Mechanisms of exercise-induced cardioprotection

Physiology

Volumn 29, Issue 1, 2014, Pages 27-38

  Powers, Scott K ^a   Smuder, Ashley J ^a   Kavazis, Andreas N ^b   Quindry, John C ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN;

ANIMAL; CORONARY ARTERY DISEASE; EXERCISE; HEART; HEART MUSCLE; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REPERFUSION INJURY; REVIEW;

ANIMALS; CORONARY ARTERY DISEASE; EXERCISE; HEART; HUMANS; MITOCHONDRIAL PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM;

EID: 84891525876     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00030.2013     Document Type: Review

References (124)

1. Adderley SR, Fitzgerald DJ. Oxidative damage of cardiomyo-cytes is limited by extracellular regulated kinases 1/2-medi-ated induction of cyclooxygenase-2. J Bioi Chem 274: 5038-5046, 1999.
2. Adlam VJ, Harrison JC, Porteous CM, James AM, Smith RA, Murphy MP, Sammut IA. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 19: 1088-1095, 2005.
3. Andersson DC, Betzenhauser MJ, Reiken S, Meli AC, Uman-skaya A, Xie W, Shiomi T, Zalk R, Lacampagne A, Marks AR. Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Ceii Metab 14: 196-207, 2011.
4. Angelos MG, Kutala VK, Torres CA, He G, Stoner JD, Mohammad M, Kuppusamy P. Hypoxic reperfusion of the ischemic heart and oxygen radical generation. Am J Physiol Heart Circ Physioi 290: H341-H347, 2006.
5. Ardehali H. Role of the mitochondrial ATP-sensitive K+ channels in cardioprotection. Acta Biochim Pol 51: 379-390, 2004.
6. Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, Oliveira PJ, Duarte JA. Endurance training limits the functional alterations of rat heart mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardioi 109: 169-178, 2006.
7. Bianchi P, Kunduzova O, Masini E, Cambon C, Bani D, Rai-mondi L, Seguelas MH, Nistri S, Colucci W, Leducq N, Parini A. Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 112: 3297-3305, 2005.
8. Bolli R. Preconditioning: A paradigm shift in the biology of myocardial ischemia. Am J Physioi Heart Circ Physioi 291: H19-H27, 2006.
9. Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physioi Rev 79: 609-634, 1999.
10. Bolli R, Shinmura K, Tang XL, Kodani E, Xuan YT, Guo Y, Dawn B. Discovery of a new function of cyclooxygenase (COX)-2: COX-2 is a cardioprotective protein that alleviates ischemia/reperfusion injury and mediates the late phase of preconditioning. Cardiovasc Res 55: 506-519, 2002.
11. Bowles DK, Starnes JW. Exercise training improves metabolic response after ischemia in isolated working rat heart. J Appl Physiollb: 1608-1614, 1994.
12. Brown DA, Chicco AJ, Jew KN, Johnson MS, Lynch JM, Watson PA, Moore RL. Cardioprotection afforded by chronic exercise is mediated by the sarcolemmal, and not the mitochondrial, isoform of the KATP channel in the rat. J Physioi 569: 913-924, 2005.
13. Budiono BP, See Hoe LE, Peart JN, Sabapathy S, Ashton KJ, Haseler LJ, Headrick JP. Voluntary running in mice beneficially modulates myocardial ischemic tolerance, signaling kinases, and gene expression patterns. Am J Physioi Regul Integr Comp Physioi 302: R1091-R1100, 2012.
14. Burelle Y, Wambolt RB, Grist M, Parsons HL, Chow JC, Antler C, Bonen A, Keller A, Dunaway GA, Popov KM, Hochachka PW, Allard MF. Regular exercise is associated with a protective metabolic phenotype in the rat heart. Am J Physioi Heart Circ Physioi 287: H1055-H1063, 2004.
15. Calvert JW, Lefer DJ. Role of beta-adrenergic receptors and nitric oxide signaling in exercise-mediated cardioprotection. Physiology 28: 216-224, 2013.
16. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S, Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12: 534-541, 2011.
17. Chen Z, Siu B, Ho YS, Vincent R, Chua CC, Hamdy RC, Chua BH. Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J Mol Cell Cardiol 30: 2281-2289, 1998.
18. Coombes JS, Powers SK, Hamilton KL, Demirel HA, Shanely RA, Zergeroglu MA, Sen CK, Packer L, Ji LL. Improved cardiac performance after ischemia in aged rats supplemented with vitamin E and alpha-lipoic acid. Am J Physiol Regul Integr Comp Physiol 279: R2149-R2155, 2000.
19. Davis ME, Grumbach IM, Fukai T, Cutchins A, Harrison DG. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor kappaB binding. J Biol Chem 279: 163-168, 2004.
20. de Waard MC, van Haperen R, Soullie T, Tempel D, de Crom R, Duncker DJ. Beneficial effects of exercise training after myocardial infarction require full eNOS expression. J Mol Cell Cardiol 48: 1041-1049, 2010.
21. Demirel HA, Hamilton KL, Shanely RA, Tumer N, Koroly MJ, Powers SK. Age and attenuation of exercise-induced myocardial HSP72 accumulation. Am J Physiol Heart Circ Physiol 285: H1609-H1615, 2003.
22. Demirel HA, Powers SK, Caillaud C, Coombes JS, Naito H, Fletcher LA, Vrabas I, Jessup JV, Ji LL. Exercise training reduces myocardial lipid peroxi-dation following short-term ischemia-reperfu-sion. Med Sci Sports Exerc 30: 1211-1216, 1998.
23. Demirel HA, Powers SK, Zergeroglu MA, Shanely RA, Hamilton K, Coombes J, Naito H. Short-term exercise improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. J Appl Physiol 91: 2205-2212, 2001.
24. Doustar Y, Soufi FG, Jafary A, Saber MM, Ghias-sie R. Role of four-week resistance exercise in preserving the heart against ischaemia-reperfu-sion-induced injury. Cardiovasc J Afr 23: 451-455, 2012.
25. Downey JM. Free radicals and their involvement during long-term myocardial ischemia and reper-fusion. Annu Rev Physiol 52: 487-504, 1990.
26. Dzeja PP, Hoyer K, Tian R, Zhang S, Nemutlu E, Spindler M, Ingwall JS. Rearrangement of energetic and substrate utilization networks compensate for chronic myocardial creatine kinase deficiency. J Physiol 589: 5193-5211, 2011.
27. Foster MW, Hess DT, Stamler JS. Protein S-ni-trosylation in health and disease: a current perspective. Trends Mol Med 15: 391-404, 2009.
28. Frasier CR, Moore RL, Brown DA. Exercise-induced cardiac preconditioning: how exercise protects your achy-breaky heart. J Appl Physiol 111: 905-915, 2011.
29. Frasier CR, Moukdar F, Patel HD, Sloan RC, Stewart LM, Alleman RJ, La Favor JD, Brown DA. Redox-dependent increases in glutathione re-ductase and exercise preconditioning: role of NADPH oxidase and mitochondria. Cardiovasc Res 98: 47-55, 2013.
30. Frasier CR, Sloan RC, Bostian PA, Gonzon MD, Kurowicki J, Lopresto SJ, Anderson EJ, Brown DA. Short-term exercise preserves myocardial glutathione and decreases arrhythmias after thiol oxidation and ischemia in isolated rat hearts. J Appl Physiol 111: 1751-1759, 2011.
31. French JP, Hamilton KL, Quindry JC, Lee Y, Upchurch PA, Powers SK. Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain. FASEB J 22: 2862-2871, 2008.
32. French JP, Quindry JC, Falk DJ, Staib JL, Lee Y, Wang KK, Powers SK. Ischemia-reperfusion-induced calpain activation and SERCA2a degradation are attenuated by exercise training and calpain inhibition. Am J Physiol Heart Circ Physiol 290: H128-H136, 2006.
33. Garcia-Dorado D, Ruiz-Meana M, Inserte J, Rodriguez-Sinovas A, Piper HM. Calcium-mediated cell death during myocardial reperfusion. Cardiovasc Res 94: 168-180, 2012.
34. Gonzalez DR, Treuer AV, Castellanos J, Dulce RA, Hare JM. Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 285: 28938-28945, 2010.
35. Gottlieb RA. Mitochondria and apoptosis. Biol Signals Recept 10: 147-161, 2001.
36. Gottlieb RA. Mitochondrial signaling in apoptosis: mitochondrial daggers to the breaking heart. Basic Res Cardiol 98: 242-249, 2003.
37. Gottlieb RA, Mentzer RM Jr. Cardioprotection through autophagy: ready for clinical trial? Autophagy 7: 434-435, 2011.
38. Green DJ, Maiorana A, O'Driscoll G, Taylor R. Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol 561: 1-25, 2004.
39. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 305: 626-629, 2004.
40. Gross GJ, Peart JN. KATP channels and myocardial preconditioning: an update. Am J Physiol Heart Circ Physiol 285: H921-H930, 2003.
41. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, Baither Y, Gielen S, Thiele H, Gummert JF, Mohr FW, Schuler G. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107: 3152-3158, 2003.
42. Hamilton KL, Powers SK, Sugiura T, Kim S, Lennon S, Tumer N, Mehta JL. Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins. Am J Physiol Heart Circ Physiol 281: H1346-H1352, 2001.
43. Hamilton KL, Quindry JC, French JP, Staib J, Hughes J, Mehta JL, Powers SK. MnSOD antisense treatment and exercise-induced protection against arrhythmias. Free Radic Biol Med 37: 1360-1368, 2004.
44. Hamilton KL, Staib JL, Phillips T, Hess A, Lennon SL, Powers SK. Exercise, antioxidants, and HSP72: protection against myocardial ischemia/reperfusion. Free Radic Biol Med 34: 800-809, 2003.
45. Haskell WL, Sims C, Myll J, Bortz WM, St Goar FG, Alderman EL. Coronary artery size and dilating capacity in ultradistance runners. Circulation 87: 1076-1082, 1993.
46. Hoshida S, Yamashita N, Otsu K, Hori M. Repeated physiologic stresses provide persistent cardioprotection against ischemia-reperfusion injury in rats. J Am Coll Cardiol 40: 826-831, 2002.
47. Hsu AL, Ching TT, Wang DS, Song X, Rangnekar VM, Chen CS. The cyclooxygenase-2 inhibitor celecoxib induces apoptosis by blocking Akt activation in human prostate cancer cells independently of Bcl-2. J Biol Chem 275: 11397-11403, 2000.
48. Hutter JJ, Mestril R, Tam EK, Sievers RE, Dillmann WH, Wolfe CL. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 94: 1408-1411, 1996.
49. Ignarro LJ, Balestrieri ML, Napoli C. Nutrition, physical activity, and cardiovascular disease: an update. Cardiovasc Res 73: 326-340, 2007.
50. Inserte J, Hernando V, Garcia-Dorado D. Contribution of calpains to myocardial ischaemia/reperfusion injury. Cardiovasc Res 96: 23-31, 2012.
51. Jayakumar J, Suzuki K, Sammut IA, Smolenski RT, Khan M, Latif N, Abunasra H, Murtuza B, Amrani M, Yacoub MH. Heat shock protein 70 gene transfection protects mitochondrial and ventricular function against ischemia-reperfusion injury. Circulation 104: 303-307, 2001.
52. Joyner MJ, Green DJ. Exercise protects the cardiovascular system: effects beyond traditional risk factors. J Physiol 587: 5551-5558, 2009.
53. Judge S, Jang YM, Smith A, Selman C, Phillips T, Speakman JR, Hagen T, Leeuwenburgh C. Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am J Physiol Regul Integr Comp Physiol 289: R1564-R1572, 2005.
54. Julia P, Young HH, Buckberg GD, Kofsky ER, Bugyi HI. Studies of myocardial protection in the immature heart. II. Evidence for importance of amino acid metabolism in tolerance to ischemia. J Thorac Cardiovasc Surg 100: 888-895, 1990.
55. Kang PM, Yue P, Liu Z, Tarnavski O, Bodyak N, Izumo S. Alterations in apoptosis regulatory factors during hypertrophy and heart failure. Am J Physiol Heart Circ Physiol 287: H72-H80, 2004.
56. Kavazis AN. Exercise preconditioning of the myocardium. Sports Med 39: 923-935, 2009
57. Kavazis AN, Alvarez S, Talbert E, Lee Y, Powers SK. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol Heart Circ Physiol 297: H144-H152, 2009.
58. Kavazis AN, McClung JM, Hood DA, Powers SK. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol Heart Circ Physiol 294: H928-H935, 2008.
59. Kloner RA, Hale SL, Dai W, Gorman RC, Shuto T, Koomalsingh KJ, Gorman JH, 3rd Sloan RC, Frasier CR, Watson CA, Bostian PA, Kypson AP, Brown DA. Reduction of ischemia/reperfusion injury with bendavia, a mitochondria-targeting cytoprotective Peptide. J Am Heart Assoc 1: e001644, 2012.
60. Kong X, Tweddell JS, Gross GJ, Baker JE. Sarcolemmal and mitochondrial K(ATP)channels mediate cardioprotection in chronically hypoxic hearts. J Mol Cell Cardiol 33: 1041-1045, 2001.
61. Kubli DA, Gustafsson AB. Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res 111: 1208-1221, 2012.
62. Laughlin MH, Bowles DK, Duncker DJ. The coronary circulation in exercise training. Am J Physiol Heart Circ Physiol 302: H10-H23, 2012.
63. Lee Y, Min K, Talbert EE, Kavazis AN, Smuder AJ, Willis WT, Powers SK. Exercise protects cardiac mitochondria against ischemia-reperfusion injury. Med Sci Sports Exerc 44: 397-405, 2012.
64. Lefer DJ. Nitrite therapy for protection against ischemia-reperfusion injury. Am J Physiol Renal Physiol 290: F777-F778, 2006.
65. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787: 1395-1401, 2009
66. Lennon SL, Quindry J, Hamilton KL, French J, Staib J, Mehta JL, Powers SK. Loss of exercise-induced cardioprotection after cessation of exercise. J Appi Physioi 96: 1299-1305, 2004.
67. Lennon SL, Quindry JC, French JP, Kim S, Mehta JL, Powers SK. Exercise and myocardial tolerance to ischaemia-reperfusion. Acta Physioi Scand 182: 161-169, 2004.
68. Leon AS, Bloor CM. Effects of exercise and its cessation on the heart and its blood supply. J Appi Physioi 24: 485-490, 1968.
69. Libonati JR, Gaughan JP, Hefner CA, Gow A, Paolone AM, Houser SR. Reduced ischemia and reperfusion injury following exercise training. Med Sci Sports Exerc 29: 509-516, 1997.
70. Libonati JR, Kendrick ZV, Houser SR. Sprint training improves postischemic, left ventricular dia-stolic performance. J Appi Physioi 99: 2121-2127, 2005.
71. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Thorn T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J. Heart disease and stroke statistics: 2010 update: a report from the American Heart Association. Circulation 121: e46-e215, 2010.
72. Lofgren B, Povlsen JA, Rasmussen LE, Stottrup NB, Solskov L, Krarup PM, Kristiansen SB, Botker HE, Nielsen TT. Amino acid transamination is crucial for ischaemic cardioprotection in normal and preconditioned isolated rat hearts: focus on L-glutamate. Exp Physioi 95: 140-152, 2010.
73. Marcil M, Bourduas K, Ascah A, Burelle Y. Exercise training induces respiratory substrate-specific decrease in Ca2+-induced permeability transition pore opening in heart mitochondria. Am J Physioi Heart Circ Physioi 290: H1549-H1557, 2006.
74. Martindale JJ, Fernandez R, Thuerauf D, Whit-taker R, Gude N, Sussman MA, Glembotski CC. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ Res 98: 1186-1193, 2006.
75. Miller LE, Hosick PA, Wrieden J, Hoyt E, Quindry JC. Evaluation of arrhythmia scoring systems and exercise-induced cardioprotection. Med Sci Sports Exerc 44: 435-441, 2012.
76. Murlasits Z, Lee Y, Powers SK. Short-term exercise does not increase ER stress protein expression in cardiac muscle. Med Sci Sports Exerc 39: 1522-1528, 2007.
77. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-rep-erfusion injury. Physioi Rev 88: 581-609, 2008.
78. Nagy O, Hajnal A, Parratt JR, Vegh A. Delayed exercise-induced protection against arrhythmias in dogs: effect of celecoxib. EurJ Pharmacol 499: 197-199, 2004.
79. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature 305: 147-148, 1983.
80. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsu-kamoto O, Takashima S, Hirata A, Fujita M, Na-gamachi Y, Nakatani T, Yutani C, Ozawa K, Ogawa S, Tomoike H, Hori M, Kitakaze M. Prolonged endoplasmic reticulum stress in hypertro-phic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 110: 705-712, 2004.
81. Ong SB, Hall AR, Hausenloy DJ. Mitochondrial dynamics in cardiovascular health and disease. Antioxid Redox Signal 19: 400-414, 2012.
82. Padrao AI, Ferreira R, Vitorino R, Alves RM, Figueiredo P, Duarte JA, Amado F. Effect of lifestyle on age-related mitochondrial protein oxidation in mice cardiac muscle. Eur J Appl Physiol 112: 1467-1474, 2012.
83. Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, Ward JL, 3rd Goodyear LJ, Tong Q. Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Milano) 1: 771-783, 2009.
84. Patel HH, Gross ER, Peart JN, Hsu AK, Gross GJ. Sarcolemmal KATP channel triggers delayed ischemic preconditioning in rats. Am J Physiol Heart Circ Physiol 288: H445-H447, 2005.
85. Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, Seif I, Parini A, Cuvillier O. Oxidative stress-dependent sphingosine ki-nase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res 100: 41-49, 2007.
86. Peng TI, Jou MJ. Oxidative stress caused by mi-tochondrial calcium overload. Ann NY Acad Sci 1201: 183-188, 2010.
87. Porter K, Medford HM, McIntosh CM, Marsh SA. Cardioprotection requires flipping the 'post-translational modification' switch. Life Sci 90: 89-98, 2012.
88. Powers SK, Criswell D, Lawler J, Martin D, Lieu FK, Ji LL, Herb RA. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. Am J Physiol Heart Circ Physiol 265: H2094-H2098, 1993.
89. Powers SK, Demirel HA, Vincent HK, Coombes JS, Naito H, Hamilton KL, Shanely RA, Jessup J. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol Regul Integr Comp Physiol 275: R1468-R1477, 1998.
90. Powers SK, Jackson MJ. Exercise-induced oxida-tive stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
91. Powers SK, Murlasits Z, Wu M, Kavazis AN. Ischemia-reperfusion-induced cardiac injury: a brief review. Med Sci Sports Exerc 39: 1529-1536, 2007.
92. Powers SK, Quindry JC, Kavazis AN. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 44: 193-201, 2008.
93. Quindry J, French J, Hamilton K, Lee Y, Mehta JL, Powers S. Exercise training provides cardiopro-tection against ischemia-reperfusion induced apoptosis in young and old animals. Exp Geron-tol 40: 416-425, 2005.
94. Quindry JC, French J, Hamilton KL, Lee Y, Selsby J, Powers S. Exercise does not increase cycloox-ygenase-2 myocardial levels in young or senescent hearts. J Physiol Sci 60: 181-186, 2010.
95. Quindry JC, Hamilton KL, French JP, Lee Y, Mur-lasits Z, Tumer N, Powers SK. Exercise-induced HSP-72 elevation and cardioprotection against infarct and apoptosis. J Appl Physiol 103: 1056-1062, 2007.
96. Quindry JC, Miller L, McGinnis G, Kliszczewicz B, Irwin JM, Landram M, Urbiztondo Z, Nanayak-kara G, Amin R. Ischemia reperfusion injury, KATP channels, and exercise-induced cardiopro-tection against apoptosis. J Appl Physiol 113: 498-506, 2012.
97. Quindry JC, Schreiber L, Hosick P, Wrieden J, Irwin JM, Hoyt E. Mitochondrial KATP channel inhibition blunts arrhythmia protection in ische-mic exercised hearts. Am J Physiol Heart Circ Physiol 299: H175-H183, 2010.
98. Reeve JL, Duffy AM, O'Brien T, Samali A. Don't lose heart: therapeutic value of apoptosis prevention in the treatment of cardiovascular disease. J Cell Mol Med 9: 609-622, 2005.
99. Rodrigo GC, Standen NB. ATP-sensitive potassium channels. Curr Pharm Des 11: 1915-1940, 2005.
100. Sciarretta S, Hariharan N, Monden Y, Zablocki D, Sadoshima J. Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr Cardiol 32: 275-281, 2011.
101. Shinmura K, Tang XL, Wang Y, Xuan YT, Liu SQ, Takano H, Bhatnagar A, Bolli R. Cyclooxygen-ase-2 mediates the cardioprotective effects of the late phase of ischemic preconditioning in conscious rabbits. Proc Nati Acad Sci USA 97: 10197-10202, 2000.
102. Siems W, Capuozzo E, Lucano A, Salerno C, Crifo C. High sensitivity of plasma membrane ion transport ATPases from human neutrophils towards 4-hydroxy-2,3-trans-nonenal. Life Sci 73: 2583-2590, 2003.
103. Soufi FG, Saber MM, Ghiassie R, Alipour M. Role of 12-week resistance training in preserving the heart against ischemia-reperfusion-induced injury. Cardiol J 18: 140-145, 2011.
104. Stanley WC, Lopaschuk GD, McCormack JG. Regulation of energy substrate metabolism in the diabetic heart. Cardiovasc Res 34: 25-33, 1997.
105. Starnes JW, Barnes BD, Olsen ME. Exercise training decreases rat heart mitochondria free radical generation but does not prevent Ca2+-induced dysfunction. J Appi Physioi 102: 1793-1798, 2007.
106. Starnes JW, Beyer RE, Edington DW. Myocardial adaptations to endurance exercise in aged rats. Am J Physioi Heart Circ Physioi 245: H560-H566, 1983.
107. Starnes JW, Choilawala AM, Taylor RP, Nelson MJ, Delp MD. Myocardial heat shock protein 70 expression in young and old rats after identical exercise programs. J Gerontoi A Bioi Sci Med Sci 60: 963-969, 2005.
108. Starnes JW, Rumsey WL. Cardiac energetics and performance of exercised and food-restricted rats during aging. Am J Physioi Heart Circ Physioi 254: H599-H608, 1988.
109. Steel R, Doherty JP, Buzzard K, Clemons N, Hawkins CJ, Anderson RL. Hsp72 inhibits apoptosis upstream of the mitochondria and not through interactions with Apaf-1. J Bioi Chem 279: 51490-51499, 2004.
110. Sun B, Wang JH, Lv YY, Zhu SS, Yang J, Ma JZ. Proteomic adaptation to chronic high intensity swimming training in the rat heart. Comp Biochem Physioi D Genomics Proteomics 3: 108-117, 2008.
111. Suzuki K, Murtuza B, Sammut IA, Latif N, Jayaku-mar J, Smolenski RT, Kaneda Y, Sawa Y, Matsuda H, Yacoub MH. Heat shock protein 72 enhances manganese superoxide dismutase activity during myocardial ischemia-reperfusion injury, associated with mitochondrial protection and apoptosis reduction. Circulation 106: 270-276, 2002.
112. Taylor RP, Ciccolo JT, Starnes JW. Effect of exercise training on the ability of the rat heart to tolerate hydrogen peroxide. Cardiovasc Res 58: 575-581, 2003.
113. Taylor RP, Harris MB, Starnes JW. Acute exercise can improve cardioprotection without increasing heat shock protein content. Am J Physioi Heart Circ Physioi 276: H1098-H1102, 1999.
114. Taylor RP, Olsen ME, Starnes JW. Improved postischemic function following acute exercise is not mediated by nitric oxide synthase in the rat heart. Am J Physioi Heart Circ Physioi 292: H601-H607, 2007.
115. Vitadello M, Penzo D, Petronilli V, Michieli G, Gomirato S, Menabo R, Di Lisa F, Gorza L. Over-expression of the stress protein Grp94 reduces cardiomyocyte necrosis due to calcium overload and simulated ischemia. FASEB J 17: 923-925, 2003.
116. Vogt AM, Poolman M, Ackermann C, Yildiz M, Schoels W, Fell DA, Kubler W. Regulation of gly-colytic flux in ischemic preconditioning. A study employing metabolic control analysis. J Biol Chem 277: 24411-24419, 2002.
117. Webb A, Bond R, McLean P, Uppal R, Benjamin N, Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 101: 13683-13688, 2004.
118. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic car-dioprotection via manganese superoxide dismu-tase activation. J Exp Med 189: 1699-1706, 1999.
119. Yan Z, Lira VA, Greene NP. Exercise training-induced regulation of mitochondrial quality. Ex-erc Sport Sci Rev 40: 159-164, 2012.
120. Zhang LQ, Zhang XQ, Ng YC, Rothblum LI, Musch TI, Moore RL, Cheung JY. Sprint training normalizes Ca2+ transients and SR function in postinfarction rat myocytes. J Appi Physioi 89: 38-46, 2000.
121. Zhang PL, Lun M, Teng J, Huang J, Blasick TM, Yin L, Herrera GA, Cheung JY. Preinduced molecular chaperones in the endoplasmic reticulum protect cardiomyocytes from lethal injury. Ann Ciin Lab Sci 34: 449-457, 2004.
122. Zingman LV, Zhu Z, Sierra A, Stepniak E, Burnett CM, Maksymov G, Anderson ME, Coetzee WA, Hodgson-Zingman DM. Exercise-induced expression of cardiac ATP-sensitive potassium channels promotes action potential shortening and energy conservation. J Mol Cell Cardiol 51: 72-81, 2011.
123. Zoll J, N'Guessan B, Ribera F, Lampert E, Fortin D, Veksler V, Bigard X, Geny B, Lonsdorfer J, Ventura-Clapier R, Mettauer B. Preserved response of mitochondrial function to short-term endurance training in skeletal muscle of heart transplant recipients. J Am Coll Cardiol 42: 126-132, 2003.
124. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 70: 181-190, 2006.