP. Targeting cell death in the reperfused heart: pharmacological approaches for cardioprotection. Int. J. Cardiol. doi:10.1016/j.ijcard.2012.03. 055 (2012) (Epub ahead of print).
4. Machado NG, Alves MG, Carvalho RA, Oliveira PJ. Mitochondrial involvement in cardiac apoptosis during ischemia and reperfusion: can we close the box? Cardiovasc. Toxicol. 9(4), 211-227 (2009).
5. Dorn GW 2nd. Apoptotic and non-apoptotic programmed cardiomyocyte death in ventricular remodelling. Cardiovasc. Res. 81(3), 465-473 (2009).
6. Hamacher-Brady A, Brady NR, Gottlieb RA. The interplay between pro-death and pro-survival signaling pathways in myocardial ischemia/reperfusion injury: apoptosis meets autophagy. Cardiovasc. Drugs Ther. 20(6), 445-462 (2006). (Pubitemid 46150867)
7. Webster KA, Graham RM, Thompson JW et al. Redox stress and the contributions of BH3-only proteins to infarction. Antioxid. Redox. Signal. 8(9-10), 1667-1676 (2006). (Pubitemid 44726340)
8. Degterev A, Yuan J. Expansion and evolution of cell death programmes. Nat. Rev. Mol. Cell. Biol. 9(5), 378-390 (2008). (Pubitemid 351574200)
9. Jung JE, Kim GS, Chen H et al. Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol. Neurobiol. 41(2-3), 172-179 (2010).
10. Nieminen AL. Apoptosis and necrosis in health and disease: role of mitochondria. Int. Rev. Cytol. 224, 29-55 (2003).
11. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat. Med. 17(7), 796-808 (2011).
12. Baines CP, Kaiser RA, Purcell NH et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662 (2005). (Pubitemid 40488559)
13. Nakagawa T, Shimizu S, Watanabe T et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434(7033), 652-658 (2005). (Pubitemid 40488558)
14. Halestrap AP. What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46, 821-831 (2009).
15. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrialdependent cell death. Nat. Cell. Biol. 9(5), 550-555 (2007). (Pubitemid 46696536)
16. Gustafsson AB, Gottlieb RA. Bcl-2 family members and apoptosis, taken to heart. Am. J. Physiol. Cell. Physiol. 292, C45-C51 (2006).
17. Juhaszova M, Zorov DB, Kim SH et al. Glycogen synthase kinase-3b mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 113(11), 1535-1549 (2004). (Pubitemid 39071677)
18. Hunter DR, Haworth RA, Southard JH. Relationship between configuration, function, and permeability in calcium-treated mitochondria. J. Biol. Chem. 1251(16), 5069-5077 (1976).
19. 2+ trigger site. Arch. Biochem. Biophys. 195(2), 460-467 (1979). (Pubitemid 9235078)
20. 2+ overload. Eur. J. Biochem. 178, 489-501 (1988). (Pubitemid 19021853)
21. Nazareth W, Yafei N, Crompton M. Inhibition of anoxia-induced injury in heart myocytes by cyclosporin-A. J. Mol. Cell. Cardiol. 23, 1351-1354 (1991).
22. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 116, 205-219 (2004). (Pubitemid 38167313)
23. Tsujimoto Y, Nakagawa T, Shimizu S. Mitochondrial membrane permeability transition and cell death. Biochim. Biophys. Acta 1757, 1297-1300 (2006). (Pubitemid 44442106)
24. Whelan RS, Konstantinidis K, Wei AC et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc. Natl Acad. Sci. USA 109, 6566-6571 (2012).
25. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399, 483-487 (1999). (Pubitemid 29258855)
26. Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell. Biol. 152, 237-250 (2001). (Pubitemid 34285595)
27. Crompton M. On the involvement of mitochondrial intermembrane junctional complexes in apoptosis. Curr. Med. Chem. 10, 1473-1484 (2003). (Pubitemid 36896551)
28. Lemasters JJ, Holmuhamedov E. Voltagedependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim. Biophys. Acta 1762, 1181-1190 (2006).
29. Majewski N, Nogueira V, Bhaskar P et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830 (2004). (Pubitemid 39586539)
30. Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS. The voltage-dependent anion channel (VDAC): function in intracellular signaling, cell life and cell death. Curr. Pharm. Design 12, 2249-2270 (2006). (Pubitemid 43891398)
31. Zaid H, Abu-Hamad S, Israelson A, Nathan I, Shoshan-Barmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ. 12, 751-760 (2005). (Pubitemid 40945982)
32. Cheng E H Y, Sheiko T, Fisher JK, Craigen WJ, Korsmeyer SJ. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 5632, 513-517 (2003). (Pubitemid 36900308)
33. Kim R, Emi M, Tanabe K, Murakami S, Uchida Y, Arihiro K. Regulation and interplay of apoptotic and non-apoptotic cell death. J. Pathol. 208, 319-326 (2006). (Pubitemid 43210518)
34. Rostovtseva TK, Antonsson B, Suzuki M, Youle RJ, Colombini M, Bezrukov SM. Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 279, 13575-13583 (2004). (Pubitemid 38468883)
35. Szabó I, Zoratti M. The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. J. Biol. Chem. 266(6), 3376-3379 (1991). (Pubitemid 21909221)
36. Kaufmann T, Strasser A, Jost PJ. Fas death receptor signalling: roles of Bid and XIAP. Cell Death Differ. 19(1), 42-50 (2012).
37. Jeremias I, Kupatt C, Martin-Villaba A et al. Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia. Circulation 102, 915-920 (2000).
38. Lee P, Sata M, Lefer DJ et al. 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 (2003). (Pubitemid 36142871)
39. Zhao WS, Xu L, Wang LF et al. A 60-s postconditioning protocol by percutaneous coronary intervention inhibits myocardial apoptosis in patients with acute myocardial infarction. Apoptosis 14(10), 1204-1211 (2009).
40. 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 102(1), 43-53 (2000).
41. 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 102(1), 33-42 (2000).
42. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA 2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell 8(3), 613-621 (2001). (Pubitemid 32946938)
43. Yang QH, Church-Hajduk R, Ren J, Newton ML, Du C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 17(12), 1487-1496 (2003). (Pubitemid 36734706)
44. Oakes SA, Scorrano L, Opferman JT et al. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 102(1), 105-110 (2005). (Pubitemid 40094436)
45. Bassik MC, Scorrano L, Oakes SA, Pozzan T, Korsmeyer SJ. Phosphorylation of BCL-2 regulates ER Ca2+ homeostasis and apoptosis. EMBO J. 23(5), 1207-1216 (2004). (Pubitemid 38436884)
46. Oakes SA, Opferman JT, Pozzan T, Korsmeyer SJ, Scorrano L. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem. Pharmacol. 66(8), 1335-1340 (2003). (Pubitemid 38373319)
47. Scorrano L, Oakes SA, Opferman JT et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300(5616), 135-139 (2003). (Pubitemid 36423046)
48. Thompson JW, Graham RM, Webster KA. DNase activation by hypoxia-acidosis parallels but is independent of programmed cell death. Life Sci. 91(7-8), 223-229 (2012).
49. Ravichandran KS, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7(12), 964-974 (2007). (Pubitemid 350166061)
50. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ. Res. 110(8), 1125-1138 (2012).
51. Verfaillie T, Salazar M, Velasco G, Agostinis P. Linking ER stress to autophagy: potential implications for cancer therapy. Int. J. Cell. Biol. 2010, 930509 (2010).
52. Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circ. Res. 104(2), 150-158 (2009).
53. Sadoshima J. The role of autophagy during ischemia/reperfusion. Autophagy 4(4), 402-403 (2008). (Pubitemid 351705134)
54. 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 99(20), 12825-12830 (2002).
55. Webster KA, Graham RM, Bishopric NH. BNip3 and signal-specific programmed death in the heart. J. Mol. Cell. Cardiol. 38(1), 35-45 (2005). (Pubitemid 40038650)
56. Diwan A, Krenz M, Syed FM et al. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J. Clin. Invest. 117(10), 2825-2833 (2007). (Pubitemid 47529613)
57. Groenendyk J, Sreenivasaiah PK, Do HK, Agellon LB, Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ. Res. 107(10), 1185-1197 (2010).
58. Giricz Z, Mentzer RM Jr, Gottlieb RA. Autophagy, myocardial protection and the metabolic syndrome. J. Cardiovasc. Pharmacol. 60(2), 125-132 (2012).
59. Li Q, Zhou LY, Gao GF, Jiao JQ, Li PF. Mitochondrial network in the heart. Protein Cell 3(6), 410-418 (2012).
60. Inserte J, Barrabés JA, Hernando V, Garcia-Dorado D. Orphan targets for reperfusion injury. Cardiovasc. Res. 83(2), 169-178 (2009).
61. Pott C, Eckardt L, Goldhaber JI. Triple threat: the Na+/Ca2+ exchanger in the pathophysiology of cardiac arrhythmia, ischemia and heart failure. Curr. Drug Targets 12(5), 737-747 (2011).
62. Bers DM. Cardiac excitation contraction coupling. Nature 415, 198-205 (2002).
63. Chen-Izu Y, McCulle SL, Ward CW et al. Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys. J. 91, 1-13 (2006).
64. Collins TJ, Lipp P, Berridge MJ, Bootman MD. Mitochondrial Ca (2+) uptake depends on the spatial and temporal profile of cytosolic Ca (2+) signals. J. Biol. Chem. 276, 26411-26420 (2001).
65. Jones PP, Bazzazi H, Kargacin GJ, Colyer J. Inhibition of cAMP dependent protein kinase under conditions occurring in the cardiac dyad during a Ca2+ transient. Biophys. J. 91, 433-443 (2006).
66. Peskoff A, Post JA, Langer GA. Sarcolemmal calcium binding sites in heart: II. Mathematical model for diffusion of calcium released from the sarcoplasmic reticulum into the dyadic region. J. Membr. Biol. 129, 59-69 (1992).
67. Shannon TR, Wang F, Puglisi J, Weber C, Bers DM. A mathematical treatment of integrated Ca dynamics within the ventricular myocyte. Biophys. J. 87, 3351-3371 (2004). (Pubitemid 40468590)
68. Weber CR, Piacentino V 3rd, Ginsburg KS, Houser SR, Bers DM. Na (+)-Ca (2+) exchange current and submembrane [Ca (2+)] during the cardiac action potential. Circ. Res. 90, 182-189 (2002). (Pubitemid 34627087)
69. Rizzuto R, Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 86, 369-408 (2006).
70. Lee JA, Allen DG. Mechanisms of acute ischemic contractile failure of the heart. Role of intracellular calcium. J. Clin. Invest. 88(2), 361-367 (1991).
71. Arnaudeau S, Kelley WL, Walsh JV Jr, Demaurex N. Mitochondria recycle Ca (2) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J. Biol. Chem. 276, 29430-29439 (2001).
72. Cox DA, Matlib MA. A role for the mitochondrial Na (+)-Ca2+ exchanger in the regulation of oxidative phosphorylation in isolated heart mitochondria. J. Biol. Chem. 268, 938-947 (1993). (Pubitemid 23019725)
73. Territo PR, French SA, Balaban RS. Simulation of cardiac work transitions, in vitro: effects of simultaneous Ca2+ and ATPase additions on isolated porcine heart mitochondria. Cell Calcium 30, 19-27 (2001). (Pubitemid 32591289)
74. Maack C, O'Rourke B. Excitationcontraction coupling and mitochondrial energetics. Basic Res. Cardiol. 102(5), 369-392 (2007).
75. Kirichok Y, Krapivinsky G, Clapham DE. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364 (2004). (Pubitemid 38133664)
76. Maak C, O'Rourke B. Excitation-contraction coupling and mitochondrial bioenergetics. Basic Res. Cardiol. 102, 369-392 (2007).
77. Maack C, Cortassa S, Aon MA, Ganesan AN, Liu T, O'Rourke B. Elevated cytosolic Na+ decreases mitochondrial Ca2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 99, 172-182 (2006). (Pubitemid 44297041)
78. Skulachev VP. Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem. Sci. 26(1), 23-29 (2001). (Pubitemid 32124706)
79. Szabadkai G, Simoni AM, Chami M, Wieckowski MR, Youle RJ, Rizzuto R. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol. Cell 16(1), 59-68 (2004). (Pubitemid 39330152)
80. Turrens JF. Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344 (2003). (Pubitemid 37321833)
81. Kowaltowski AJ, De Souza-Pinto NC, Castilho RF, Vercesi AE. Mitochondria and reactive oxygen species. Free Radic. Biol. Med. 47(4), 333-343 (2009).
82. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 47, 143-183 (2007).
83. Dougherty CJ, Kubasiak LA, Frazier DP et al. Mitochondrial signals initiate the activation of c-Jun. N-terminal kinase (JNK) by hypoxia-reoxygenation. FASEB J. 18(10), 1060-1070 (2004). (Pubitemid 38859214)
84. Frazier DP, Wilson A, Dougherty CJ et al. PKC-a and TAK-1 are intermediates in the activation of c-Jun. NH2-terminal kinase by hypoxia-reoxygenation. Am. J. Physiol. Heart Circ. Physiol. 292(4), H1675-H1684 (2007). (Pubitemid 46572384)
85. Halestrap AP, Clarke SJ, Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta 1767(8), 1007-1031 (2007). (Pubitemid 47101788)
86. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS) - induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med. 192, 1001-1014 (2000).
87. Aon MA, Cortassa S, Marban E, O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278, 44735-44744 (2003). (Pubitemid 37377231)
88. Inserte J, Barrabés JA, Hernando V, Garcia-Dorado D. Orphan targets for reperfusion injury. Cardiovasc. Res. 83(2), 169-178 (2009).
89. Garcia-Dorado D, Theroux P, Duran JM et al. Selective inhibition of the contractile apparatus. A new approach to modification of infarct size, infarct composition, and infarct geometry during coronary artery occlusion and reperfusion. Circulation 85, 1160-1174 (1992).
90. Sebbag L, Verbinski SG, Reimer KA, Jennings RB. Protection of ischemic myocardium in dogs using intracoronary 2, 3-butanedione monoxime (BDM). J. Mol. Cell. Cardiol. 35, 165-176 (2003). (Pubitemid 36269191)
91. Schlack W, Uebing A, Schafer M et al. Regional contractile blockade at the onset of reperfusion reduces infarct size in the dog heart. Pflugers Arch. 428, 134-141 (1994). (Pubitemid 24238857)
92. Siegmund B, Klietz T, Schwartz P, Piper HM. Temporary contractile blockade prevents hypercontracture in anoxic-reoxygenated cardiomyocytes. Am. J. Physiol. 260, H426-H435 (1991).
93. Garcia-Dorado D, Inserte J, Ruiz-Meana M et al. Gap junction uncoupler heptanol prevents cell-to-cell progression of hypercontracture and limits necrosis during myocardial reperfusion. Circulation 96, 3579-3586 (1997). (Pubitemid 27513436)
94. Rodriguez-Sinovas A, Garcia-Dorado D, Ruiz-Meana M, Soler-Soler J. Enhanced effect of gap junction uncouplers on macroscopic electrical properties of reperfused myocardium during myocardial reperfusion. Circulation 96, 3579-3586 (2004).
95. Kokoszka JE, Waymire KG, Levy SE et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461-465 (2004). (Pubitemid 38168501)
96. Rodriguez Enriquez S, He LH, Lemasters JJ. Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int. J. Biochem. Cell. Biol. 36, 2463-2472 (2004). (Pubitemid 39119759)
97. Crompton M. On the involvement of mitochondrial intermembrane junctional complexes in apoptosis. Curr. Med. Chem. 10, 1473-1484 (2003). (Pubitemid 36896551)
98. Lemasters JJ, Holmuhamedov E. Voltagedependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim. Biophys. Acta 1762, 1181-1190 (2006).
99. Majewski N, Nogueira V, Bhaskar P et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830 (2004). (Pubitemid 39586539)
100. Piot C, Croisille P, Staat P et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N. Engl. J. Med. 359(5), 473-481 (2008).
101. Blachly-Dyson E, Forte M. VDAC channels. IUBMB Life 52, 113-118 (2001). (Pubitemid 33731563)
102. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399, 483-487 (1999). (Pubitemid 29258855)
103. Van Der 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 3, 159-167 (1999). (Pubitemid 29292617)
104. Mathupala SP, Ko YH, Pedersen PL. Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 25(34), 4777-4786 (2006). (Pubitemid 44187625)
105. Pastorino JG, Hoek JB, Shulga N. Activation of glycogen synthase kinase 3b disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapyinduced cytotoxicity. Cancer Res. 65, 10545-10554 (2005). (Pubitemid 41743749)
106. Miura T, Miki T. GSK-3b, a therapeutic target for cardiomyocyte protection. Circ. J. 73(7), 1184-1192 (2009).
107. 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. 280, H2313-H2320 (2001).
108. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltagedependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl Acad. Sci. USA 97, 3100-3105 (2000). (Pubitemid 30183262)
109. Gustafsson AB, Gottlieb RA. Bcl-2 family members and apoptosis, taken to heart. Am. J. Physiol. Cell Physiol. 292, C45-C51 (2006).
110. Juhaszova M, Zorov DB, Kim SH et al. Glycogen synthase kinase-3b mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 113(11), 1535-1549 (2004). (Pubitemid 39071677)
111. Ruiz-Meana M, Garcia-Dorado D, Miro-Casas E, Abellan A, Soler-Soler J. Mitochondrial Ca2+ uptake during simulated ischemia does not affect permeability transition pore opening upon simulated reperfusion. Cardiovasc. Res. 71, 715-724 (2006). (Pubitemid 44848013)
112. Ichas F, Jouaville LS, Mazat JP. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89(7), 1145-1153 (1997). (Pubitemid 127678747)
113. Petronilli V, Miotto G, Canton M et al. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76(2), 725-734 (1999). (Pubitemid 29264555)
114. Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell. Biol. 18(4), 157-164 (2008).
115. Lindsten T, Ross AJ, King A et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 6(6), 1389-1399 (2000). (Pubitemid 32045931)
116. Wei MC, Zong WX, Cheng EH et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292(5517), 727-730 (2001). (Pubitemid 32385543)
117. Kinnally KW, Antonsson B. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 12(5), 857-868 (2007). (Pubitemid 46653291)
118. Peixoto PM, Ryu SY, Bombrun A, Antonsson B, Kinnally KW. MAC inhibitors suppress mitochondrial apoptosis. Biochem. J. 423(3), 381-387 (2009).
119. Westphal D, Dewson G, Czabotar PE, Kluck RM. Molecular biology of Bax and Bak activation and action. Biochim. Biophys. Acta 1813(4), 521-531 (2011).
120. Hom J, Sheu SS. Morphological dynamics of mitochondria - a special emphasis on cardiac muscle cells. J. Mol. Cell. Cardiol. 46(6), 811-820 (2009).
121. Jourdain A, Martinou JC. Mitochondrial outer-membrane permeabilization and remodelling in apoptosis. Int. J. Biochem. Cell. Biol. 41(10), 1884-1889 (2009).
122. Yamaguchi R, Lartigue L. Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol. Cell 31(4), 557-569 (2008).
123. Whelan RS, Konstantinidis K, Wei AC et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc. Natl Acad. Sci. USA 109(17), 6566-6571 (2012).
124. Guo L, Pietkiewicz D, Pavlov EV et al. Effects of cytochrome c on the mitochondrial apoptosis-induced channel MAC. Am. J. Physiol. 286, C1109-C1117 (2004). (Pubitemid 38506926)
125. Tissier R, Berdeaux A, Ghaleh B et al. Making the heart resistant to infarction: how can we further decrease infarct size? Front. Biosci. 13, 284-301 (2008). (Pubitemid 351594778)
126. Skyschally A, Schulz R, Heusch G. Pathophysiology of myocardial infarction: protection by ischemic pre-and postconditioning. Herz 33(2), 88-100 (2008). (Pubitemid 351437850)
127. Zidar N, Jera J, Maja J, Dusan S. Caspases in myocardial infarction. Adv. Clin. Chem. 44, 1-33 (2007).
128. Churchill EN, Mochly-Rosen D. The roles of PKCd and e isoenzymes in the regulation of myocardial ischaemia/reperfusion injury. Biochem. Soc. Trans. 35(Pt 5), 1040-1042 (2007). (Pubitemid 350206423)
129. Palaniyandi SS, Sun L, Ferreira JC, Mochly-Rosen D. Protein kinase C in heart failure: a therapeutic target? Cardiovasc. Res. 82(2), 229-239 (2009).
130. Gustafsson AB, Tsai JG, Logue SE, Crow MT, Gottlieb RA. Apoptosis repressor with caspase recruitment domain protects against cell death by interfering with Bax activation. J. Biol. Chem. 279(20), 21233-21238 (2004). (Pubitemid 38656528)
131. Nam YJ, Mani K, Ashton AW et al. Inhibition of both the extrinsic and intrinsic death pathways through nonhomotypic death-fold interactions. Mol. Cell 15(6), 901-912 (2004). (Pubitemid 39277987)
132. Liu HR, Gao E, Hu A et al. Role of Omi/HtrA2 in apoptotic cell death after myocardial ischemia and reperfusion. Circulation 111(1), 90-96 (2005). (Pubitemid 40070849)
133. Bhuiyan MS, Fukunaga K. Activation of HtrA 2, a mitochondrial serine protease mediates apoptosis: current knowledge on HtrA2 mediated myocardial ischemia/reperfusion injury. Cardiovasc. Ther. 26(3), 224-232 (2008).
134. 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 1773(4), 577-583 (2007). (Pubitemid 46441511)
135. Roubille F, Combes S, Leal-Sanchez J et al. Myocardial expression of a dominant-negative form of Daxx decreases infarct size and attenuates apoptosis in an in vivo mouse model of ischemia/reperfusion injury. Circulation 116(23), 2709-2717 (2007). (Pubitemid 350291243)
136. Hochhauser E, Cheporko Y, Yasovich N et al. Bax deficiency reduces infarct size and improves long-term function after myocardial infarction. Cell. Biochem. Biophys. 47(1), 11-20 (2007).
137. Imahashi K, Schneider MD, Steenbergen C, Murphy E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ. Res. 95(7), 734-741 (2004). (Pubitemid 39331934)
138. Wei J, Wang W, Chopra I et al. c-Jun. N-terminal kinase (JNK-1) confers protection against brief but not extended ischemia during acute myocardial infarction. J. Biol. Chem. 286(16), 13995-14006 (2011).
139. Freude B, Masters TN, Robiczek F et al. Apoptosis is initiated by myocardial ischaemia and executed during reperfusion. J. Mol. Cell. Cardiol. 32, 197-208 (2000). (Pubitemid 30670343)
140. Van Cruchten S, Van Der Broeck W. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat. Histol. Embryol. 31, 214-223 (2002).
141. Scarabelli TM, Stephanou A, Rayment N. Apoptosis of endothelial cells precedes myocyte cell apoptosis in ischaemia/reperfusion injury. Circulation 104, 253-256 (2001). (Pubitemid 32666943)
142. Dumont EA, Hofstra L, Van Heerde WL et al. Cardiomyocyte death induced by myocardial ischemia and reperfusion measurement with recombinant human annexin-V in a mouse model. Circulation 102, 1564-1568 (2000).
143. Dumont EA, Reutelingsperger CP, Smits JF et al. Real-time imaging of apoptotic cell-membrane changes at the single-cell level in the beating murine heart. Nat. Med. 7, 1352-1355 (2001). (Pubitemid 34007941)
144. Hofstra L, Liem IH, Dumont EA et al. Visualisation of cell death in vivo in patients with acute myocardial infarction. Lancet 356, 209-212 (2000). (Pubitemid 30446976)
145. Nutt LK, Gogvadze V, Uthaisang W, Mirnikjoo B, McConkey DJ, Orrenius S. Indirect effects of Bax and Bak initiate the mitochondrial alterations that lead to cytochrome c release during arsenic trioxide-induced apoptosis. Cancer Biol. Ther. 4, 459-467 (2005). (Pubitemid 41351266)
146. Zheng Y, Shi Y, Tian C et al. Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide. Oncogene 23, 1239-1247 (2004). (Pubitemid 38297178)
147. Przygodzki T, Sokal A, Bryszewska M. Calcium ionophore A23187 action on cardiac myocytes is accompanied by enhanced production of reactive oxygen species. Biochim. Biophys. Acta 1740, 481-488 (2005). (Pubitemid 40804760)
148. Lax A, Soler F, Fernandez-Belda F. Cytoplasmic Ca2+ signals and cellular death by apoptosis in myocardiac H9c2 cells. Biochim. Biophys. Acta 1736, 937-947 (2006). (Pubitemid 44332596)
149. Wei MC, Zon WX, Cheng E H Y et al. Proapoptotic Bax and Bak; a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730 (2001). (Pubitemid 32385543)
150. Capano M, Crompton M. 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 (2006).
151. Lundberg KC, Szweda LI. Initiation of mitochondrial-mediated apoptosis during cardiac reperfusion. Arch. Biochem. Biophys. 432, 50-57 (2004). (Pubitemid 39425028)
152. Huang J, Nakamura K, Ito Y et al. Bcl-xL gene transfer inhibits Bax translocation and prolongs cardiac cold preservation time in rats. Circulation 112, 76-83 (2005). (Pubitemid 40962572)
153. Nutt LK, Pataer A, Pahler J et al. Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+ stores. J. Biol. Chem. 277, 9219-9225 (2002). (Pubitemid 34953002)
154. Nutt LK, Chandra J, Pataer A et al. Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 277, 20301-20308 (2002). (Pubitemid 34967324)
155. Hetz C, Vitte PA, Bombrun A et al. Bax channel inhibitors prevent mitochondrionmediated apoptosis and protect neurons in a model of global brain ischemia. J. Biol. Chem. 280, 42960-42970 (2005). (Pubitemid 43049259)
156. Takahashi M, Tanonaka K, Yoshida H et al. Possible involvement of calpain activation in pathogenesis of chronic heart failure after acute myocardial infarction. J. Cardiovasc. Pharacol. 47, 413-421 (2006). (Pubitemid 44309695)
157. Wencker D, Chandra M, Nguyen K et al. A mechanistic role for cardiac myocyte apoptosis in heart failure. J. Clin. Invest. 111, 1497-1404 (2003).
158. Saez ME, Ramirez-Lorca R, Moron FJ, Ruiz A. The therapeutic potential of the calpain family: new aspects. Drug Discov. Today 11, 917-923 (2006). (Pubitemid 44425428)
159. Engel T, Plesnila N, Prehn JH, Henshall DC. In vivo contributions of BH3-only proteins to neuronal death following seizures, ischemia, and traumatic brain injury. J. Cereb. Blood Flow Metab. 31(5), 1196-1210 (2011).
160. Chen M, Won DJ, Krajewski S, Gottlieb RA. Calpain and mitochondria in ischemia reperfusion injury. J. Biol. Chem. 277, 29282-29286 (2002).
161. Saez ME, Ramirez-Lorca R, Moron FJ, Ruiz A. The therapeutic potential of the calpain family: new aspects. Drug Discov. Today 11, 917-923 (2006). (Pubitemid 44425428)
162. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell. Biol. 17, 617-625 (2005). (Pubitemid 41540411)
163. Matsui T, Rosenzweig A. Convergent signal transduction pathways controlling cardiomyocyte survival and function: the role of PI 3-kinase and Akt. J. Mol. Cell. Cardiol. 38, 63-71 (2005). (Pubitemid 40038652)
164. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 22, 8983-8998 (2003). (Pubitemid 38121699)
165. Webster KA. Aktion in the nucleus. Circ. Res. 94, 856-859 (2004). (Pubitemid 38490060)
166. Yamashita K, Kajstura J, Discher DJ, Wasserlauf BJ, Anversa P, Webster KA. Reperfusion-activated Akt kinase prevents apoptosis in transgenic mouse hearts overexpressing insulin-like growth factor-1. Circ. Res. 88, 609-614 (2001). (Pubitemid 32275797)
167. Murriel CL, Churchill E, Inagaki K, Szweda LI, Mochly-Rosen D. Protein kinase Cd activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria. J. Biol. Chem. 279, 47985-47991 (2004). (Pubitemid 39540950)
168. The Direct Inhibition of f-Protein Kinase C Enzyme to Limit Total Infarct Size in Acute Myocardial Infarction (DELTA MI) Investigators. Intracoronary KAI-9803 as an adjunct to primary percutaneous coronary intervention for acute ST-segment elevation myocardial infarction. Circulation 117, 886-896 (2008).
169. Metzler B, Xu Q, Mayr M. Circulation 118 (letter) (2008).
170. Graham RM, Frazier D, Thompson JW et al. A unique pathway of cardiac myocyte death caused by hypoxia-acidosis. J. Exp. Biol. 207, 3189-3200 (2004). (Pubitemid 39275293)
171. Hamacher-Brady A, Brady NR, Gottlieb RA, Gustafsson AB. Autophagy as a protective response to Bnip3-mediated apoptotic signaling in the heart. Autophagy 2(4), 307-309 (2006). (Pubitemid 44342377)
172. Shaw J, Kirshenbaum LA. Molecular regulation of autophagy and apoptosis during ischemic and non-ischemic cardiomyopathy. Autophagy 4(4), 427-434 (2008). (Pubitemid 351705139)
173. Burton TR, Gibson SB. The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ. 16(4), 515-523 (2009).
174. Ray R, Chen G, Van De Velde C et al. 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(2), 1439-1448 (2000). (Pubitemid 30051204)
175. Hamacher-Brady A, Brady NR, Logue SE et al. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 14(1), 146-157 (2007). (Pubitemid 44911902)
176. Ray R, Chen G, Van De Velde C et al. 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(2), 1439-1448 (2000). (Pubitemid 30051204)
177. Chaanine AH, Jeong D, Liang L et al. JNK modulates FOXO3a for the expression of the mitochondrial death and mitophagy marker BNIP3 in pathological hypertrophy and in heart failure. Cell Death Dis. 3, 265 (2012).
178. Shibue T, Suzuki S, Okamoto H et al. Differential contribution of Puma and Noxa in dual regulation of p53-mediated apoptotic pathways. EMBO J. 25, 4952-4962 (2006). (Pubitemid 44607039)
179. Yu J, Zhang L. No PUMA, no death: implications for p53-dependent apoptosis. Cancer Cell 4, 248-249 (2003). (Pubitemid 37329788)
180. Erlacher M, Michalak EM, Kelly PN et al. BH3-only proteins Puma and Bim are rate-limiting for g-radiation-and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 106, 4131-4138 (2005). (Pubitemid 41775918)
181. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115, 2656-2664 (2005). (Pubitemid 41434389)
182. Kim JY, Ahn HJ, Ryu JH, Suk K, Park JH. BH3-only protein Noxa is a mediator of hypoxic cell death induced by hypoxiainducible factor 1a. J. Exp. Med. 199, 113-124 (2004).
183. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J. Cell. Biol. 162, 587-597 (2003). (Pubitemid 37022937)
184. Toth A, Jeffers JR, Nickson P et al. Targeted deletion of puma attenuates cardiomyocyte death and improves cardiac function during ischemia/reperfusion. Am. J. Physiol. Heart Circ. Physiol. 291(1), H52-H60 (2006).
185. Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, Srivastava D. MiR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J. Exp. Med. 14, 208(3), 549-560 (2011).
186. Bolli R, Chugh AR, D'Amario D et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO), initial results of a randomised Phase 1 trial. Lancet 378(9806), 1847-1857 (2011).