Both aerobic exercise and resveratrol supplementation attenuate doxorubicin-induced cardiac injury in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 2, 2013, Pages

  Dolinsky, Vernon W ^a,b   Rogan, Kyle J ^a   Sung, Miranda M ^a   Zordoky, Beshay N ^a   Haykowsky, Mark J ^a   Young, Martin E ^c   Jones, Lee W ^d   Dyck, Jason R B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d DUKE CANCER INSTITUTE   (United States)

Author keywords

Cardiotoxicity; Exercise; Oxidative stress; Resveratrol

Indexed keywords

4 HYDROXYNONENAL; ADENOSINE TRIPHOSPHATASE (CALCIUM); ATRIAL NATRIURETIC FACTOR; DOXORUBICIN; MITOFUSIN 1; MITOFUSIN 2; RESVERATROL; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE;

AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG EXPOSURE; ECHOCARDIOGRAPHY; ELECTRON TRANSPORT; FEMALE; HEART INJURY; HEART PROTECTION; IN VIVO STUDY; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREADMILL EXERCISE;

CARDIOTOXICITY; EXERCISE; OXIDATIVE STRESS; RESVERATROL;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIOXIDANTS; BIOLOGICAL MARKERS; BLOOD PRESSURE; BLOTTING, WESTERN; DIETARY SUPPLEMENTS; DOXORUBICIN; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FEMALE; GTP PHOSPHOHYDROLASES; HEART DISEASES; LIPID PEROXIDATION; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; PHYSICAL CONDITIONING, ANIMAL; STILBENES; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84880166032     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00044.2013     Document Type: Article

References (55)

1. Ascensao A, Ferreira R, Magalhaes J. Exercise-induced cardioprotection-biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int J Cardiol 117: 16-30, 2007.
2. Benard G, Karbowski M. Mitochondrial fusion and division: regulation and role in cell viability. Semin Cell Dev Biol 20: 365-374, 2009.
3. Berthiaume JM, Wallace KB. Persistent alterations to the gene expression profile of the heart subsequent to chronic Doxorubicin treatment. Cardiovasc Toxicol 7: 178-191, 2007.
4. Chen MB, Wu XY, Gu JH, Guo QT, Shen WX, Lu PH. Activation of AMP-activated protein kinase contributes to doxorubicin-induced cell death and apoptosis in cultured myocardial H9c2 cells. Cell Biochem Biophys 60: 311-322, 2011.
5. Chicco AJ, Hydock DS, Schneider CM, Hayward R. Low-intensity exercise training during doxorubicin treatment protects against cardiotoxicity. J Appl Physiol 100: 519-527, 2006.
6. Committee CCSsS. Canadian Cancer Statistics 2009. Toronto, Canada: Canadian Cancer Society, 2009.
7. Courneya KS, Segal RJ, Mackey JR, Gelmon K, Reid RD, Friedenreich CM, Ladha AB, Proulx C, Vallance JK, Lane K, Yasui Y, McKenzie DC. Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol 25: 4396-4404, 2007.
8. Danz ED, Skramsted J, Henry N, Bennett JA, Keller RS. Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radic Biol Med 46: 1589-1597, 2009.
9. Dolinsky VW, Chan AY, Robillard Frayne I, Light PE, Des Rosiers C, Dyck JR. Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB1. Circulation 119: 1643-1652, 2009.
10. Dolinsky VW, Dyck JR. Calorie restriction and resveratrol in cardiovascular health and disease. Biochim Biophys Acta 1812: 1477-1489, 2011.
11. Dolinsky VW, Jones KE, Sidhu RS, Haykowsky M, Czubryt MP, Gordon T, Dyck JR. Improvements in skeletal muscle strength and cardiac function induced by resveratrol contribute to enhanced exercise performance in rats. J Physiol 590: 2783-2799, 2012.
12. Dolinsky VW, Morton JS, Oka T, Robillard-Frayne I, Bagdan M, Lopaschuk GD, Des Rosiers C, Walsh K, Davidge ST, Dyck JR. Calorie restriction prevents hypertension and cardiac hypertrophy in the spontaneously hypertensive rat. Hypertension 56: 412-421, 2010.
13. Dolinsky VW, Rueda-Clausen CF, Morton JS, Davidge ST, Dyck JR. Continued postnatal administration of resveratrol prevents diet-induced metabolic syndrome in rat offspring born growth restricted. Diabetes 60: 2274-2284, 2011.
14. Duraj J, Bodo J, Sulikova M, Rauko P, Sedlak J. Diverse resveratrol sensitization to apoptosis induced by anticancer drugs in sensitive and resistant leukemia cells. Neoplasma 53: 384-392, 2006.
15. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments: what the cardiologist needs to know. Nat Rev Cardiol 7: 564-575, 2010.
16. Gratia S, Kay L, Potenza L, Seffouh A, Novel-Chate V, Schnebelen C, Sestili P, Schlattner U, Tokarska-Schlattner M. Inhibition of AMPK signalling by doxorubicin: at the crossroads of the cardiac responses to energetic, oxidative, and genotoxic stress. Cardiovasc Res 95: 290-299, 2012.
17. Gupta SC, Kannappan R, Reuter S, Kim JH, Aggarwal BB. Chemosensitization of tumors by resveratrol. Ann NY Acad Sci 1215: 150-160, 2011.
18. Haykowsky MJ, Liang Y, Pechter D, Jones LW, McAlister FA, Clark AM. A meta-analysis of the effect of exercise training on left ventricular remodeling in heart failure patients: the benefit depends on the type of training performed. J Am Coll Cardiol 49: 2329-2336, 2007.
19. Haykowsky MJ, Mackey JR, Thompson RB, Jones LW, Paterson DI. Adjuvant trastuzumab induces ventricular remodeling despite aerobic exercise training. Clin Cancer Res 15: 4963-4967, 2009.
20. Hequet O, Le QH, Moullet I, Pauli E, Salles G, Espinouse D, Dumontet C, Thieblemont C, Arnaud P, Antal D, Bouafia F, Coiffier B. Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. J Clin Oncol 22: 1864-1871, 2004.
21. Hydock DS, Lien CY, Jensen BT, Schneider CM, Hayward R. Exercise preconditioning provides long-term protection against early chronic doxorubicin cardiotoxicity. Integr Cancer Ther 10: 47-57, 2011.
22. Jones LW, Eves ND, Courneya KS, Chiu BK, Baracos VE, Hanson J, Johnson L, Mackey JR. Effects of exercise training on antitumor efficacy of doxorubicin in MDA-MB-231 breast cancer xenografts. Clin Cancer Res 11: 6695-6698, 2005.
23. Jones LW, Liang Y, Pituskin EN, Battaglini CL, Scott JM, Hornsby WE, Haykowsky M. Effect of exercise training on peak oxygen consumption in patients with cancer: a meta-analysis. Oncologist 16: 112-120, 2011.
24. 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 299: H1515-H1524, 2010.
25. 2+ ATPase function is increased by aerobic interval training. Eur J Cardiovasc Prev Rehabil 15: 145-148, 2008.
26. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122, 2006.
27. Mattson MP. Roles of the lipid peroxidation product 4-hydroxynonenal in obesity, the metabolic syndrome, and associated vascular and neurodegenerative disorders. Exp Gerontol 44: 625-633, 2009.
28. Meinardi MT, van Veldhuisen DJ, Gietema JA, Dolsma WV, Boomsma F, van den Berg MP, Volkers C, Haaksma J, de Vries EG, Sleijfer DT, van der Graaf WT. Prospective evaluation of early cardiac damage induced by epirubicin-containing adjuvant chemotherapy and locoregional radiotherapy in breast cancer patients. J Clin Oncol 19: 2746-2753, 2001.
29. Migrino RQ, Aggarwal D, Konorev E, Brahmbhatt T, Bright M, Kalyanaraman B. Early detection of doxorubicin cardiomyopathy using two-dimensional strain echocardiography. Ultrasound Med Biol 34: 208-214, 2008.
30. Neilan TG, Jassal DS, Scully MF, Chen G, Deflandre C, McAllister H, Kay E, Austin SC, Halpern EF, Harmey JH, Fitzgerald DJ. Iloprost attenuates doxorubicin-induced cardiac injury in a murine model without compromising tumour suppression. Eur Heart J 27: 1251-1256, 2006.
31. O'Connor CM, Whellan DJ, Lee KL, Keteyian SJ, Cooper LS, Ellis SJ, Leifer ES, Kraus WE, Kitzman DW, Blumenthal JA, Rendall DS, Miller NH, Fleg JL, Schulman KA, McKelvie RS, Zannad F, Pina IL. Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. J Am Med Assoc 301: 1439-1450, 2009.
32. Olson RD, Gambliel HA, Vestal RE, Shadle SE, Charlier HA Jr, Cusack BJ. Doxorubicin cardiac dysfunction: effects on calcium regulatory proteins, sarcoplasmic reticulum, and triiodothyronine. Cardiovasc Toxicol 5: 269-283, 2005.
33. Perez EA, Suman VJ, Davidson NE, Kaufman PA, Martino S, Dakhil SR, Ingle JN, Rodeheffer RJ, Gersh BJ, Jaffe AS. Effect of doxorubicin plus cyclophosphamide on left ventricular ejection fraction in patients with breast cancer in the North Central Cancer Treatment Group N9831 Intergroup Adjuvant Trial. J Clin Oncol 22: 3700-3704, 2004.
34. Perez EA, Suman VJ, Davidson NE, Sledge GW, Kaufman PA, Hudis CA, Martino S, Gralow JR, Dakhil SR, Ingle JN, Winer EP, Gelmon KA, Gersh BJ, Jaffe AS, Rodeheffer RJ. Cardiac safety analysis of doxorubicin and cyclophosphamide followed by paclitaxel with or without trastuzumab in the North Central Cancer Treatment Group N9831 adjuvant breast cancer trial. J Clin Oncol 26: 1231-1238, 2008.
35. Rimbaud S, Ruiz M, Piquereau J, Mateo P, Fortin D, Veksler V, Garnier A, Ventura-Clapier R. Resveratrol improves survival, hemodynamics and energetics in a rat model of hypertension leading to heart failure. PLoS One 6: e26391, 2011.
36. Rius C, Abu-Taha M, Hermenegildo C, Piqueras L, Cerda-Nicolas JM, Issekutz AC, Estan L, Cortijo J, Morcillo EJ, Orallo F, Sanz MJ. Trans-but not cis-resveratrol impairs angiotensin-II-mediated vascular inflammation through inhibition of NF-kappaB activation and peroxisome proliferator-activated receptor-gamma upregulation. J Immunol 185: 3718-3727, 2010.
37. Scott JM, Khakoo A, Mackey JR, Haykowsky MJ, Douglas PS, Jones LW. Modulation of anthracycline-induced cardiotoxicity by aerobic exercise in breast cancer: current evidence and underlying mechanisms. Circulation 124: 642-650, 2011.
38. Shadfar S, Couch ME, McKinney KA, Weinstein LJ, Yin X, Rodriguez JE, Guttridge DC, Willis M. Oral resveratrol therapy inhibits cancer-induced skeletal muscle and cardiac atrophy in vivo. Nutr Cancer 63: 749-762, 2011.
39. Simunek T, Sterba M, Popelova O, Adamcova M, Hrdina R, Gersl V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 61: 154-171, 2009.
40. Swain SM, Whaley FS, Gerber MC, Weisberg S, York M, Spicer D, Jones SE, Wadler S, Desai A, Vogel C, Speyer J, Mittelman A, Reddy S, Pendergrass K, Velez-Garcia E, Ewer MS, Bianchine JR, Gams RA. Cardioprotection with dexrazoxane for doxorubicin-containing therapy in advanced breast cancer. J Clin Oncol 15: 1318-1332, 1997.
41. Swank AM, Horton J, Fleg JL, Fonarow GC, Keteyian S, Goldberg L, Wolfel G, Handberg EM, Bensimhon D, Illiou MC, Vest M, Ewald G, Blackburn G, Leifer E, Cooper L, Kraus WE. Modest Increase in Peak VO2 is Related to Better Clinical Outcomes in Chronic Heart Failure Patients: Results from Heart Failure and a Controlled Trial to Investigate Outcomes of Exercise Training (HF-ACTION). Circ Heart Fail 5: 579-585, 2012.
42. Tan-Chiu E, Yothers G, Romond E, Geyer CE Jr, Ewer M, Keefe D, Shannon RP, Swain SM, Brown A, Fehrenbacher L, Vogel VG, Seay TE, Rastogi P, Mamounas EP, Wolmark N, Bryant J. Assessment of cardiac dysfunction in a randomized trial comparing doxorubicin and cyclophosphamide followed by paclitaxel, with or without trastuzumab as adjuvant therapy in node-positive, human epidermal growth factor receptor 2-overexpressing breast cancer: NSABP B-31. J Clin Oncol 23: 7811-7819, 2005.
43. Tatlidede E, Sehirli O, Velioglu-Ogunc A, Cetinel S, Yegen BC, Yarat A, Suleymanoglu S, Sener G. Resveratrol treatment protects against doxorubicin-induced cardiotoxicity by alleviating oxidative damage. Free Radic Res 43: 195-205, 2009.
44. Thandapilly SJ, Wojciechowski P, Behbahani J, Louis XL, Yu L, Juric D, Kopilas MA, Anderson HD, Netticadan T. Resveratrol prevents the development of pathological cardiac hypertrophy and contractile dysfunction in the SHR without lowering blood pressure. Am J Hypertens 23: 192-196, 2010.
45. Toklu HZ, Sehirli O, Ersahin M, Suleymanoglu S, Yiginer O, Emekli-Alturfan E, Yarat A, Yegen BC, Sener G. Resveratrol improves cardiovascular function and reduces oxidative organ damage in the renal, cardiovascular and cerebral tissues of two-kidney, one-clip hypertensive rats. J Pharm Pharmacol 62: 1784-1793, 2010.
46. Trudeau M, Charbonneau F, Gelmon K, Laing K, Latreille J, Mackey J, McLeod D, Pritchard K, Provencher L, Verma S. Selection of adjuvant chemotherapy for treatment of node-positive breast cancer. Lancet Oncol 6: 886-898, 2005.
47. van Dalen EC, Caron HN, Dickinson HO, Kremer LC. Cardioprotective interventions for cancer patients receiving anthracyclines. Cochrane Database of Syst Rev CD003917, 2005.
48. Von Hoff DD, Layard MW, Basa P, Davis HL Jr, Von Hoff AL, Rozencweig M, Muggia FM. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 91: 710-717, 1979.
49. Wang TJ, Evans JC, Benjamin EJ, Levy D, LeRoy EC, Vasan RS. Natural history of asymptomatic left ventricular systolic dysfunction in the community. Circulation 108: 977-982, 2003.
50. Weiss RB. The anthracyclines: will we ever find a better doxorubicin? Semin Oncol 19: 670-686, 1992.
51. Whellan DJ, Nigam A, Arnold M, Starr AZ, Hill J, Fletcher G, Ellis SJ, Cooper L, Onwuanyi A, Chandler B, Keteyian SJ, Ewald G, Kao A, Gheorghiade M. Benefit of exercise therapy for systolic heart failure in relation to disease severity and etiology-findings from the Heart Failure and A Controlled Trial Investigating Outcomes of Exercise Training study. Am Heart J 162: 1003-1010, 2011.
52. Whitesall SE, Hoff JB, Vollmer AP, D'Alecy LG. Comparison of simultaneous measurement of mouse systolic arterial blood pressure by radiotelemetry and tail-cuff methods. Am J Physiol Heart Circ Physiol 286: H2408-H2415, 2004.
53. Wonders KY, Hydock DS, Schneider CM, Hayward R. Acute exercise protects against doxorubicin cardiotoxicity. Integr Cancer Ther 7: 147-154, 2008.
54. Yi X, Bekeredjian R, DeFilippis NJ, Siddiquee Z, Fernandez E, Shohet RV. Transcriptional analysis of doxorubicin-induced cardiotoxicity. Am J Physiol Heart Circ Physiol 290: H1098-H1102, 2006.
55. Zhang C, Feng Y, Qu S, Wei X, Zhu H, Luo Q, Liu M, Chen G, Xiao X. Resveratrol attenuates doxorubicin-induced cardiomyocyte apoptosis in mice through SIRT1-mediated deacetylation of p53. Cardiovasc Res 90: 538-545, 2011.