Interleukin-6 mediates exercise preconditioning against myocardial ischemia reperfusion injury

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 11, 2015, Pages H1423-H1433

  McGinnis, Graham Ripley ^a   Ballmann, Christopher ^a   Peters, Bridget ^a   Nanayakkara, Gayani ^b   Roberts, Michael ^a   Amin, Rajesh ^b   Quindry, John C ^a  

^a AUBURN UNIVERSITY   (United States)

^b AUBURN UNIVERSITY   (United States)

Author keywords

Cardioprotection; Myocardial infarction; Myokine

Indexed keywords

CYCLOOXYGENASE 2; INTERLEUKIN 6; STAT3 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL STRESS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSOLIC FRACTION; EXERCISE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HEART ARRHYTHMIA; HEART PROTECTION; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REPERFUSION INJURY; TREADMILL EXERCISE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; GENETICS; HEART INFARCTION PREVENTION; HEART MUSCLE; KINESIOTHERAPY; METABOLISM; MYOCARDIAL REPERFUSION INJURY; NECROSIS; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CYCLOOXYGENASE 2; EXERCISE THERAPY; INTERLEUKIN-6; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NECROSIS; NITRIC OXIDE SYNTHASE TYPE II; PHYSICAL EXERTION; RECEPTORS, INTERLEUKIN-6; STAT3 TRANSCRIPTION FACTOR;

EID: 84930858136     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00850.2014     Document Type: Article

References (60)

1. Adser H, Wojtaszewski JF, Jakobsen AH, Kiilerich K, Hidalgo J, Pilegaard H. Interleukin-6 modifies mRNA expression in mouse skeletal muscle. Acta Physiol (Oxf) 202: 165–173, 2011.
2. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H. Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19: 786–788, 2005.
3. Bolli R, Stein AB, Guo Y, Wang OL, Rokosh G, Dawn B, Molkentin JD, Sanganalmath SK, Zhu Y, Xuan YT. A murine model of inducible, cardiac-specific deletion of STAT3: its use to determine the role of STAT3 in the upregulation of cardioprotective proteins by ischemic preconditioning. J Mol Cell Cardiol 50: 589–597, 2011.
4. Botker HE, Kharbanda R, Schmidt MR, Bottcher M, Kaltoft AK, Terkelsen CJ, Munk K, Andersen NH, Hansen TM, Trautner S, Lassen JF, Christiansen EH, Krusell LR, Kristensen SD, Thuesen L, Nielsen SS, Rehling M, Sorensen HT, Redington AN, Nielsen TT. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 375: 727–734, 2010.
5. 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 569: 913–924, 2005.
6. Buja LM. Myocardial ischemia and reperfusion injury. Cardiovasc Pathol 14: 170–175, 2005.
7. Buja LM, Weerasinghe P. Unresolved issues in myocardial reperfusion injury. Cardiovasc Pathol 19: 29–35, 2010.
8. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 47: 2277–2282, 2006.
9. Dawn B, Xuan YT, Guo Y, Rezazadeh A, Stein AB, Hunt G, Wu WJ, Tan W, Bolli R. IL-6 plays an obligatory role in late preconditioning via JAK-STAT signaling and upregulation of iNOS and COX-2. Cardiovasc Res 64: 61–71, 2004.
10. 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.
11. Dickson EW, Hogrefe CP, Ludwig PS, Ackermann LW, Stoll LL, Denning GM. Exercise enhances myocardial ischemic tolerance via an opioid receptor-dependent mechanism. Am J Physiol Heart Circ Physiol 294: H402–H408, 2008.
12. Fahmi A, Smart N, Punn A, Jabr R, Marber M, Heads R. p42/p44- MAPK and PI3K are sufficient for IL-6 family cytokines/gp130 to signal to hypertrophy and survival in cardiomyocytes in the absence of JAK/ STAT activation. Cell Signal 25: 898–909, 2012.
13. Fischer P, Hilfiker-Kleiner D. Survival pathways in hypertrophy and heart failure: the gp130-STAT3 axis. Basic Res Cardiol 102: 279–297, 2007.
14. Frasier CR, Moore RL, Brown DA. Exercise-induced cardiac preconditioning: how exercise protects your achy-breaky heart. J Appl Physiol 111: 905–915, 2011.
15. 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.
16. Gottlieb RA, Engler RL. Apoptosis in myocardial ischemia-reperfusion. Ann NY Acad Sci 874: 412–426, 1999.
17. Gray SR, Clifford M, Lancaster R, Leggate M, Davies M, Nimmo MA. The response of circulating levels of the interleukin-6/interleukin-6 receptor complex to exercise in young men. Cytokine 47: 98–102, 2009.
18. Gray SR, Ratkevicius A, Wackerhage H, Coats P, Nimmo MA. The effect of interleukin-6 and the interleukin-6 receptor on glucose transport in mouse skeletal muscle. Exp Physiol 94: 899–905, 2009.
19. Gustafsson AB, Gottlieb RA.: Eat your heart out: Role of autophagy in myocardial ischemia/reperfusion. Autophagy 4: 416–421, 2008.
20. Gustafsson AB, Gottlieb RA. Recycle or die: the role of autophagy in cardioprotection. J Mol Cell Cardiol 44: 654–661, 2008.
21. Gwechenberger M, Mendoza LH, Youker KA, Frangogiannis NG, Smith CW, Michael LH, Entman ML. Cardiac myocytes produce interleukin-6 in culture and in viable border zone of reperfused infarctions. Circulation 99: 546–551, 1999.
22. 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.
23. 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.
24. Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13: 251–262, 2012.
25. Herlitz J, Bengtson A, Hjalmarson A, Karlson BW. Morbidity during five years after myocardial infarction and its relation to infarct size. Clin Cardiol 11: 672–677, 1988.
26. Hiscock N, Chan MH, Bisucci T, Darby IA, Febbraio MA. Skeletal myocytes are a source of interleukin-6 mRNA expression and protein release during contraction: evidence of fiber type specificity. FASEB J 18: 992–994, 2004.
27. Kavazis AN. Exercise preconditioning of the myocardium. Sports Med 39: 923–935, 2009.
28. Keller P, Penkowa M, Keller C, Steensberg A, Fischer CP, Giralt M, Hidalgo J, Pedersen BK. Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J 19: 1181–1183, 2005.
29. Kharbanda RK, Nielsen TT, Redington AN. Translation of remote ischaemic preconditioning into clinical practice. Lancet 374: 1557–1565, 2009.
30. Lai NC, Gao MH, Tang E, Tang R, Guo T, Dalton ND, Deng A, Tang T. Pressure overload-induced cardiac remodeling and dysfunction in the absence of interleukin 6 in mice. Lab Invest 92: 1518–1526, 2012.
31. Lauritzen HP, Brandauer J, Schjerling P, Koh HJ, Treebak JT, Hirshman MF, Galbo H, Goodyear LJ. Contraction and AICAR stimulate IL-6 vesicle depletion from skeletal muscle fibers in vivo. Diabetes 62: 3081–3092, 2013.
32. Leggate M, Nowell MA, Jones SA, Nimmo MA. The response of interleukin-6 and soluble interleukin-6 receptor isoforms following intermittent high intensity and continuous moderate intensity cycling. Cell Stress Chap 15: 827–833, 2010.
33. 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 96: 1299–1305, 2004.
34. 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.
35. Lin H, Sinner MF, Brody JA, Arking DE, Lunetta KL, Rienstra M, Lubitz SA, Magnani JW, Sotoodehnia N, McKnight B, McManus DD, Boerwinkle E, Psaty BM, Rotter JI, Bis JC, Gibbs RA, Muzny D, Kovar CL, Morrison AC, Gupta M, Folsom AR, Kaab S, Heckbert SR, Alonso A, Ellinor PT, Benjamin EJ, Group CAFW. Targeted sequencing in candidate genes for atrial fibrillation: the Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Targeted Sequencing Study. Heart Rhythm 11: 452–457, 2014.
36. MacDonald C, Wojtaszewski JF, Pedersen BK, Kiens B, Richter EA. Interleukin-6 release from human skeletal muscle during exercise: relation to AMPK activity. J Appl Physiol 95: 2273–2277, 2003.
37. Matsushita K, Iwanaga S, Oda T, Kimura K, Shimada M, Sano M, Umezawa A, Hata J, Ogawa S. Interleukin-6/soluble interleukin-6 receptor complex reduces infarct size via inhibiting myocardial apoptosis. Lab Invest 85: 1210–1223, 2005.
38. Maxeiner H, Mufti S, Krehbiehl N, Dulfer F, Helmig S, Schneider J, Boning A, Matejec R, Weigand MA, Schluter KD, Wenzel S. Interleukin- 6 contributes to the paracrine effects of cardiospheres cultured from human, murine and rat hearts. J Cell Physiol 229: 1681–1689, 2014.
39. Miller L, McGinnis G, Peters B, Ballmann C, Nanayakkara G, Amin R, Quindry J. Involvement of the delta opioid receptor in exerciseinduced cardioprotection. Exp Physiol In press.
40. 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.
41. Miller TD, Christian TF, Hopfenspirger MR, Hodge DO, Gersh BJ, Gibbons RJ. Infarct size after acute myocardial infarction measured by quantitative tomographic 99mTc sestamibi imaging predicts subsequent mortality. Circulation 92: 334–341, 1995.
42. Moldoveanu AI, Shephard RJ, Shek PN. Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol 89: 1499–1504, 2000.
43. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124–1136, 1986.
44. Ono T, Maekawa K, Watanabe S, Oka H, Kuboki T. Muscle contraction accelerates IL-6 mRNA expression in the rat masseter muscle. Arch Oral Biol 52: 479–486, 2007.
45. Pedersen BK, Akerstrom TC, Nielsen AR, Fischer CP. Role of myokines in exercise and metabolism. J Appl Physiol 103: 1093–1098, 2007.
46. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88: 1379–1406, 2008.
47. Powers SK, Quindry JC, Kavazis AN. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 44: 193–201, 2008.
48. Powers SK, Sollanek KJ, Wiggs MP, Demirel HA, Smuder AJ. Exercise-induced improvements in myocardial antioxidant capacity: the antioxidant players and cardioprotection. Free Radic Res 48: 43–51, 2014.
49. 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 40: 416–425, 2005.
50. 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 60: 181–186, 2010.
51. 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.
52. Quindry JC, Miller L, McGinnis G, Kliszczewicz B, Irwin JM, Landram M, Urbiztondo Z, Nanayakkara G, Amin R. Ischemia reperfusion injury, KATP channels, and exercise-induced cardioprotection against apoptosis. J Appl Physiol 113: 498–506, 2012.
53. 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 299: H175–H183, 2010.
54. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Rosamond WD, Sorlie PD, Stafford RS, Turan TN, Turner MB, Wong ND, Wylie-Rosett J. Heart disease and stroke statistics--2011 update: a report from the American Heart Association. Circulation 123: e18–e209, 2011.
55. Schulman D, Latchman DS, Yellon DM. Effect of aging on the ability of preconditioning to protect rat hearts from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 281: H1630–H1636, 2001.
56. Smart N, Mojet MH, Latchman DS, Marber MS, Duchen MR, Heads RJ. IL-6 induces PI 3-kinase and nitric oxide-dependent protection and preserves mitochondrial function in cardiomyocytes. Cardiovasc Res 69: 164–177, 2006.
57. Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund Pedersen B. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin- 6. J Physiol 529: 237–242, 2000.
58. Szabo-Fresnais N, Lefebvre F, Germain A, Fischmeister R, Pomerance M. A new regulation of IL-6 production in adult cardiomyocytes by beta-adrenergic and IL-1 beta receptors and induction of cellular hypertrophy by IL-6 trans-signalling. Cell Signal 22: 1143–1152, 2010.
59. Trenerry MK, Carey KA, Ward AC, Cameron-Smith D. STAT3 signaling is activated in human skeletal muscle following acute resistance exercise. J Appl Physiol 102: 1483–1489, 2007.
60. Ullum H, Haahr PM, Diamant M, Palmo J, Halkjaer-Kristensen J, Pedersen BK. Bicycle exercise enhances plasma IL-6 but does not change IL-1 alpha, IL-1 beta, IL-6, or TNF-alpha pre-mRNA in BMNC. J Appl Physiol 77: 93–97, 1994.