Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway

Free Radical Biology and Medicine

Volumn 46, Issue 12, 2009, Pages 1589-1597

  Brookins Danz, Elizabeth D ^a   Skramsted, Jeremy ^a   Henry, Nicholas ^a   Bennett, James A ^a   Keller, Rebecca S ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Cardiotoxicity; Doxorubicin; Free radicals; Mitochondria; Resveratrol; ROS; Sirt1

Indexed keywords

DOXORUBICIN; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; RESVERATROL; SIRTUIN 1;

ANIMAL CELL; ARTICLE; CARDIOTOXICITY; CELL SURVIVAL; DRUG EFFECT; HEART MUSCLE CELL; HEART PROTECTION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; CARDIOTONIC AGENTS; CELL DEATH; CELLS, CULTURED; DOXORUBICIN; DRUG EVALUATION, PRECLINICAL; HEART FAILURE; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; NIACINAMIDE; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; SIRTUINS; STILBENES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 67349234999     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.03.011     Document Type: Article

References (61)

1. Aggarwal B.B., Bhardwaj A., Aggarwal R.S., Seeram N.P., Shishodia S., and Takada Y. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res. 24 (2004) 2783-2840
2. Akao M., Ohler A., O'Rourke B., and Marban E. Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circ. Res. 88 (2001) 1267-1275
3. Alcendor R.R., Gao S., Zhai P., Zablocki D., Holle E., Yu X., Tian B., Wagner T., Vatner S.F., and Sadoshima J. Sirt1 regulates aging and resistance to oxidative stress in the heart. Circ. Res. 100 (2007) 1512-1521
4. Alcendor R.R., Kirshenbaum L.A., Imai S., Vatner S.F., and Sadoshima J. Silent information regulator 2alpha, a longevity factor and class III histone deacetylase, is an essential endogenous apoptosis inhibitor in cardiac myocytes. Circ. Res. 95 (2004) 971-980
5. Assem M., Teyssier J.R., Benderitter M., Terrand J., Laubriet A., Javouhey A., David M., and Rochette L. Pattern of superoxide dismutase enzymatic activity and RNA changes in rat heart ventricles after myocardial infarction. Am. J. Pathol. 151 (1997) 549-555
6. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., and Sinclair D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444 (2006) 337-342
7. Beauchamp C., and Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44 (1971) 276-287
8. Bhat K.P., Lantvit D., Christov K., Mehta R.G., Moon R.C., and Pezzuto J.M. Estrogenic and antiestrogenic properties of resveratrol in mammary tumor models. Cancer Res. 61 (2001) 7456-7463
9. Bhat K.P., and Pezzuto J.M. Resveratrol exhibits cytostatic and antiestrogenic properties with human endometrial adenocarcinoma (Ishikawa) cells. Cancer Res. 61 (2001) 6137-6144
10. Bitterman K.J., Anderson R.M., Cohen H.Y., Latorre-Esteves M., and Sinclair D.A. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J. Biol. Chem. 277 (2002) 45099-45107
11. Blander G., and Guarente L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73 (2004) 417-435
12. Brachmann C.B., Sherman J.M., Devine S.E., Cameron E.E., Pillus L., and Boeke J.D. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 9 (1995) 2888-2902
13. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., Tran H., Ross S.E., Mostoslavsky R., Cohen H.Y., Hu L.S., Cheng H.L., Jedrychowski M.P., Gygi S.P., Sinclair D.A., Alt F.W., and Greenberg M.E. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004) 2011-2015
14. Cao Z., and Li Y. Potent induction of cellular antioxidants and phase 2 enzymes by resveratrol in cardiomyocytes: protection against oxidative and electrophilic injury. Eur. J. Pharmacol. 489 (2004) 39-48
15. Chen C.J., Yu W., Fu Y.C., Wang X., Li J.L., and Wang W. Resveratrol protects cardiomyocytes from hypoxia-induced apoptosis through the SIRT1-FoxO1 pathway. Biochem. Biophys. Res. Commun. 378 (2009) 389-393
16. Das D.K., Sato M., Ray P.S., Maulik G., Engelman R.M., Bertelli A.A., and Bertelli A. Cardioprotection of red wine: role of polyphenolic antioxidants. Drugs Exp. Clin. Res. 25 (1999) 115-120
17. Das S., Cordis G.A., Maulik N., and Das D.K. Pharmacological preconditioning with resveratrol: role of CREB-dependent Bcl-2 signaling via adenosine A3 receptor activation. Am. J. Physiol, Heart Circ. Physiol. 288 (2005) 328-335
18. Das S., Falchi M., Bertelli A., Maulik N., and Das D.K. Attenuation of ischemia/reperfusion injury in rats by the anti-inflammatory action of resveratrol. Arzneimittelforschung 56 (2006) 700-706
19. Dasgupta B., and Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 7217-7222
20. den Hartog G.J., Haenen G.R., Boven E., van der Vijgh W.J., and Bast A. Lecithinized copper,zinc-superoxide dismutase as a protector against doxorubicin-induced cardiotoxicity in mice. Toxicol. Appl. Pharmacol. 194 (2004) 180-188
21. Doroshow J.H. Effect of anthracycline antibiotics on oxygen radical formation in rat heart. Cancer Res. 43 (1983) 460-472
22. Doroshow J.H., Locker G.Y., and Myers C.E. Enzymatic defenses of the mouse heart against reactive oxygen metabolites: alterations produced by doxorubicin. J. Clin. Invest. 65 (1980) 128-135
23. Dudley J., Das S., Mukherjee S., and Das D.K. Resveratrol, a unique phytoalexin present in red wine, delivers either survival signal or death signal to the ischemic myocardium depending on dose. J. Nutr. Biochem. (2008)
24. Goh S.S., Woodman O.L., Pepe S., Cao A.H., Qin C., and Ritchie R.H. The red wine antioxidant resveratrol prevents cardiomyocyte injury following ischemia-reperfusion via multiple sites and mechanisms. Antioxid. Redox Signal. 9 (2007) 101-113
25. Hasinoff B.B., Schnabl K.L., Marusak R.A., Patel D., and Huebner E. Dexrazoxane (ICRF-187) protects cardiac myocytes against doxorubicin by preventing damage to mitochondria. Cardiovasc. Toxicol. 3 (2003) 89-99
26. Herrick-Davis K., Grinde E., and Mazurkiewicz J.E. Biochemical and biophysical characterization of serotonin 5-HT2C receptor homodimers on the plasma membrane of living cells. Biochemistry 43 (2004) 13963-13971
27. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., and Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425 (2003) 191-196
28. Hung L.M., Su M.J., and Chen J.K. Resveratrol protects myocardial ischemia-reperfusion injury through both NO-dependent and NO-independent mechanisms. Free Radic. Biol. Med. 36 (2004) 774-781
29. Hung L.M., Su M.J., Chu W.K., Chiao C.W., Chan W.F., and Chen J.K. The protective effect of resveratrols on ischaemia-reperfusion injuries of rat hearts is correlated with antioxidant efficacy. Br. J. Pharmacol. 135 (2002) 1627-1633
30. Iwase H., Robin E., Guzy R.D., Mungai P.T., Vanden Hoek T.L., Chandel N.S., Levraut J., and Schumacker P.T. Nitric oxide during ischemia attenuates oxidant stress and cell death during ischemia and reperfusion in cardiomyocytes. Free Radic. Biol. Med. 43 (2007) 590-599
31. Jang M., Cai L., Udeani G.O., Slowing K.V., Thomas C.F., Beecher C.W., Fong H.H., Farnsworth N.R., Kinghorn A.D., Mehta R.G., Moon R.C., and Pezzuto J.M. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275 (1997) 218-220
32. Juan M.E., Vinardell M.P., and Planas J.M. The daily oral administration of high doses of trans-resveratrol to rats for 28 days is not harmful. J. Nutr. 132 (2002) 257-260
33. Kim D.S., Woo E.R., Chae S.W., Ha K.C., Lee G.H., Hong S.T., Kwon D.Y., Kim M.S., Jung Y.K., Kim H.M., Kim H.K., Kim H.R., and Chae H.J. Plantainoside D protects adriamycin-induced apoptosis in H9c2 cardiac muscle cells via the inhibition of ROS generation and NF-kappaB activation. Life Sci. 80 (2007) 314-323
34. Konorev E.A., Kennedy M.C., and Kalyanaraman B. Cell-permeable superoxide dismutase and glutathione peroxidase mimetics afford superior protection against doxorubicin-induced cardiotoxicity: the role of reactive oxygen and nitrogen intermediates. Arch. Biochem. Biophys. 368 (1999) 421-428
35. Kops G.J., Dansen T.B., Polderman P.E., Saarloos I., Wirtz K.W., Coffer P.J., Huang T.T., Bos J.L., Medema R.H., and Burgering B.M. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419 (2002) 316-321
36. Kotamraju S., Konorev E.A., Joseph J., and Kalyanaraman B. Doxorubicin-induced apoptosis in endothelial cells and cardiomyocytes is ameliorated by nitrone spin traps and ebselen: role of reactive oxygen and nitrogen species. J. Biol. Chem. 275 (2000) 33585-33592
37. L'Ecuyer T., Sanjeev S., Thomas R., Novak R., Das L., Campbell W., and Heide R.V. DNA damage is an early event in doxorubicin-induced cardiac myocyte death. Am. J. Physiol, Heart Circ. Physiol. 291 (2006) 1273-1280
38. 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., and Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127 (2006) 1109-1122
39. Lansford R., Bearman G., and Fraser S.E. Resolution of multiple green fluorescent protein color variants and dyes using two-photon microscopy and imaging spectroscopy. J. Biomed. Opt. 6 (2001) 311-318
40. Li K., Sung R.Y., Huang W.Z., Yang M., Pong N.H., Lee S.M., Chan W.Y., Zhao H., To M.Y., Fok T.F., Li C.K., Wong Y.O., and Ng P.C. Thrombopoietin protects against in vitro and in vivo cardiotoxicity induced by doxorubicin. Circulation 113 (2006) 2211-2220
41. Lipshultz S.E., Colan S.D., Gelber R.D., Perez-Atayde A.R., Sallan S.E., and Sanders S.P. Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N. Engl. J. Med. 324 (1991) 808-815
42. Mathur A., Hong Y., Kemp B.K., Barrientos A.A., and Erusalimsky J.D. Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovasc. Res. 46 (2000) 126-138
43. Ni Y.G., Wang N., Cao D.J., Sachan N., Morris D.J., Gerard R.D., Kuro O.M., Rothermel B.A., and Hill J.A. FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 20517-20522
44. Olson H.M., and Capen C.C. Subacute cardiotoxicity of adriamycin in the rat: biochemical and ultrastructural investigations. Lab. Invest. 37 (1977) 386-394
45. Olson R.D., and Mushlin P.S. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 4 (1990) 3076-3086
46. Orallo F., Alvarez E., Camina M., Leiro J.M., Gomez E., and Fernandez P. The possible implication of trans-resveratrol in the cardioprotective effects of long-term moderate wine consumption. Mol. Pharmacol. 61 (2002) 294-302
47. Reiter R.J., Tan D.X., Qi W., Manchester L.C., Karbownik M., and Calvo J.R. Pharmacology and physiology of melatonin in the reduction of oxidative stress in vivo. Biol. Signals Recept. 9 (2000) 160-171
48. Rezk Y.A., Balulad S.S., Keller R.S., and Bennett J.A. Use of resveratrol to improve the effectiveness of cisplatin and doxorubicin: study in human gynecologic cancer cell lines and in rodent heart. Am. J. Obstet. Gynecol. 194 (2006) 23-26
49. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., and Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 (2005) 113-118
50. Ross R.S., Pham C., Shai S.Y., Goldhaber J.I., Fenczik C., Glembotski C.C., Ginsberg M.H., and Loftus J.C. Beta1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ. Res. 82 (1998) 1160-1172
51. Salvatorelli E., Guarnieri S., Menna P., Liberi G., Calafiore A.M., Mariggio M.A., Mordente A., Gianni L., and Minotti G. Defective one- or two-electron reduction of the anticancer anthracycline epirubicin in human heart: relative importance of vesicular sequestration and impaired efficiency of electron addition. J. Biol. Chem. 281 (2006) 10990-11001
52. Sarvazyan N. Visualization of doxorubicin-induced oxidative stress in isolated cardiac myocytes. Am. J. Physiol. 271 (1996) 2079-2085
53. Sato M., Maulik N., and Das D.K. Cardioprotection with alcohol: role of both alcohol and polyphenolic antioxidants. Ann. N.Y. Acad. Sci. 957 (2002) 122-135
54. Shan K., Lincoff A.M., and Young J.B. Anthracycline-induced cardiotoxicity. Ann. Intern. Med. 125 (1996) 47-58
55. Tao R., Karliner J.S., Simonis U., Zheng J., Zhang J., Honbo N., and Alano C.C. Pyrroloquinoline quinone preserves mitochondrial function and prevents oxidative injury in adult rat cardiac myocytes. Biochem. Biophys. Res. Commun. 363 (2007) 257-262
56. Weiss R.B. The anthracyclines: will we ever find a better doxorubicin?. Semin. Oncol. 19 (1992) 670-686
57. Wood J.G., Rogina B., Lavu S., Howitz K., Helfand S.L., Tatar M., and Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430 (2004) 686-689
58. Xu M., and Ashraf M. Melatonin protection against lethal myocyte injury induced by doxorubicin as reflected by effects on mitochondrial membrane potential. J. Mol. Cell. Cardiol. 34 (2002) 75-79
59. Yen H.C., Oberley T.D., Vichitbandha S., Ho Y.S., and St Clair D.K. The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice. J. Clin. Invest. 98 (1996) 1253-1260
60. Zhou B., Wu L.J., Li L.H., Tashiro S., Onodera S., Uchiumi F., and Ikejima T. Silibinin protects against isoproterenol-induced rat cardiac myocyte injury through mitochondrial pathway after up-regulation of SIRT1. J. Pharmacol. Sci. 102 (2006) 387-395
61. Zhu B.Q., Simonis U., Cecchini G., Zhou H.Z., Li L., Teerlink J.R., and Karliner J.S. Comparison of pyrroloquinoline quinone and/or metoprolol on myocardial infarct size and mitochondrial damage in a rat model of ischemia/reperfusion injury. J. Cardiovasc. Pharmacol. Ther. 11 (2006) 119-128