Exercise-induced improvements in myocardial antioxidant capacity: the antioxidant players and cardioprotection

References

• Powers SK, Quindry JC, Kavazis AN. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 2008;44:193–201.
   PubMed Web of Science ®Google Scholar
• Kavazis AN. Exercise preconditioning of the myocardium. Sports Med 2009;39:923–935.
   PubMed Web of Science ®Google Scholar
• Frasier CR, Moore RL, Brown DA. Exercise-induced cardiac preconditioning: how exercise protects your achy-breaky heart. J Appl Physiol 2011;111:905–915.
   PubMed Web of Science ®Google Scholar
• Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008;88:1243–1276.
   PubMed Web of Science ®Google Scholar
• Murphy MP. Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications. Antioxid Redox Signal 2012;16: 476–495.
   PubMed Web of Science ®Google Scholar
• Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M. Glutathione peroxidase family – an evolutionary overview. FEBS J 2008;275:3959–3970.
   PubMed Web of Science ®Google Scholar
• Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, MacCoss MJ, et al. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009;119:2789–2797.
   PubMed Web of Science ®Google Scholar
• Berndt C, Lillig CH, Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol 2007;292:H1227–H1236.
   PubMed Web of Science ®Google Scholar
• Yin F, Sancheti H, Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 2012;17:1714–1727.
   PubMed Web of Science ®Google Scholar
• Wood ZA, Schroder E, Robin Harris J, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 2003;28:32–40.
   PubMed Web of Science ®Google Scholar
• Brinkmann C, Brixius K. Peroxiredoxins and sports: new insights on the antioxidative defense. J Physiol Sci 2013;63:1–5.
   PubMed Web of Science ®Google Scholar
• Hall A, Nelson K, Poole LB, Karplus PA. Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid Redox Signal 2011;15:795–815.
   PubMed Web of Science ®Google Scholar
• Lash LH. Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem Biol Interact 2006;163:54–67.
   PubMed Web of Science ®Google Scholar
• Ferrandez MD, De la Fuente M. Effects of age, sex and physical exercise on the phagocytic process of murine peritoneal macrophages. Acta Physiol Scand 1999;166:47–53.
   PubMedGoogle Scholar
• Rupp H. Differential effect of physical exercise routines on ventricular myosin and peripheral catecholamine stores in normotensive and spontaneously hypertensive rats. Circ Res 1989;65:370–377.
   PubMed Web of Science ®Google Scholar
• Powers SK, Murlasits Z, Wu M, Kavazis AN. Ischemia- reperfusion-induced cardiac injury: a brief review. Med Sci Sports Exerc 2007;39:1529–1536.
   PubMed Web of Science ®Google Scholar
• Bowles DK, Starnes JW. Exercise training improves metabolic response after ischemia in isolated working rat heart. J Appl Physiol 1994;76:1608–1614.
   PubMed Web of Science ®Google Scholar
• Demirel HA, Powers SK, Caillaud C, Coombes JS, Naito H, Fletcher LA, et al. Exercise training reduces myocardial lipid peroxidation following short-term ischemia-reperfusion. Med Sci Sports Exerc 1998;30:1211–1216.
   PubMed Web of Science ®Google Scholar
• 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 2001;91:2205–2212.
   PubMed Web of Science ®Google Scholar
• 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 Physiol 2005;569:913–924.
   PubMed Web of Science ®Google Scholar
• 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 2001;281: H1346–H1352.
   PubMed Web of Science ®Google Scholar
• 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 2004;37:1360–1368.
   PubMed Web of Science ®Google Scholar
• 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;34:800–809.
   PubMed Web of Science ®Google Scholar
• Hoshida S, Yamashita N, Otsu K, Hori M. Repeated physiologic stresses provide persistent cardioprotection against ischemia-reperfusion injury in rats. J Am Coll Cardiol 2002; 40:826–831.
   PubMed Web of Science ®Google Scholar
• Lennon SL, Quindry J, Hamilton KL, French J, Staib J, Mehta JL, Powers SK. Loss of exercise-induced cardioprotection after cessation of exercise. J Appl Physiol 2004;96: 1299–1305.
   PubMed Web of Science ®Google Scholar
• Lennon SL, Quindry JC, French JP, Kim S, Mehta JL, Powers SK. Exercise and myocardial tolerance to ischaemia-reperfusion. Acta Physiol Scand 2004;182:161–169.
   PubMedGoogle Scholar
• Lennon SL, Quindry JC, Hamilton KL, French JP, Hughes J, Mehta JL, Powers SK. Elevated MnSOD is not required for exercise-induced cardioprotection against myocardial stunning. Am J Physiol Heart Circ Physiol 2004;287: H975–H980.
   PubMed Web of Science ®Google Scholar
• Libonati JR. Exercise training improves left ventricular isovolumic relaxation. Med Sci Sports Exerc 2000;32: 1399–1405.
   PubMed Web of Science ®Google Scholar
• Libonati JR, Gaughan JP, Hefner CA, Gow A, Paolone AM, Houser SR. Reduced ischemia and reperfusion injury following exercise training. Med Sci Sports Exerc 1997;29: 509–516.
   PubMed Web of Science ®Google Scholar
• Libonati JR, Kendrick ZV, Houser SR. Sprint training improves postischemic, left ventricular diastolic performance. J Appl Physiol 2005;99:2121–2127.
   PubMed Web of Science ®Google Scholar
• Miller LE, Hosick PA, Wrieden J, Hoyt E, Quindry JC. Evaluation of arrhythmia scoring systems and exercise- induced cardioprotection. Med Sci Sports Exerc 2012;44: 435–441.
   PubMed Web of Science ®Google Scholar
• Quindry JC, French J, Hamilton KL, Lee Y, Selsby J, Powers SK. Cyclooxygenase-2 is unaltered by exercise in the young and old heart. Med Sci Sports Exerc 2006;38:S416.
   Web of Science ®Google Scholar
• Quindry JC, French J, Hamilton KL, Lee Y, Selsby J, Powers S. Exercise does not increase cyclooxygenase-2 myocardial levels in young or senescent hearts. J Physiol Sci 2010;60:181–186.
   PubMed Web of Science ®Google Scholar
• Quindry JC, Hamilton KL, French JP, Lee Y, Murlasits Z, Tumer N, Powers SK. Exercise-induced HSP-72 elevation and cardioprotection against infarct and apoptosis. J Appl Physiol 2007;103:1056–1062.
   PubMed Web of Science ®Google Scholar
• Quindry JC, Miller L, McGinnis G, Kliszczewicz B, Irwin JM, Landram M, et al. Ischemia reperfusion injury, KATP channels, and exercise-induced cardioprotection against apoptosis. J Appl Physiol 2012;113:498–506.
   PubMed Web of Science ®Google Scholar
• 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:H175–H183.
   PubMed Web of Science ®Google Scholar
• 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; 102:1793–1798.
   PubMed Web of Science ®Google Scholar
• Starnes JW, Taylor RP, Ciccolo JT. Habitual low-intensity exercise does not protect against myocardial dysfunction after ischemia in rats. Eur J Cardiovasc Prev Rehabil 2005;12: 169–174.
   PubMedGoogle Scholar
• Starnes JW, Taylor RP, Park Y. Exercise improves postischemic function in aging hearts. Am J Physiol Heart Circ Physiol 2003;285:H347–H351.
   PubMed Web of Science ®Google Scholar
• Zhang LQ, Zhang XQ, Ng YC, Rothblum LI, Musch TI, Moore RL, Cheung JY. Sprint training normalizes Ca(2+) transients and SR function in postinfarction rat myocytes. J Appl Physiol 2000;89:38–46.
   PubMed Web of Science ®Google Scholar
• 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;189:1699–1706.
   PubMed Web of Science ®Google Scholar
• 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;22:2862–2871.
   PubMed Web of Science ®Google Scholar
• Powers SK, Demirel HA, Vincent HK, Coombes JS, Naito H, Hamilton KL, et al. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol 1998;275:R1468–R1477.
   PubMedGoogle Scholar
• Ascensao A, Ferreira R, Magalhaes J. Exercise-induced cardioprotection – biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int J Cardiol 2006;117:16–30.
   PubMed Web of Science ®Google Scholar
• 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: H928–H935.
   PubMed Web of Science ®Google Scholar
• 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 2012;44:397–405.
   PubMed Web of Science ®Google Scholar
• Quindry J, French J, Hamilton K, Lee Y, Mehta JL, Powers S. Exercise training provides cardioprotection against ischemia-reperfusion induced apoptosis in young and old animals. Exp Gerontol 2005;40:416–425.
   PubMed Web of Science ®Google Scholar
• 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 1998;30:2281–2289.
   PubMed Web of Science ®Google Scholar
• 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 2006; 290:H128–H136.
   PubMed Web of Science ®Google Scholar
• 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 1993;265:H2094–H2098.
   PubMed Web of Science ®Google Scholar
• Husain K, Somani SM. Response of cardiac antioxidant system to alcohol and exercise training in the rat. Alcohol 1997;14:301–307.
   PubMed Web of Science ®Google Scholar
• Ramires PR, Ji LL. Glutathione supplementation and training increases myocardial resistance to ischemia-reperfusion in vivo. Am J Physiol Heart Circ Physiol 2001;281: H679–H688.
   PubMed Web of Science ®Google Scholar
• Moran M, Delgado J, Gonzalez B, Manso R, Megias A. Responses of rat myocardial antioxidant defences and heat shock protein HSP72 induced by 12 and 24-week treadmill training. Acta Physiol Scand 2004;180:157–166.
   PubMedGoogle Scholar
• Kakarla P, Vadluri G, Reddy KS, Leeuwenburgh C. Vulnerability of the mid aged rat myocardium to the age-induced oxidative stress: influence of exercise training on antioxidant defense system. Free Radic Res 2005;39: 1211–1217.
   PubMed Web of Science ®Google Scholar
• Ferraresso RL, de Oliveira R, Macedo DV, Nunes LA, Brenzikofer R, Damas D, Hohl R. Interaction between overtraining and the interindividual variability may (not) trigger muscle oxidative stress and cardiomyocyte apoptosis in rats. Oxid Med Cell Longev 2012;2012:935483.
   PubMed Web of Science ®Google Scholar
• Ascensao A, Ferreira R, Oliveira PJ, Magalhaes J. Effects of endurance training and acute Doxorubicin treatment on rat heart mitochondrial alterations induced by in vitro anoxia-reoxygenation. Cardiovasc Toxicol 2006;6:159–172.
   PubMed Web of Science ®Google Scholar
• Harris MB, Starnes JW. Effects of body temperature during exercise training on myocardial adaptations. Am J Physiol Heart Circ Physiol 2001;280:H2271–H2280.
   PubMed Web of Science ®Google Scholar
• Hong H, Johnson P. Antioxidant enzyme activities and lipid peroxidation levels in exercised and hypertensive rat tissues. Int J Biochem Cell Biol 1995;27:923–931.
   PubMed Web of Science ®Google Scholar
• Pinho CA, Tromm CB, Tavares AM, Silva LA, Silveira PC, Souza CT, et al. Effects of different physical training protocols on ventricular oxidative stress. Life Sci 2012;90:553–559.
   PubMed Web of Science ®Google Scholar
• Atalay M, Seene T, Hanninen O, Sen CK. Skeletal muscle and heart antioxidant defences in response to sprint training. Acta Physiol Scand 1996;158:129–134.
   PubMedGoogle Scholar
• Husain K, Hazelrigg SR. Oxidative injury due to chronic nitric oxide synthase inhibition in rat: effect of regular exercise on the heart. Biochim Biophys Acta 2002;1587:75–82.
   PubMed Web of Science ®Google Scholar
• Lawler JM, Kwak HB, Kim JH, Suk MH. Exercise training inducibility of MnSOD protein expression and activity is retained while reducing prooxidant signaling in the heart of senescent rats. Am J Physiol Regul Integr Comp Physiol 2009;296:R1496–R1502.
   PubMed Web of Science ®Google Scholar
• Somani SM, Frank S, Rybak LP. Responses of antioxidant system to acute and trained exercise in rat heart subcellular fractions. Pharmacol Biochem Behav 1995;51:627–634.
   PubMed Web of Science ®Google Scholar
• 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 Physiol Heart Circ Physiol 2007;292:H601–H607.
   PubMed Web of Science ®Google Scholar
• Kavazis AN, Smuder AJ, Min K, Tumer N, Powers SK. Short-term exercise training protects against doxorubicin-induced cardiac mitochondrial damage independent of HSP72. Am J Physiol Heart Circ Physiol 2010;299:H1515–H1524.
   PubMed Web of Science ®Google Scholar
• Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. Faseb J 2004;18:1150–1152.
   PubMed Web of Science ®Google Scholar
• Gounder SS, Kannan S, Devadoss D, Miller CJ, Whitehead KS, Odelberg SJ, et al. Impaired transcriptional activity of Nrf2 in age-related myocardial oxidative stress is reversible by moderate exercise training. PLoS One 2012; 7:e45697.
   PubMed Web of Science ®Google Scholar
• Laher I, Beam J, Botta A, Barendregt R, Sulistyoningrum D, Devlin A, et al. Short-term exercise worsens cardiac oxidative stress and fibrosis in 8-month-old db/db mice by depleting cardiac glutathione. Free Radic Res 2013;47:44–54.
   PubMed Web of Science ®Google Scholar
• Chicco AJ, Schneider CM, Hayward R. Exercise training attenuates acute doxorubicin-induced cardiac dysfunction. J Cardiovasc Pharmacol 2006;47:182–189.
   PubMed Web of Science ®Google Scholar
• Chicco AJ, Hydock DS, Schneider CM, Hayward R. Low-intensity exercise training during doxorubicin treatment protects against cardiotoxicity. J Appl Physiol 2006;100:519–527.
   PubMed Web of Science ®Google Scholar
• Brown DA, Lynch JM, Armstrong CJ, Caruso NM, Ehlers LB, Johnson MS, Moore RL. Susceptibility of the heart to ischaemia-reperfusion injury and exercise-induced cardioprotection are sex-dependent in the rat. J Physiol 2005;564: 619–630.
   PubMed Web of Science ®Google Scholar
• Ji LL, Mitchell EW. Effects of Adriamycin on heart mitochondrial function in rested and exercised rats. Biochem Pharmacol 1994;47:877–885.
   PubMed Web of Science ®Google Scholar
• Lew H, Quintanilha A. Effects of endurance training and exercise on tissue antioxidative capacity and acetaminophen detoxification. Eur J Drug Metab Pharmacokinet 1991; 16:59–68.
   PubMed Web of Science ®Google Scholar
• Taylor RP, Ciccolo JT, Starnes JW. Effect of exercise training on the ability of the rat heart to tolerate hydrogen peroxide. Cardiovasc Res 2003;58:575–581.
   PubMed Web of Science ®Google Scholar
• Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, et al. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am J Physiol Heart Circ Physiol 2005;289:H722–H731.
   PubMed Web of Science ®Google Scholar
• McCommis KS, McGee AM, Laughlin MH, Bowles DK, Baines CP. Hypercholesterolemia increases mitochondrial oxidative stress and enhances the MPT response in the porcine myocardium: beneficial effects of chronic exercise. Am J Physiol Regul Integr Comp Physiol 2011;301: R1250–R1258.
   PubMed Web of Science ®Google Scholar
• Fisher-Wellman KH, Mattox TA, Thayne K, Katunga LA, La Favor JD, Neufer PD, et al. Novel role for thioredoxin reductase-2 in mitochondrial redox adaptations to obesogenic diet and exercise in the heart and skeletal muscle. J Physiol 2013; 591:3471–3486.
   PubMed Web of Science ®Google Scholar
• Richters L, Lange N, Renner R, Treiber N, Ghanem A, Tiemann K, et al. Exercise-induced adaptations of cardiac redox homeostasis and remodeling in heterozygous SOD2-knockout. J Appl Physiol 2011;111:1431–1440.
   PubMed Web of Science ®Google Scholar
• 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:H144–H152.
   PubMed Web of Science ®Google Scholar
• Ohkuwa T, Sato Y, Naoi M. Glutathione status and reactive oxygen generation in tissues of young and old exercised rats. Acta Physiol Scand 1997;159:237–244.
   PubMedGoogle Scholar
• Yamamoto T, Ohkuwa T, Itoh H, Sato Y, Naoi M. Effect of gender differences and voluntary exercise on antioxidant capacity in rats. Comp Biochem Physiol C Toxicol Pharmacol 2002;132:437–444.
   PubMed Web of Science ®Google Scholar
• Kakarla P, Kesireddy S, Christiaan L. Exercise training with ageing protects against ethanol induced myocardial glutathione homeostasis. Free Radic Res 2008;42:428–434.
   PubMed Web of Science ®Google Scholar
• Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, et al. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 2000;89:21–28.
   PubMed Web of Science ®Google Scholar
• Leeuwenburgh C, Hollander J, Leichtweis S, Griffiths M, Gore M, Ji LL. Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol 1997;272:R363–R369.
   PubMed Web of Science ®Google Scholar
• Husain K, Somani SM. Interaction of exercise and adenosine receptor agonist and antagonist on rat heart antioxidant defense system. Mol Cell Biochem 2005;270:209–214.
   PubMed Web of Science ®Google Scholar
• Bejma J, Ramires P, Ji LL. Free radical generation and oxidative stress with ageing and exercise: differential effects in the myocardium and liver. Acta Physiol Scand 2000;169:343–351.
   PubMedGoogle Scholar
• Sen CK, Atalay M, Hanninen O. Exercise-induced oxidative stress: glutathione supplementation and deficiency. J Appl Physiol 1994;77:2177–2187.
   PubMed Web of Science ®Google Scholar
• Ji LL. Antioxidant enzyme response to exercise and aging. Med Sci Sports Exerc 1993;25:225–231.
   PubMed Web of Science ®Google Scholar
• Frasier CR, Sloan RC, Bostian PA, Gonzon MD, Kurowicki J, Lopresto SJ, et al. Short-term exercise preserves myocardial glutathione and decreases arrhythmias after thiol oxidation and ischemia in isolated rat hearts. J Appl Physiol 2011; 111:1751–1759.
   PubMed Web of Science ®Google Scholar
• Khanna S, Atalay M, Laaksonen DE, Gul M, Roy S, Sen CK. Alpha-lipoic acid supplementation: tissue glutathione homeostasis at rest and after exercise. J Appl Physiol 1999;86: 1191–1196.
   PubMed Web of Science ®Google Scholar
• Gul M, Demircan B, Taysi S, Oztasan N, Gumustekin K, Siktar E, et al. Effects of endurance training and acute exhaustive exercise on antioxidant defense mechanisms in rat heart. Comp Biochem Physiol A Mol Integr Physiol 2006;143:239–245.
   PubMed Web of Science ®Google Scholar