Targeting mitochondria for cardiac protection

Current Drug Targets

Volumn 14, Issue 5, 2013, Pages 586-600

  Hernández Reséndiz, Sauri ^a   Buelna Chontal, Mabel ^a   Correa, Francisco ^a   Zazueta, Cecilia ^a  

^a INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

Author keywords

Apoptosis; Cardioprotection; Fusion and fission processes; Mitochondrial biogenesis; Mitochondrial calcium transport; Oxidative stress

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); ANION CHANNEL; CALCIUM CHANNEL; CURCUMIN; ION CHANNEL; ISORHAMNETIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL PROTEIN; N (4 CHLOROPHENYL) N' CYANO N'' (6 CYANO 3, 4 DIHYDRO 3 HYDROXY 2, 2 DIMETHYL 2H 1 BENZOPYRAN 4 YL) GUANIDINE; N (4 CHLOROPHENYL) N' CYANO N'' (6 CYANO 3,4 DIHYDRO 3 HYDROXY 2,2 DIMETHYL 2H 1 BENZOPYRAN 4 YL)GUANIDINE; POTASSIUM CHANNEL; REACTIVE OXYGEN METABOLITE; RESVERATROL; RUTHENIUM DERIVATIVE; SILIBININ; SULFORAPHANE; UNCLASSIFIED DRUG; VALSARTAN; VOLTAGE DEPENDENT ANION CHANNEL;

APOPTOSIS; AUTOPHAGY; BIOGENESIS; CALCIUM HOMEOSTASIS; CELL FUNCTION; CHANNELOPATHY; CLINICAL TRIAL (TOPIC); HEART ARRHYTHMIA; HEART DISEASE; HEART INFARCTION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; MEMBRANE CHANNEL; MITOCHONDRION; NECROSIS; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW;

ANIMALS; ANTIOXIDANTS; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CELL DEATH; DRUG DESIGN; HUMANS; ION TRANSPORT; MEMBRANE TRANSPORT MODULATORS; MITOCHONDRIA, HEART; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL TURNOVER; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE OXYGEN SPECIES;

EID: 84876700740     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450111314050008     Document Type: Review

References (186)

1. Hernández-Reséndiz S, Buelna Chontal M, Correa F, Zazueta C. Oxidative stress and mitochondrial dysfunction in cardiovascular diseases. In: Oxidative Stress and Diseases. Eds. Dr. Volodymyr Lushchak, ISBN: 978-953-51-0527-7. In TECh, 2012.
2. Modrianský M, Gabrielová E. Uncouple my heart: the benefits of inefficiency. J Bioenerg Biomembr 2009; 41: 133-6.
3. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol 2003; 4: 517-29.
4. Maack C, O'Rourke B. Excitation-contraction coupling and mitochondrial energetics. Basic Res Cardiol 2007; 102: 369-92.
5. Chen H, Chan DC. Emerging functions of mammalian mitochondrial fusion and fission. Hum Mol Genet 2005; 14: R283-9.
6. McBride HM, Neuspiel M, Wasiak S. Mitochondria: More than just a powerhouse. Curr Biol 2006; 16: R551-560.
7. Correa F, Martínez-Abundis E, Hernández-Reséndiz S, et al. Pharmacological strategies to contend against myocardial reperfusion damage: diverse chemicals for multiple targets. Curr Med Chem 2010; 17: 2261-73.
8. Stowe DF, Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 2009; 11: 1373-414.
9. Matsushima S, Ide T, Yamato M, et al. Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 2006; 113: 1779-86.
10. Madamanchi N, Vendrov A, Runge M. Oxidative stress and vascular disease. Arteriosclerosis & Thrombosis Vascular Biology 2005; 25: 29-38.
11. Dai DF, Chen T, Wanagat J, et al. Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 2010; 9: 536-44.
12. Shiomi T, Tsutsui H, Matsusaka H, et al. Overexpression of glutathione peroxidase prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 2004; 109: 544-9
13. Schriner SE, Linford NJ, Martin GM, et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005; 308: 1909-11.
14. Li L, Lorenzo PS, Bogi K, et al. Protein kinase C delta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol Cell Biol 1999; 19: 8547-58.
15. Bianchi P, Kunduzova O, Masini E, et al. Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 2005; 112; 3297-305.
16. Kaludercic N, Takimoto E, Nagayama T, et al. Monoamine oxidase A-mediated enhanced catabolism of norepinephrine contributes to adverse remodeling and pump failure in hearts with pressure overload. Circ Res 2010; 106: 193-202.
17. Bianchi P, Pimentel D, Murphy M, Colucci W, Parini A. A new hypertrophic mechanism of serotonin in cardiac myocytes: receptor-independent ROS generation. FASEB J 2005; 19: 641-3.
18. Brookes PS, Yoon Y, Robotham JL, et al. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004; 287: C817-C833.
19. Sloan RC, Moukdar F, Frasier CR, et al. Mitochondrial permeability transition in the diabetic heart: contributions of thiol redox state and mitochondrial calcium to augmented reperfusion injury. J Mol Cell Cardiol 2012; 52: 1009-18.
20. Goh SS, Woodman OL, Pepe S, Cao AH, Qin C, Ritchie RH. The red wine antioxidant resveratrol prevents cardiomyocyte injury following ischemia-reperfusion via multiple sites and mechanisms. Antioxid Redox Signal 2007; 9: 101-13.
21. Gutiérrez-Pérez A, Cortés-Rojo C, Noriega-Cisneros R, et al. Protective effects of resveratrol on calcium-induced oxidative stress in rat heart mitochondria. J Bioenerg Biomembr 2011; 43: 101-7.
22. Devika PT, Mainzen Prince PS (-)Epigallocatechin-gallate (EGCG) prevents mitochondrial damage in isoproterenol-induced cardiac toxicity in albino Wistar rats: a transmission electron microscopic and in vitro study. Pharmacol Res 2008; 57: 351-7.
23. Gabrielová E, Jabůrek M, Gaák R, et al. Dehydrosilybin attenuates the production of ROS in rat cardiomyocyte mitochondria with an uncoupler-like mechanism. J Bioenerg Biomembr 2010; 42: 499-509.
24. Mukherjee S, Lekli I, Ray D, et al. Comparison of the protective effects of steamed and cooked broccolis on ischaemia-reperfusioninduced cardiac injury. Br J Nutr 2010; 103: 815-23.
25. González-Salazar A, Molina-Jijón E, Correa F, Zarco-Márquez G, et al. Curcumin protects from cardiac reperfusion damage by attenuation of oxidant stress and mitochondrial dysfunction. Cardiovasc Toxicol 2011; 11: 357-64.
26. Edaravone Acute Brain Infarction Study Group. Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction. Cerebrovasc Dis 2003; 15: 222-9.
27. Firuzi O, Miri R, Tavakkoli M, Saso L. Antioxidant therapy: current status and future prospects. Curr Med Chem 2011; 18: 3871-88.
28. Tsujita K, Shimomura H, Kawano H, et al. Effects of Edaravone on Reperfusion Injury in Patients With Acute Myocardial Infarction. Am J Cardiol 2004; 94: 481-4.
29. Yagi H, Horinaka S, Matsuoka H. Edaravone prevented deteriorated cardiac function after myocardial ischemia-reperfusion via inhibiting lipid peroxidation in rat. Circ J 2007; 71: 1815-20.
30. Victor VM, Rocha M. Targeting antioxidants to mitochondria: a potential new therapeutic strategy for cardiovascular diseases. Curr Pharm Des 2007; 13: 845-63.
31. Adlam VJ, Harrison JC, Porteous CM, et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 2005; 19: 1088-95.
32. Graham D, Huynh NN, Hamilton CA, et al. Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009; 54: 322-8.
33. Trnka J, Blaikie FH, Smith RA, Murphy MP. A mitochondriatargeted nitroxide is reduced to its hydroxylamine by ubiquinol in mitochondria. Free Radic Biol Med 2008; 44: 1406-19.
34. Pung YF, Rocic P, Murphy MP, et al. Resolution of mitochondrial oxidative stress rescues coronary collateral growth in Zucker obese fatty rats. Arterioscler Thromb Vasc Biol 2012; 32: 325-34.
35. Martinez-Caballero S, Dejean LM, Kinnally MS, et al. Assembly of the mitochondrial apoptosis-induced channel, MAC. J Biol Chem 2009; 284: 12235-45.
36. Hoyt KR, Sharma TA, Reynolds IJ. Trifluoperazine and dibucaineinduced inhibition of glutamate-induced mitochondrial depolarization in rat cultured forebrain neurones. Br J Pharmacol 1997; 122: 803-8.
37. Polster BM, Basanez G, Young M, et al. Inhibition of Bax-induced cytochrome c release from neural cell and brain mitochondria by dibucaine and propranolol. J Neurosci 2003; 23: 2735-43.
38. Hetz C, Vitte PA, Bombrun A, et al. Bax channel inhibitors prevent mitochondrion-mediated apoptosis and protect neurons in a model of global brain ischemia. J Biol Chem 2005; 280: 42960-70.
39. Peixoto PM, Ryu SY, Bombrun A, et al. MAC inhibitors suppress mitochondrial apoptosis. Biochem J 2009; 423: 381-387.
40. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, et al. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 2010; 31: 227-85.
41. Colombini M. Regulation of the mitochondrial outer membrane channel, VDAC. J Bioenerg Biomembr 1987; 19: 309-20.
42. Gunter TE, Sheu SS Characteristics and possible functions of mitochondrial Ca(2+) transport mechanisms. Biochim Biophys Acta 2009; 1787: 1291-308.
43. Feissner RF, Skalska J, Gaum WE, Sheu SS Crosstalk signaling between mitochondrial Ca2+ and ROS. Front Biosci 2009; 14: 1197-218.
44. Bernardi P, Krauskopf A, Basso E, et al. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 2006; 273: 2077-99.
45. Halestrap AP. What is the mitochondrial permeability transition pore? J Mol Cell Cardiol 2009; 46: 821-31.
46. De Stefani D, Raffaello A, Teardo E, et al. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011; 476(7360): 336-40.
47. Miyata H, Lakatta EG, Stern MD, Silverman HS. Relation of mitochondrial and cytosolic free calcium to cardiac myocyte recovery after exposure to anoxia. Circ Res 1992; 71: 605-13.
48. Miyamae M, Camacho SA, Weiner MW, Figueredo VM. Attenuation of postischemic reperfusion injury is related to prevention of [Ca2+]m overload in rat hearts. Am J Physiol 1996; 271: H2145-53.
49. Hajnoczky G, Csordas G, Das S, et al. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium 2006; 40: 553-60.
50. Akar FG, Aon MA, Tomaselli GF, O'Rourke B. The mitochondrial origin of postischemic arrhythmias. J Clin Invest 2005; 115: 3527-35.
51. García-Rivas GdeJ, Carvajal K, Correa F, Zazueta C. Ru360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischaemic functional recovery in rats in vivo. Br J Pharmacol 2006; 149: 829-37.
52. Beavis AD. Properties of the inner membrane anion channel in intact mitochondria. J Bioenerg Biomembr 1992; 24: 77-90.
53. Brown DA, Aon MA, Akar FG, Liu T, Sorarrain N, O'Rourke B. Effects of 4'-chlorodiazepam on cellular excitation-contraction coupling and ischaemia-reperfusion injury in rabbit heart. Cardiovasc Res 2008; 79: 141-9.
54. Wang W, Fang H, Groom L, et al. Superoxide flashes in single mitochondria. Cell 2008; 134: 279-90.
55. Arteaga D, Odor O, Lopez R, Contreras G, Aranda A, Chávez, E. Impairment by cyclosporine A of reperfusion-induced arrhythmias. Life Sci 1992; 51: 1127-34.
56. Griffiths E, Halestrap A. Protection by Cyclosporin A of ischemia/ reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 1993; 25: 1461-9.
57. Kim JS, Jin Y, Lemasters JJ. Reactive oxygen species, but not Ca2+ overloading, trigger pH-and mitochondrial permeability transitiondependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol. 2006; 290: H2024-34.
58. Correa F, Soto V, Zazueta C. Mitochondrial permeability transition relevance for apoptotic triggering in the post-ischemic heart. Int J Biochem & Cell Biol 2007; 39: 787-98.
59. Oka N, Wang L, Mi W, Caldarone CA. Inhibition of mitochondrial remodeling by cyclosporine A preserves myocardial performance in a neonatal rabbit model of cardioplegic arrest. J Thorac Cardiovasc Surg 2008a; 135: 585-93.
60. Oka N, Wang L, Mi W, et al. Cyclosporine A prevents apoptosisrelated mitochondrial dysfunction after neonatal cardioplegic arrest. J Thorac Cardiovasc Surg 2008; 135: 123-30.
61. Argaud L, Prigent AF, Chalabreysse L, et al. Ceramide in the antiapoptotic effect of ischemic preconditioning. Am J Physiol Heart Circ Physiol 2004; 286: H246-51.
62. Shanmuganathan S, Hausenloy DJ, Duchen MR, Yellon DM. Mitochondrial permeability transition pore as a target for cardioprotection in the human heart. Am J Physiol Heart Circ Physiol 2005; 289: H237-42.
63. Gomez L, Li B, Mewton N, et al. Inhibition of mitochondrial permeability transition pore opening: translation to patients. Cardiovasc Res 2009; 83(2): 226-33.
64. García-Rivas GdeJ, Guerrero-Hernández A, Guerrero-Serna G, Rodríguez-Zavala JS, Zazueta C. Inhibition of the mitochondrial calcium uniporter by the oxo-bridged dinuclear ruthenium amine complex (Ru360) prevents from irreversible injury in postischemic rat heart. FEBS J 2005; 272: 3477-88.
65. Xi J, Wang H, Mueller RA, et al. Mechanism for resveratrolinduced cardioprotection against reperfusion injury involves glycogen synthase kinase 3beta and mitochondrial permeability transition pore. Eur J Pharmacol 2009; 604: 111-6.
66. Bernardi P. Mitochondrial transport of cations: channels, exchangers and permeability transition. Physiol Rev 1999; 79: 1127-55.
67. Czyz A, Szewczyk A, Nałecz MJ, Wojtczak L. The role of mitochondrial potassium fluxes in controlling the protonmotive force in energized mitochondria. Biochem Biophys Res Commun 1995; 210: 98-104.
68. Szewczyk A, Pikula S, Wojcik G, Nalecz MJ. Glibenclamide inhibits mitochondrial K+ and Na+ uniports induced by magnesium depletion. Int J Biochem Cell Biol 1996; 28: 863-971.
69. Debska G, May R, Kicinska A, et al. Potassium channel openers depolarize hippocampal mitochondria. Brain Res 2001; 892: 42-50.
70. Debska G, Kicinska A, Skalska J, et al. Opening of potassium channels modulates mitochondrial function in rat skeletal muscle. Biochim Biophys Acta 2002; 1556: 97-105.
71. Kulawiak B, Kudin AP, Szewczyk A, Kunz WS. BK channel openers inhibit ROS production of isolated rat brain mitochondria. Exp Neurol 2008; 212: 543-547.
72. Szewczyk A, Wojcik G, Lobanov NA, Nalecz MJ. The mitochondrial sulfonylurea receptor: identification and characterization. Biochem Biophys Res Commun 1997; 230: 611-5.
73. Gross GJ, Peart JN. KATP channels and myocardial preconditioning: an update. Am J Physiol Heart Circ Physiol 2003; 285: H921-H930.
74. Yang XM, Krieg T, Cui L, et al. NECA and bradykinin at reperfusion reduce infarction in rabbit hearts by signaling through PI3K, ERK, and NO. J Mol & Cell Card 2004; 36: 411-21.
75. Jang Y, Xi J, Wang H, Mueller RA, et al. Postconditioning prevents reperfusion injury by activating delta-opioid receptors. Anesthesiology 2008; 108: 243-50.
76. Kin H, Zatta AJ, Lofye MT, et al. Postconditioning reduces infarct size via adenosine receptor activation by endogenous adenosine. Cardiovasc Res 2005; 67: 124-33.
77. Jabůrek M, Costa AD, Burton JR, et al. Mitochondrial PKC epsilon and mitochondrial ATP-sensitive K+ channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ Res 2006; 99: 878-83.
78. Costa A, Garlid K. Intramitochondrial signaling: interactions among mitoKATP, PKCε, ROS, and MPT. Am J Physiol 2008; 295: H874-82.
79. Quinlan CL, Costa AD, Costa CL, et al. Conditioning the heart induces formation of signalosomes that interact with mitochondria to open mitoKATP channels. Am J Physiol Heart Circ Physiol 2008; 295: H953-H961.
80. Facundo HT, Fornazari M, Kowaltowski AJ. Tissue protection mediated by mitochondrial K+ channels. Biochim Biophys Acta 2006; 1762: 202-12.
81. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008; 88: 581-609.
82. Comelli M, Metelli G, Mavelli I. Down modulation of mitochondrial F0F1 ATP synthase by diazoxide in cardiac myoblasts: a dual effect of the drug. Am J Physiol Heart Circ Physiol 2007; 292: H820-H829.
83. Hanley PJ, Mickel M, Loffler M, et al. K(ATP) channelindependent targets of diazoxide and 5-hydroxydecanoate in the heart. J Physiol 2002; 542: 735-741.
84. Riess ML, Camara AK, Heinen A, et al. KATP channel openers have opposite effects on mitochondrial respiration under different energetic conditions. J Cardiovasc Pharmacol 2008; 51: 483-91.
85. Schafer G, Wegener C, Portenhauser R, Bojanovski, D. Diazoxide, an inhibitor of succinate oxidation. Biochem Pharmacol 1969; 18: 2678-81.
86. Droese S, Brandt U, Hanley PJ. K+-Independent actions of diazoxide question the role of inner membrane KATP channels in mitochondrial cytoprotective signaling. J Biol Chem 2006; 281: 23733-9.
87. Liu B, Zhu X, Chen CL, et al. Opening of the mitoK(ATP) channel and decoupling of mitochondrial complex II and III contribute to the suppression of myocardial reperfusion hyperoxygenation. Mol Cell Biochem 2010; 337: 25-38.
88. Minners J, Lacerda L, Yellon DM, et al. Diazoxide-induced respiratory inhibition-a putative mitochondrial K(ATP) channel independent mechanism of pharmacological preconditioning. Mol Cell Biochem 2007; 294: 11-18.
89. Lee JH, Jung IS, Lee SH, et al. Cardioprotective effects of BMS-180448, a prototype mitoK(ATP) channel opener, and the role of salvage kinases, in the rat model of global ischemia and reperfusion heart injury. Arch Pharm Res 2007; 30: 634-40.
90. Kim M, Kim MJ, Yoon IS, et al. Diazoxide acts more as a PKCepsilon activator, and indirectly activates the mitochondrial K(ATP) channel conferring cardioprotection against hypoxic injury. Brit J Pharmacol 2006; 149: 1059-70.
91. Chiu PY, Wong SM, Leung HY, et al. Acute treatment with Danshen-Gegen decoction protects the myocardium against ischemia/ reperfusion injury via the redox-sensitive PKCε/mK(ATP) pathway in rats. Phytomedicine 2011; 18: 916-25.
92. Song DK, Jang Y, Kim JH, et al. Polyphenol (-)-Epigallocatechin Gallate during Ischemia Limits Infarct Size Via Mitochondrial KATP Channel Activation in Isolated Rat Hearts. J Korean Med Sci 2010; 25: 380-6.
93. Liu Y, Sato T, Seharaseyon J, et al. Mitochondrial ATP-dependent potassium channels. Viable candidate effectors of ischemic preconditioning. Ann NY Acad Sci USA 1999; 874: 27-37.
94. Rajesh KG, Sasaguri S, Suzuki R. Ischemic preconditioning prevents reperfusion heart injury in cardiac hypertrophy by activation of mitochondrial KATP channels. Int J Cardiol 2004; 96: 41-9.
95. Headrick JP, Willems L, Ashton KJ, et al. Ischaemic tolerance in aged mouse myocardium: the role of adenosine and effects of A1 adenosine receptor overexpression. J Physiol 2003; 549: 823-33.
96. Imani A, Faghihi M, Sadr SS, et al. Noradrenaline reduces ischemia-induced arrhythmia in anesthetized rats: involvement of alpha1-adrenoceptors and mitochondrial K ATP channels. J Cardiovasc Electrophysiol 2008; 19: 309-15.
97. Piot C, Croisille C, Staat P, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008; 359: 473-81.
98. Ghaffari S, Kazemi B, Toluey M, Sepehrvand N. The effect of prethrombolytic cyclosporine-A injection on clinical outcome of acute anterior ST-elevation myocardial infarction. Cardiovasc Ther 2012; [Epub ahead of print].
99. Sumner MD, Elliott-Eller M, Weidner G, et al. Effects of pomegranate juice consumption on myocardial perfusion in patients with coronary heart disease. Am J Cardiol 2005; 96: 810-4.
100. Vang O, Ahmad N, Baile CA, et al. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 2011; 6: e19881
101. Deja MA, Malinowski M, Gołba KS, et al. Diazoxide protects myocardial mitochondria, metabolism, and function during cardiac surgery: a double-blind randomized feasibility study of diazoxidesupplemented cardioplegia. J Thorac Cardiovasc Surg 2009: 137: 997-1004.
102. Vanlangenakker N, Vanden Berghe T, Krysko DV, et al. Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 2008; 8: 207-220.
103. Abdallah Y, Kasseckert SA, Iraqi W, et al. Interplay between Ca2+ cycling and mitochondrial permeability transition pores promotes reperfusion-induced injury of cardiac myocytes. J Cell Mol Med 2011; 15: 2478-85.
104. Rutledge MR, Farah V, Adeboye AA, et al. Parathyroid hormone, a crucial mediator of pathologic cardiac remodeling in aldosteronism. Cardiovasc Drugs Ther 2013; 27(2): 161-70.
105. Henriquez M, Armisen R, Stutzin A, Quest AF. Cell death by necrosis, a regulated way to go. Curr Mol Med 2008; 8: 187-206.
106. Whelan RS, Konstantinidis K, Wei AC, et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci USA 2012; 109: 6566-71.
107. Fliss H, Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res 1996; 79: 949-956.
108. Gottlieb RA, Burleson KO, Kloner RA, et al. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 1994; 94: 1621-8.
109. Kong CW, Hsu TG, Lu FJ, Chan WL, Tsai K. Leukocyte mitochondria depolarization and apoptosis in advanced heart failure: clinical correlations and effect of therapy. J Am Coll Cardiol 2001; 38: 1693-700.
110. Saraste A, Pulkki K, Kallajoki M, et al. Apoptosis in human acute myocardial infarction. Circulation 1997; 95: 320-23.
111. Kang PM, Izumo S. Apoptosis and heart failure: a critical review of the literature. Circ Res 2000; 86: 1107-1113.
112. Ozaki T, Tomita H, Tamai M, Ishiguro S. Characteristics of mitochondrial calpains. J Biochem 2007; 142: 365-76.
113. Yu SW, Wang H, Poitras MF, et al. Mediation of poly(ADPribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002; 297: 259-63.
114. Chen M, He H, Zhan S, et al. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem 2001; 276: 30724-8.
115. Kar P, Samanta K, Shaikh S, et al. Mitochondrial calpain system: an overview. Arch Biochem Biophys 2010; 495: 1-7.
116. Smith MA, Schnellmann RG. Mitochondrial calpain 10 is degraded by Lon protease after oxidant injury. Arch Biochem Biophys 2012; 517: 144-52.
117. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrialdependent cell death. Nat Cell Biol 2007; 9: 550-5.
118. Cuervo A. Autophagy in sickness and in health. Trends Cell Biol 2004; 14: 70-77.
119. Tolkovsky AM. Mitophagy. Biochim Biophys Acta 2009; 1793: 1508-15.
120. 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 2012; 3: 265.
121. Sung B, Sun GB, Xiao J, et al. Isorhamnetin inhibits H2O2-induced activation of the intrinsic apoptotic pathway in H9c2 cardiomyocytes through scavenging reactive oxygen species and ERK inactivation. J Cell Biochem 2012; 473-85.
122. Martínez-Abundis E, Correa F, Pavón N, Zazueta C. Bax distribution into mitochondrial detergent-resistant microdomains is related to ceramide and cholesterol content in postischemic hearts. FEBS J 2009; 276: 5579-88.
123. Yoshida K, Inui M, Harada K, et al. Reperfusion of rat heart after brief ischemia induces proteolysis of calspectin (nonerythroid spectrin or fodrin) by calpain. Circ Res 1995; 77: 603-10.
124. Hernando V, Inserte J, Sartorio CL, Parra VM, et al. Calpain translocation and activation as pharmacological targets during myocardial ischemia/reperfusion. J Mol Cell Cardiol 2010; 49: 271-9.
125. Matsumura Y, Kusuoka H, Inoue M, et al. Protective effect of the protease inhibitor leupeptin against myocardial stunning. J Cardiovasc Pharmacol 1993; 22: 135-42.
126. Donkor IO. A survey of calpain inhibitors. Curr Med Chem 2000; 7: 1171-88.
127. Yoshikawa Y, Zhang GX, Obata K, et al. Cardioprotective effects of a novel calpain inhibitor SNJ-1945 for reperfusion injury after cardioplegic cardiac arrest. Am J Physiol Heart Circ Physiol 2010; 298: H643-H651.
128. Khalil PN, Neuhof C, Huss R, Pollhammer M, et al. 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: 124-31.
129. Balakumar P, Singh M. Anti-tumour necrosis factor-α therapy in heart failure: future directions. Basic Clin Pharmacol Toxicol 2006; 99: 391-7.
130. Chung ES, Packer M, Lo KH, Fasanmade AA, Willerson JT. Randomized, double-blind, placebo-controlled, pilot trial of infliximab, a chimeric monoclonal antibody to tumor necrosis factor-alpha, in patients with moderate-to-severe heart failure: results of the anti-TNF Therapy Against Congestive Heart Failure (ATTACH) trial. Circulation 2003; 107: 3133-40.
131. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Attenuation of ischemia/reperfusion injury in rats by a caspase inhibitor. Circulation 1998; 97: 276-81.
132. Laugwitz KL, Moretti A, Weig HJ, et al. Blocking caspaseactivated apoptosis improves contractility in failing myocardium. Hum Gene Ther 2001; 12: 2051-63.
133. Wencker D, Chandra M, Nguyen K, et al. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest 2003; 111: 1497-504.
134. Kang PM, Izumo S. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med 2003; 9: 177-82.
135. Shioi T, McMullen JR, Tarnavski O, et al. Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation 2003; 107: 1664-70.
136. Kushwaha SS, Raichlin E, Sheinin Y, et al. Sirolimus affects cardiomyocytes to reduce left ventricular mass in heart transplant recipients. Eur Heart J 2008; 29: 2742-50.
137. Scarpulla R. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiological Revisions 2008; 88: 611-38.
138. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006; 127: 1109-22.
139. Picard F, Kurtev M, Chung N, et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004; 429: 771-776.
140. Planavila A, Iglesias R, Giralt M, Villarroya F. Sirt1 acts in association with PPARα to protect the heart from hypertrophy, metabolic dysregulation, and inflammation. Cardiovasc Res 2011; 90: 276-84.
141. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 2007; 356: 1140-51.
142. Ingwall JS. Energy metabolism in heart failure and remodelling. Cardiovasc Res 2009; 81: 412-9.
143. Seymour EM, Singer AA, Bennink MR, et al. Chronic intake of a phytochemical-enriched diet reduces cardiac fibrosis and diastolic dysfunction caused by prolonged salt-sensitive hypertension. J Gerontol A Biol Sci Med Sci 2008; 63: 1034-42.
144. Thandapilly SJ, Wojciechowski P, Behbahani J, et al. Resveratrol prevents the development of pathological cardiac hypertrophy and contractile dysfunction in the SHR without lowering blood pressure. Am J Hypertens 2010; 23: 192-6.
145. Wojciechowski P, Juric D, Louis XL, et al. Resveratrol arrests and regresses the development of pressure overload-but not volume 962-8.
146. Csiszar A, Labinskyy N, Pinto JT, et al. Resveratrol induces mitochondrial biogenesis in endothelial cells. Am J Physiol Heart Circ Physiol 2009; 297: H13-20.
147. Um JH, Park SJ, Kang H, et al. AMP-activated protein kinasedeficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2010; 59: 554-63.
148. Rimbaud S, Ruiz M, Piquereau J, et al. Resveratrol improves survival, hemodynamics and energetics in a rat model of hypertension leading to heart failure. PLoS One 2011; 6: e26391.
149. Jian B, Yang S, Chaudry IH, Raju R. Resveratrol improves cardiac contractility following trauma-hemorrhage by modulating Sirt1. Mol Med 2012; 18: 209-14.
150. Villalba JM, Alcaín FJ. Sirtuin activators and inhibitors. Biofactors 2012; 38: 349-59.
151. Palacios OM, Carmona JJ, Michan S, et al. Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging, 2009; 1: 771-83.
152. Parodi-Rullan R, Barreto-Torres G, Ruiz L, et al. Direct renin inhibition exerts an anti-hypertrophic effect associated with improved mitochondrial function in post-infarction heart failure in diabetic rats. Cell Physiol Biochem 2012; 29: 841-50.
153. Irrcher I, Ljubicic V, Kirwan AF, Hood DA. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS ONE 2008; 3: e3614.
154. Mensink M, Hesselink M, Russell AP, et al. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1α and PPARβ/δ gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. International Journal of Obesity 2007; 31: 1302-10.
155. Bastin J, Aubey F, Rötig A, et al. Activation of peroxisome proliferator-activated receptor pathway stimulates the mitochondrial respiratory chain and can correct deficiencies in patients' cells lacking its components. J Clinical Endoc & Metabol 2008; 93: 1433-41.
156. Detmer S, Chan D. Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 2007; 8: 870-879.
157. Cerveny K, Tamura Y, Zhang Z, Jensen R, Sesaki H. Regulation of mitochondrial fusion and division. Trends in Cellular Biology 2007; 17: 563-9.
158. Gomes LC, Scorrano L. High levels of Fis1, a pro-fission mitochondrial protein, trigger autophagy. Biochim Biophys Acta 2008; 1777: 860-6.
159. Gottlieb RA, Gustafsson AB. Mitochondrial turnover in the heart. Biochim Biophys Acta 2011; 1813: 1295-1301.
160. Eura Y, Ishihara N, Yokota S, Mihara K. Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J Biochem 2003; 134: 333-44.
161. Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci USA 2004; 101: 15927-32.
162. Frank S, Gaume B, Bergmann-Leitner E, et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Develop Cell 2001; 1: 515-25.
163. Ingerman E, Perkins E, Marino M, et al. Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 2005; 170: 1021-7.
164. Yoon Y, Krueger W, Oswald B, McNiven M. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol & Cell Biol 2003; 23: 5409-5420.
165. Zungu M, Schisler J, Willis MS. Regulation of Mitochondrial Fusion and Fission by Ubiquitin and Small Ubiquitin-Like Modifier and Their Potential Relevance in the Heart. Circ J 2011; 75: 2513-21.
166. Brady N, Hamacher-Brady A, Westerhoff H, Gottlieb R. A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. Antioxidants & Redox Signal 2006; 8: 1651-65.
167. Kowald A, Kirkwood T. Evolution of the mitochondrial fusionfission cycle and its role in aging. Proc Natl Acad Sci USA 2011; 108: 10237-42.
168. Papanicolaou K, Khairallah R, Ngoh G, et al. Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol & Cell Biol 2011; 31: 1309-28.
169. Baricault L, Ségui B, Guégand L, et al. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp Cell Res 2007; 313: 3800-8.
170. Parra V, Eisner V, Chiong M, et al. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc Res 2008; 77: 387-97.
171. Hom J, Yu T, Yoon Y, Porter G, Sheu S. Regulation of mitochondrial fission by intracellular Ca(2+) in rat ventricular myocytes. Biochim Biophys Acta 2010; 1797: 913-21.
172. Javadov S, Rajapurohitam V, Kilic A, et al. Expression of mitochondrial fusion-fission proteins during post-infaction remodeling: the effect of NHE-1 inhibition. Basic Res Cardiol 2011; 106: 99-109.
173. Palaniyandi SS, Qi X, Yogalingam G, et al. Regulation of mitochondrial processes: A target for heart failure. Drug Discovery Today Dis Mech 2010; 7: e95-e102.
174. Ong SB, Subrayan S, Lim SY, et al. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion Injury. Circulation 2010; 121: 2012-22.
175. Baines CP, Song CX, Zheng YT, et al. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 2003; 92: 873-80.
176. Clarke SJ, Khaliulin I, Das M, Parker JE, Heesom KJ, Halestrap AP. Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res 2008; 102: 1082-90.
177. Mital R, Zhang W, Cai M, et al. Antioxidant network expression abrogates oxidative posttranslational modifications in mice. Am J Physiol Heart Circ Physiol 2011; 300: H1960-H1970.
178. Martin C, Schulz R, Post H, et al. Microdialysis-based analysis of interstitial NO in situ: NO synthase-independent NO formation during myocardial ischemia. Cardiovasc Res 2007; 74: 46-55.
179. Burwell LS, Brookes PS. Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia-reperfusion injury. Antioxid Redox Signal 2008; 10: 579-99.
180. Sun J, Murphy E. Protein S-nitrosylation and cardioprotection. Circ Res 2010; 106: 285-96.
181. Burwell LS, Nadtochiy SM, Tompkins AJ, Young S, Brookes PS. Direct evidence for S-nitrosation of mitochondrial complex I. Biochem J 2006; 394: 627-34.
182. Sawicki G, Juddutt B. Valsartan reverses post-translational modifications of the δ-subunit of ATP synthase during in vivo canine reperfused myocardial infarction. Proteomics 2007; 7: 2100-10.
183. Feng J, Zhu M, Schaub MC, et al. Phosphoproteome analysis of isoflurane-protected heart mitochondria: phosphorylation of adenine nucleotide translocator-1 on Tyr194 regulates mitochondrial function. Cardiovasc Res 2008; 80: 20-9.
184. Mayr M, Liem D, Zhang J, et al. Proteomic and metabolomic analysis of cardioprotection: Interplay between protein kinase C epsilon and delta in regulating glucose metabolism of murine hearts. J Mol Cell Cardiol 2009; 46: 268-77.
185. Murriel CL, Mochly-Rosen D. Opposing roles of delta and epsilon PKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch Biochem Biophys 2003; 420: 246-54.
186. Sivaraman V, Hausenloy D, Kolvekar S, et al. The divergent roles of protein kinase C epsilon and delta in simulated ischaemia reperfusion injury in human myocardium. J Mol Cell Cardiol 2009; 46: 758-64.