Exercise-induced protection against reperfusion arrhythmia involves stabilization of mitochondrial energetics

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 10, 2016, Pages H1360-H1370

  Alleman, Rick J ^a   Tsang, Alvin M ^a   Ryan, Terence E ^a   Patteson, Daniel J ^a   McClung, Joseph M ^a   Spangenburg, Espen E ^a   Shaikh, Saame Raza ^a   Darrell Neufer, P ^a   Brown, David A ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Arrhythmia; Cardioprotection; Exercise; Membrane potential; Mitochondria

Indexed keywords

GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; THIOREDOXIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIARRHYTHMIC ACTIVITY; ARTICLE; CONTROLLED STUDY; EXERCISE; HEART FIBRILLATION; HEART PROTECTION; HEART VENTRICLE ARRHYTHMIA; HOMEOSTASIS; IN VITRO STUDY; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; TACHYCARDIA; ACTION POTENTIAL; ANIMAL; ARRHYTHMIAS, CARDIAC; CARDIAC MUSCLE CELL; DISEASE MODEL; ENERGY METABOLISM; HEART MITOCHONDRION; HEART RATE; ISOLATED HEART; KINESIOTHERAPY; METABOLISM; MYOCARDIAL REPERFUSION INJURY; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROCEDURES; RUNNING; TIME FACTOR;

ACTION POTENTIALS; ANIMALS; ARRHYTHMIAS, CARDIAC; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; EXERCISE THERAPY; GLUTATHIONE; HEART RATE; ISOLATED HEART PREPARATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PHYSICAL EXERTION; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RUNNING; TIME FACTORS;

EID: 84983792626     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00858.2015     Document Type: Article

References (73)

1. Ahsan MK, Lekli I, Ray D, Yodoi J, Das DK. Redox regulation of cell survival by the thioredoxin superfamily: an implication of redox gene therapy in the heart. Antioxid Redox Signal 11: 2741–2758, 2009.
2. Aiello EA, Jabr RI, Cole WC. Arrhythmia and delayed recovery of cardiac action potential during reperfusion after ischemia. Role of oxygen radical-induced no-reflow phenomenon. Circ Res 77: 153–162, 1995.
3. Akar FG, Aon MA, Tomaselli GF, O’Rourke B. The mitochondrial origin of postischemic arrhythmias. J Clin Invest 115: 3527–3535, 2005.
4. Akita Y, Otani H, Matsuhisa S, Kyoi S, Enoki C, Hattori R, Imamura H, Kamihata H, Kimura Y, Iwasaka T. Exercise-induced activation of cardiac sympathetic nerve triggers cardioprotection via redox-sensitive activation of eNOS and upregulation of iNOS. Am J Physiol Heart Circ Physiol 292: H2051–H2059, 2007.
5. Alleman RJ, Katunga LA, Nelson MA, Brown DA, Anderson EJ. The “Goldilocks Zone” from a redox perspective: adaptive vs. deleterious responses to oxidative stress in striated muscle. Front Physiol 5: 358, 2014.
6. Aon MA, Cortassa S, Maack C, O’Rourke B. Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. J Biol Chem 282: 21889–21900, 2007.
7. 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.
8. Ascensao A, Ferreira R, Magalhaes J. Exercise-induced cardioprotec-tion: biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int J Cardiol 117: 16–30, 2007.
9. 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 Cardiol 109: 169–178, 2006.
10. Bolli R, Jeroudi MO, Patel BS, DuBose CM, Lai EK, Roberts R, McCay PB. Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog. Proc Natl Acad Sci USA 86: 4695–4699, 1989.
11. Bowles DK, Farrar RP, Starnes JW. Exercise training improves cardiac function after ischemia in the isolated, working rat heart. Am J Physiol Heart Circ Physiol 263: H804–H809, 1992.
12. 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 79: 141–149, 2008.
13. Brown DA, Aon MA, Frasier CR, Sloan RC, Maloney AH, Anderson EJ, O’Rourke B. Cardiac arrhythmias induced by glutathione oxidation can be inhibited by preventing mitochondrial depolarization. J Mol Cell Cardiol 48: 673–679, 2010.
14. 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 K ATP channel in the rat. J Physiol 569: 913–924, 2005.
15. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL, Moore RL. Short-term treadmill running in the rat: what kind of stressor is it? J Appl Physiol 103: 1979–1985, 2007.
16. Ceconi C, Curello S, Cargnoni A, Ferrari R, Albertini A, Visioli O. The role of glutathione status in the protection against ischaemic and reperfusion damage: effects of N-acetyl cysteine. J Mol Cell Cardiol 20: 5–13, 1988.
17. Chouchani ET, Pell VR, Gaude E, Aksentijevic D, Sundier SY, Robb EL, Logan A, Nadtochiy SM, Ord EN, Smith AC, Eyassu F, Shirley R, Hu CH, Dare AJ, James AM, Rogatti S, Hartley RC, Eaton S, Costa AS, Brookes PS, Davidson SM, Duchen MR, Saeb-Parsy K, Shattock MJ, Robinson AJ, Work LM, Frezza C, Krieg T, Murphy MP. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515: 431–435, 2014.
18. Cortassa S, O’Rourke B, Aon MA. Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim Biophys Acta 1837: 287–295, 2014.
19. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341: 233–249, 1999.
20. Curtis MJ, Hancox JC, Farkas A, Wainwright CL, Stables CL, Saint DA, Clements-Jewery H, Lambiase PD, Billman GE, Janse MJ, Pugsley MK, Ng GA, Roden DM, Camm AJ, Walker MJ. The Lambeth Conventions (II): guidelines for the study of animal and human ventricular and supraventricular arrhythmias. Pharmacol Ther 139: 213–248, 2013.
21. 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.
22. Dou Y, Arlock P, Arner A. Blebbistatin specifically inhibits actin-myosin interaction in mouse cardiac muscle. Am J Physiol Cell Physiol 293: C1148–C1153, 2007.
23. Du G, Mouithys-Mickalad A, Sluse FE. Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic Biol Med 25: 1066–1074, 1998.
24. Du G, Willet K, Mouithys-Mickalad A, Sluse-Goffart CM, Droy-Lefaix MT, Sluse FE. EGb 761 protects liver mitochondria against injury induced by in vitro anoxia/reoxygenation. Free Radic Biol Med 27: 596–604, 1999.
25. Ferdaoussi M, Dai X, Jensen MV, Wang R, Peterson BS, Huang C, Ilkayeva O, Smith N, Miller N, Hajmrle C, Spigelman AF, Wright RC, Plummer G, Suzuki K, Mackay JP, van de Bunt M, Gloyn AL, Ryan TE, Norquay LD, Brosnan MJ, Trimmer JK, Rolph TP, Kibbey RG, Manning Fox JE, Colmers WF, Shirihai OS, Neufer PD, Yeh ET, Newgard CB, MacDonald PE. Isocitrate-to-SENP1 signaling amplifies insulin secretion and rescues dysfunctional beta cells. J Clin Invest 125: 3847–3860, 2015.
26. Fishman GI, Chugh SS, Dimarco JP, Albert CM, Anderson ME, Bonow RO, Buxton AE, Chen PS, Estes M, Jouven X, Kwong R, Lathrop DA, Mascette AM, Nerbonne JM, O’Rourke B, Page RL, Roden DM, Rosenbaum DS, Sotoodehnia N, Trayanova NA, Zheng ZJ. Sudden cardiac death prediction and prevention: report from a Na-tional Heart, Lung, and Blood Institute and Heart Rhythm Society Work-shop. Circulation 122: 2335–2348, 2010.
27. Frasier CR, Moore RL, Brown DA. Exercise-induced cardiac precon-ditioning: how exercise protects your achy-breaky heart. J Appl Physiol 111: 905–915, 2011.
28. Frasier CR, Moukdar F, Patel HD, Sloan RC, Stewart LM, Alleman RJ, La Favor JD, Brown DA. Redox-dependent increases in glutathione reductase and exercise preconditioning: role of NADPH oxidase and mitochondria. Cardiovasc Res 98: 47–55, 2013.
29. Frasier CR, Sloan RC, Bostian PA, Gonzon MD, Kurowicki J, Lo-presto 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.
30. Ganitkevich V, Reil S, Schwethelm B, Schroeter T, Benndorf K. Dynamic responses of single cardiomyocytes to graded ischemia studied by oxygen clamp in on-chip picochambers. Circ Res 99: 165–171, 2006.
31. Giustarini D, Dalle-Donne I, Milzani A, Fanti P, Rossi R. Analysis of GSH and GSSG after derivatization with N-ethylmaleimide. Nat Protoc 8: 1660–1669, 2013.
32. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics Committee, Stroke Statistics Subcommit-tee. Executive summary: heart disease and stroke statistics—2014 update: a report from the American Heart Association. Circulation 129: 399–410, 2014.
33. 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.
34. Hull SS Jr, Vanoli E, Adamson PB, Verrier RL, Foreman RD, Schwartz PJ. Exercise training confers anticipatory protection from sudden death during acute myocardial ischemia. Circulation 89: 548–552, 1994.
35. Husain K, Somani SM. Response of cardiac antioxidant system to alcohol and exercise training in the rat. Alcohol 14: 301–307, 1997.
36. Jew KN, Moore RL. Exercise training alters an anoxia-induced, gliben-clamide-sensitive current in rat ventricular cardiocytes. J Appl Physiol 92: 1473–1479, 2002.
37. Judge S, Jang YM, Smith A, Selman C, Phillips T, Speakman JR, Hagen T, Leeuwenburgh C. Exercise by lifelong voluntary wheel run-ning reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am J Physiol Regul Integr Comp Physiol 289: R1564–R1572, 2005.
38. Kand’ar R, Zakova P, Lotkova H, Kucera O, Cervinkova Z. Deter-mination of reduced and oxidized glutathione in biological samples using liquid chromatography with fluorimetric detection. J Pharm Biomed Anal 43: 1382–1387, 2007.
39. 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.
40. King N, Korolchuk S, McGivan JD, Suleiman MS. A new method of quantifying glutathione levels in freshly isolated single superfused rat cardiomyocytes. J Pharmacol Toxicol Methods 50: 215–222, 2004.
41. 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.
42. 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.
43. 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 Regul Integr Comp Physiol 272: R363–R369, 1997.
44. 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 287: H975–H980, 2004.
45. Lyon AR, Joudrey PJ, Jin D, Nass RD, Aon MA, O’Rourke B, Akar FG. Optical imaging of mitochondrial function uncovers actively propa-gating waves of mitochondrial membrane potential collapse across intact heart. J Mol Cell Cardiol 49: 565–575, 2010.
46. Manning A, Bernier M, Crome R, Little S, Hearse D. Reperfusion-induced arrhythmias: a study of the role of xanthine oxidase-derived free radicals in the rat heart. J Mol Cell Cardiol 20: 35–45, 1988.
47. Maranzana E, Barbero G, Falasca AI, Lenaz G, Genova ML. Mito-chondrial respiratory supercomplex association limits production of reac-tive oxygen species from complex I. Antioxid Redox Signal 19: 1469-1480, 2013.
48. Matsumoto-Ida M, Akao M, Takeda T, Kato M, Kita T. Real-time 2-photon imaging of mitochondrial function in perfused rat hearts sub-jected to ischemia/reperfusion. Circulation 114: 1497–1503, 2006.
49. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1–13, 2009.
50. Nichols M, Townsend N, Scarborough P, Rayner M. Cardiovascular disease in Europe 2014: epidemiological update. Eur Heart J 35: 2950-2959, 2014.
51. Nieminen T, Scirica BM, Pegler JR, Tavares C, Pagotto VP, Kanas AF, Sobrado MF, Nearing BD, Umez-Eronini AA, Morrow DA, Belardinelli L, Verrier RL. Relation of T-wave alternans to mortality and nonsustained ventricular tachycardia in patients with non-ST-segment elevation acute coronary syndrome from the MERLIN-TIMI 36 trial of ranolazine vs. placebo. Am J Cardiol 114: 17–23, 2014.
52. Nishida K, Otsu K. Autophagy during cardiac remodeling. J Mol Cell Cardiol. In press.
53. O’Rourke B, Ramza BM, Marban E. Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science 265: 962–966, 1994.
54. Orr AL, Ashok D, Sarantos MR, Shi T, Hughes RE, Brand MD. Inhibitors of ROS production by the ubiquinone-binding site of mitochon-drial complex I identified by chemical screening. Free Radic Biol Med 65: 1047–1059, 2013.
55. Qin F, Siwik DA, Lancel S, Zhang J, Kuster GM, Luptak I, Wang L, Tong X, Kang YJ, Cohen RA, Colucci WS. Hydrogen peroxide-medi-ated SERCA cysteine 674 oxidation contributes to impaired cardiac myocyte relaxation in senescent mouse heart. J Am Heart Assoc 2: e000184, 2013.
56. 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 103: 1056–1062, 2007.
57. Quindry JC, Miller L, McGinnis G, Kliszczewicz B, Irwin JM, Lan-dram M, Urbiztondo Z, Nanayakkara G, Amin R. Ischemia reperfusion injury, K ATP channels, and exercise-induced cardioprotection against ap-optosis. J Appl Physiol 113: 498–506, 2012.
58. Quindry JC, Schreiber L, Hosick P, Wrieden J, Irwin JM, Hoyt E. Mitochondrial K ATP channel inhibition blunts arrhythmia protection in ischemic exercised hearts. Am J Physiol Heart Circ Physiol 299: H175-H183, 2010.
59. Richters L, Lange N, Renner R, Treiber N, Ghanem A, Tiemann K, Scharffetter-Kochanek K, Bloch W, Brixius K. Exercise-induced adap-tations of cardiac redox homeostasis and remodeling in heterozygous SOD2-knockout mice. J Appl Physiol 111: 1431–1440, 2011.
60. Sanchez G, Escobar M, Pedrozo Z, Macho P, Domenech R, Hartel S, Hidalgo C, Donoso P. Exercise and tachycardia increase NADPH oxidase and ryanodine receptor-2 activity: possible role in cardioprotection. Car-diovasc Res 77: 380–386, 2008.
61. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191–1212, 2001.
62. Sloan RC, Moukdar F, Frasier CR, Patel HD, Bostian PA, Lust RM, Brown DA. Mitochondrial permeability transition in the diabetic heart: contributions of thiol redox state and mitochondrial calcium to augmented reperfusion injury. J Mol Cell Cardiol 52: 1009–1018, 2012.
63. Slodzinski MK, Aon MA, O’Rourke B. Glutathione oxidation as a trigger of mitochondrial depolarization and oscillation in intact hearts. J Mol Cell Cardiol 45: 650–660, 2008.
64. 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 292: H601–H607, 2007.
65. Tritto I, Duilio C, Santoro G, Elia PP, Cirillo P, De Simone C, Chiariello M, Ambrosio G. A short burst of oxygen radicals at reflow induces sustained release of oxidized glutathione from postischemic hearts. Free Radic Biol Med 24: 290–297, 1998.
66. Wachtell K, Okin PM, Olsen MH, Dahlof B, Devereux RB, Ibsen H, Kjeldsen SE, Lindholm LH, Nieminen MS, Thygesen K. Regression of electrocardiographic left ventricular hypertrophy during antihypertensive therapy and reduction in sudden cardiac death: the LIFE Study. Circula-tion 116: 700–705, 2007.
67. Willet K, Detry O, Sluse FE. Resistance of isolated pulmonary mito-chondria during in vitro anoxia/reoxygenation. Biochim Biophys Acta 1460: 346–352, 2000.
68. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic cardioprotection via manganese super-oxide dismutase activation. J Exp Med 189: 1699–1706, 1999.
69. Yan XS, Ma JH, Zhang PH. Modulation of K ATP currents in rat ventricular myocytes by hypoxia and a redox reaction. Acta Pharmacol Sin 30: 1399–1414, 2009.
70. Yu L, Fink BD, Herlein JA, Sivitz WI. Mitochondrial function in diabetes: novel methodology and new insight. Diabetes 62: 1833–1842, 2013.
71. Zhou L, Cortassa S, Wei AC, Aon MA, Winslow RL, O’Rourke B. Modeling cardiac action potential shortening driven by oxidative stress-induced mitochondrial oscillations in guinea pig cardiomyocytes. Biophys J 97: 1843–1852, 2009.
72. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accom-panying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192: 1001–1014, 2000.
73. Zweier JL, Flaherty JT, Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84: 1404–1407, 1987