Exercise protects cardiac mitochondria against ischemia-reperfusion injury

Medicine and Science in Sports and Exercise

Volumn 44, Issue 3, 2012, Pages 397-405

  Lee, Youngil ^a,b   Min, Kisuk ^a   Talbert, Erin E ^a   Kavazis, Andreas N ^c   Smuder, Ashley J ^a   Willis, Wayne T ^d   Powers, Scott K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

ANTIOXIDANTS; EXERCISE INDUCED CARDIOPROTECTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANALYSIS OF VARIANCE; ANIMAL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ENDURANCE; ENZYMOLOGY; HEART CONTRACTION; HEART MITOCHONDRION; MALE; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; PHYSIOLOGY; RANDOMIZATION; RAT; REPERFUSION INJURY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; MALE; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; OXIDATIVE STRESS; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 84857624825     PISSN: 01959131     EISSN: 15300315     Source Type: Journal    
DOI: 10.1249/MSS.0b013e318231c037     Document Type: Article

References (41)

1. Adlam VJ, Harrison JC, Porteous CM, et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J. 2005;19(9):1088-95. (Pubitemid 40946434)
2. Ascensao A, Magalhaes J, Soares JM, et al. Endurance training limits the functional alterations of rat heart mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardiol. 2006;109(2): 169-78.
3. Bowles DK, Starnes JW. Exercise training improves metabolic response after ischemia in isolated working rat heart. J Appl Physiol. 1994;76(4):1608-14. (Pubitemid 24125680)
4. Brown DA, Chicco AJ, Jew KN, et al. Cardioprotection afforded by chronic exercise is mediated by the sarcolemmal, and not the mitochondrial, isoform of the KATP channel in the rat. J Physiol. 2005;569(Pt 3):913-24. (Pubitemid 41830232)
5. Chen Q, Lesnefsky EJ. Depletion of cardiolipin and cytochrome c during ischemia increases hydrogen peroxide production from the electron transport chain. Free Radic Biol Med. 2006;40(6):976-82. (Pubitemid 43376007)
6. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ. Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion. J Pharmacol Exp Ther. 2006;319(3):1405-12.
7. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol. 2008;294(2):C460-6. (Pubitemid 351276913)
8. Chicco AJ, Johnson MS, Armstrong CJ, et al. Sex-specific and exercise-acquired cardioprotection is abolished by sarcolemmal KATP channel blockade in the rat heart. Am J Physiol Heart Circ Physiol. 2007;292(5):H2432-7. (Pubitemid 47084626)
9. Criswell D, Powers S, Dodd S, et al. High intensity traininginduced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc. 1993;25(10):1135-40. (Pubitemid 23298826)
10. 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. 2008;22(8):2862-71.
11. Gottlieb RA. Mitochondria: execution central. FEBS Lett. 2000; 482(1-2):6-12.
12. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res. 2004;61(3):372-85. (Pubitemid 38210145)
13. 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. 2003;34(7): 800-9. (Pubitemid 36316063)
14. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7(3):153-63.
15. Kavazis AN. Exercise preconditioning of the myocardium. Sports Med. 2009;39(11):923-35.
16. 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. 2009;297(1):H144-52.
17. Kavazis AN, McClung JM, Hood DA, Powers SK. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol Heart Circ Physiol. 2008;294(2):H928-35. (Pubitemid 351253305)
18. Kavazis AN, Talbert EE, Smuder AJ, Hudson MB, Nelson WB, Powers SK. Mechanical ventilation induces diaphragmatic mitochondrial dysfunction and increased oxidant production. Free Radic Biol Med. 2009;46(6):842-50.
19. Kumar D, Jugdutt BI. Apoptosis and oxidants in the heart. J Lab Clin Med. 2003;142(5):288-97. (Pubitemid 37487398)
20. Lennon SL, Quindry JC, French JP, Kim S, Mehta JL, Powers SK. Exercise and myocardial tolerance to ischaemia-reperfusion. Acta Physiol Scand. 2004;182(2):161-9. (Pubitemid 39371863)
21. Lennon SL, Quindry J, Hamilton KL, et al. Loss of exerciseinduced cardioprotection after cessation of exercise. J Appl Physiol. 2004;96(4):1299-305. (Pubitemid 38392664)
22. Lesnefsky EJ, Gudz TI, Migita CT, et al. Ischemic injury to mitochondrial electron transport in the aging heart: damage to the iron-sulfur protein subunit of electron transport complex III. Arch Biochem Biophys. 2001;385(1):117-28. (Pubitemid 32988989)
23. Lesnefsky EJ, Slabe TJ, Stoll MS, Minkler PE, Hoppel CL. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol. 2001;280(6):H2770-8.
24. Lloyd-Jones D, Adams RJ, Brown TM, et al. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation. 2010;121(7):e46-215.
25. 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 Physiol Heart Circ Physiol. 2006;290(4):H1549-57.
26. Messer JI, Jackman MR, Willis WT. Pyruvate and citric acid cycle carbon requirements in isolated skeletal muscle mitochondria. Am J Physiol Cell Physiol. 2004;286(3):C565-72. (Pubitemid 38292662)
27. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem. 1977;252(23):8731-9. (Pubitemid 8243644)
28. Powers SK, Criswell D, Lawler J, et al. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. Am J Physiol. 1993;265(6 Pt 2):H2094-8. (Pubitemid 24030440)
29. Powers SK, Demirel HA, Vincent HK, et al. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol. 1998;275(5 Pt 2):R1468-77.
30. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243-76.
31. Powers SK, Murlasits Z, Wu M, Kavazis AN. Ischemia- reperfusion-induced cardiac injury: a brief review. Med Sci Sports Exerc. 2007;39(9):1529-36. (Pubitemid 47360976)
32. Powers SK, Quindry JC, Kavazis AN. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med. 2008;44(2):193-201.
33. Quindry JC, Hamilton KL, French JP, et al. Exercise-induced HSP-72 elevation and cardioprotection against infarct and apoptosis. J Appl Physiol. 2007;103(3):1056-62. (Pubitemid 47358893)
34. Quindry JC, Schreiber L, Hosick P, Wrieden J, Irwin JM, Hoyt E. Mitochondrial KATP channel inhibition blunts arrhythmia protection in ischemic exercised hearts. Am J Physiol Heart Circ Physiol. 2010;299(1):H175-83.
35. 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. 2005;9(3):609-22. (Pubitemid 44151949)
36. Starnes JW, Barnes BD, Olsen ME. Exercise training decreases rat heart mitochondria free radical generation but does not prevent Ca2+-induced dysfunction. J Appl Physiol. 2007;102(5): 1793-8. (Pubitemid 46701946)
37. Szabadkai G, Duchen MR. Mitochondria: the hub of cellular Ca2+ signaling. Physiology (Bethesda). 2008;23:84-94.
38. Tompkins AJ, Burwell LS, Digerness SB, Zaragoza C, Holman WL, Brookes PS. Mitochondrial dysfunction in cardiac ischemia- reperfusion injury: ROS from complex I, without inhibition. Biochim Biophys Acta. 2006;1762(2):223-31. (Pubitemid 43006028)
39. Venditti P, Masullo P, Di Meo S. Effects of myocardial ischemia and reperfusion on mitochondrial function and susceptibility to oxidative stress. Cell Mol Life Sci. 2001;58(10): 1528-37. (Pubitemid 32964420)
40. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation. J Exp Med. 1999;189(11): 1699-706. (Pubitemid 29272686)
41. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem. 1997;253(2):162-8. (Pubitemid 27508167)