Phosphodiesterase-5 inhibition with sildenafil attenuates cardiomyocyte apoptosis and left ventricular dysfunction in a chronic model of doxorubicin cardiotoxicity

Circulation

Volumn 111, Issue 13, 2005, Pages 1601-1610

  Fisher, Patrick W ^a   Salloum, Fadi ^a   Das, Anindita ^a   Hyder, Haroon ^a   Kukreja, Rakesh C ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Anthracyclines; Apoptosis; Cardiomyopathy; Heart failure; Phosphodiesterase inhibitors

Indexed keywords

5 HYDROXYDECANOIC ACID; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DESMIN; DNA NUCLEOTIDYLEXOTRANSFERASE; DOXORUBICIN; N(G) NITROARGININE METHYL ESTER; PHOSPHODIESTERASE V; PROTEIN BCL 2; SILDENAFIL;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; ELECTROCARDIOGRAM; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART PROTECTION; HEART RATE; HEART VENTRICLE PRESSURE; IMMUNOFLUORESCENCE; IN VITRO STUDY; ISOLATED HEART; LIGATION; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RANDOMIZATION; ST SEGMENT; WESTERN BLOTTING;

3',5'-CYCLIC-GMP PHOSPHODIESTERASE; ANIMALS; APOPTOSIS; CARDIOMYOPATHIES; CHRONIC DISEASE; DOXORUBICIN; DRUG THERAPY, COMBINATION; HEART FAILURE, CONGESTIVE; MALE; MICE; MICE, INBRED ICR; MYOCYTES, CARDIAC; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; PIPERAZINES; PREMEDICATION; VENTRICULAR DYSFUNCTION, LEFT;

EID: 17144405644     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000160359.49478.C2     Document Type: Article

References (47)

1. Bristow MR, Billingham ME, Mason JW, Daniels JR. Clinical spectrum of anthracycline cardiotoxicity. Cancer Treat Rep. 1978;62:873-879.
2. Steinherz LJ, Steinherz PG, Tan CT, Heller G, Murphy ML. Cardiac toxicity 4 to 20 years after completing anthracycline therapy. JAMA. 1991;266:672-677.
3. Steinherz LJ, Steinherz PG, Tan C. Cardiac failure and dysrhythmias 6-19 years after anthracycline therapy: a series of 15 patients. Med Pediatr Oncol. 1995;24:352-361.
4. Meyers C. The role of iron in doxorubicin-induced cardiomyopathy. Semin Oncol. 1998;25:10-14.
5. Nazeyrollas P, Prevost A, Baccard N, Manot L, Devillier P, Millart H. Effects of amifostine on perfused isolated rat heart and on acute doxorubicin-induced cardiotoxicity. Cancer Chemother Pharmacol. 1999;43:227-232.
6. Kumar D, Kirshenbaum LA, Li T, Danelisen I, Singal PK. Apoptosis in Adriamycin cardiomyopathy and its modulation by probucol. Antioxid Redox Signal. 2001;3:135-145.
7. Koning J, Palmer P, Franks CR, Mulder DE, Speyer JL, Green MD, Hellmann K. Cardioxane-ICRF-187 towards anticancer drug specificity through selective toxicity reduction. Cancer Treat Rev. 1991;18:1-19.
8. Liu X, Chen Z, Chua CC, Ma YS, Youngberg GA, Hamdy R, Chua BH. Melatonin as an effective protector against doxorubicin-induced cardiotoxicity. Am J Physiol. 2002;283:H254-H263.
9. Kotamraju S, Konorev EA, Joseph J, 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. 2000;275:33585-33592.
10. Olson RD, Mushlin PS. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 1990;4:3076-3086.
11. Sawyer DB, Fukazawa R, Arstall MA, Kelly RA. Daunorubicin-induced apoptosis in rat cardiac myocytes is inhibited by dexrazoxane. Circ Res. 1999;84:257-265.
12. Narula J, Haider N, Virmani R, DiSalvo TG, Kolodgie FD, Hajjar RJ, Schmidt U, Semigran MJ, Dec GW, Khaw BA. Apoptosis in myocytes in end-stage heart failure. N Engl J Med. 1996;335:1182-1189.
13. Singal PK, Iliskovic N. Doxorubicin-induced cardiomyopathy. N Engl J Med. 1998;339:900-905.
14. Ockaili R, Salloum F, Hawkins J, Kukreja RC. Sildenafil induces powerful cardioprotective effect via opening of mitochondrial K(ATP) channels in rabbits. Am J Physiol. 2002;283:H1263-H1269.
15. Salloum F, Yin C, Xi L, Kukreja RC. Sildenafil induces delayed preconditioning through inducible nitric oxide synthase-dependent pathway in mouse heart. Circ Res. 2003;92:595-597.
16. Kukreja RC, Ockaili R, Salloum F, Yin C, Hawkins J, Das A, Xi L. Cardioprotection with phosphodiesterase-5 inhibition: a novel preconditioning strategy. J Mol Cell Cardiol. 2004;36:165-173.
17. Didenko VV, Boudreaux DJ, Baskin DS. Substantial background reduction in ligase-based apoptosis detection using newly designed hairpin oligonucleotide probes. Biotechniques. 1999;27:1130-1132.
18. Cesselli D, Jakoniuk I, Barlucchi L, Beltrami AP, Hintze TH, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. Oxidative stress-mediated cardiac cell death is a major determinant of ventricular dysfunction and failure in dog dilated cardiomyopathy. Circ Res. 2001;89:279-286.
19. van Acker FA, van Acker SA, Kramer K, Haenen GR, Bast A, van der Vijgh WJ. 7-Monohydroxyethylrutoside protects against chronic doxorubicin-induced cardiotoxicity when administered only once per week. Clin Cancer Res. 2000;6:1337-1341.
20. van Acker SA, Kramer K, Voest EE, Grimbergen JA, Zhang J, van der Vijgh WJ, Bast A. Doxorubicin-induced cardiotoxicity monitored by ECG in freely moving mice: a new model to test potential protectors. Cancer Chemother Pharmacol. 1996;38:95-101.
21. Mattson MP, Kroemer G. Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol Med. 2003;9:196-205.
22. Antonsson B. Mitochondria and the Bcl-2 family proteins in apoptosis signaling pathways. Mol Cell Biochem. 2004;256:141-155.
23. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993;75:241-251.
24. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 1997;275:1132-1136.
25. Le Marc H, Spinelli W, Rosen MR. The effects of doxorubicin on ventricular tachycardia. Circulation. 1986;74:881-889.
26. Jabr RI, Cole WC. Alterations in electrical activity and membrane currents induced by intracellular oxygen-derived free radical stress in guinea pig ventricular myocytes. Circ Res. 1993;72:1229-1244.
27. Kalivendi SV, Kotamraju S, Zhao H, Joseph J, Kalyanaraman B. Doxorubicin-induced apoptosis is associated with increased transcription of endothelial nitric-oxide synthase: effect of antiapoptotic antioxidants and calcium. J Biol Chem. 2001;276:47266-47276.
28. Paxinou E, Weisse M, Chen Q, Souza JM, Hertkorn C, Selak M, Daikhin E, Yudkoff M, Sowa G, Sessa WC, Ischiropoulos H. Dynamic regulation of metabolism and respiration by endogenously produced nitric oxide protects against oxidative stress. Proc Natl Acad Sci U S A. 2001;98: 11575-11580.
29. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M, Pisconti A, Brunelli S, Cardile A, Francolini M, Cantoni O, Carruba MO, Moncada S, Clementi E. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci U S A. 2004;101:16507-16512.
30. Beltran B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S. The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc Natl Acad Sci U S A. 2000;97:14602-14607.
31. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem. 1997;272:31138-31148.
32. Fulda S, Meyer E, Friesen C, Susin SA, Kroemer G, Debatin KM. Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene. 2001;20:1063-1075.
33. Papadopoulou LC, Theophilidis G, Thomopoulos GN, Tsiftsoglou AS. Structural and functional impairment of mitochondria in Adriamycin-induced cardiomyopathy in mice: suppression of cytochrome c oxidase II gene expression. Biochem Pharmacol. 1999;57:481-489.
34. Kalyanaraman B, Joseph J, Kalivendi S, Wang S, Konorev E, Kotamraju S. Doxorubicin-induced apoptosis: implications in cardiotoxicity. Mol Cell Biochem. 2002;234:119-124.
35. Davies KJ, Doroshow JH. Redox cycling of anthracyclines by cardiac mitochondria, I: anthracycline radical formation by NADH dehydrogenase. J Biol Chem. 1986;261:3060-3067.
36. Konorev EA, Kennedy MC, 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. 1999;368:421-428.
37. Doroshow JH, Locker GY, Myers CE. Enzymatic defenses of the mouse heart against reactive oxygen metabolites: alterations produced by doxorubicin. J Clin Invest. 1980;65:128-135.
38. Childs AC, Phaneuf SL, Dirks AJ, Phillips T, Leeuwenburgh C. Doxorubicin treatment in vivo causes cytochrome c release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2:Bax ratio. Cancer Res. 2002;62:4592-4598.
39. Weisleder N, Taffet GE, Capetanaki Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc Natl Acad Sci U S A. 2004;101:769-774.
40. Dinsdale D, Lee JC, Dewson G, Cohen GM, Peter ME. Intermediate filaments control the intracellular distribution of caspases during apoptosis. Am J Pathol. 2004;164:395-407.
41. Wang X, Osinska H, Dorn GW, Nieman M, Lorenz JN, Gerdes AM, Witt S, Kimball T, Gulick J, Robbins J. Mouse model of desmin-related cardiomyopathy. Circulation. 2001;103:2402-2407.
42. Heling A, Zimmermann R, Kostin S, Maeno Y, Hein S, Devaux B, Bauer E, Klovekorn W-P, Schlepper M, Schaper W, Schaper J. Increased expression of cytoskeletal, linkage, and extracellular proteins in failing human myocardium. Circ Res. 2000;86:846-853.
43. Watkins SC, Samuel JL, Marotte F, Bertier-Savalle B, Rappaport L. Microtubules and desmin filaments during onset of heart hypertrophy in rat: a double immunoelectron microscope study. Circ Res. 1987;60:327-336.
44. Watson PA, Hannan R, Carl LL, Giger KE. Desmin gene expression in cardiac myocytes is responsive to contractile activity and stretch. Am J Physiol. 1996;270:C1228-C1235.
45. Lim, PH, Moorthy P, Benton KG. The clinical safety of Viagra. Ann N Y Acad Sci. 2002;962:378-388.
46. Watanabe H, Ohashi K, Takeuchi K, Yamashita K, Yokoyama T, Tran QK, Satoh H, Terada H, Ohashi H, Hayashi H. Sildenafil for primary and secondary pulmonary hypertension. Clin Pharmacol Ther. 2002;71:398-402.
47. Minow R, Benjamin R, Lee E, Gottlieb J. Adriamycin cardiomyopathy: risk factors. Cancer. 1977;39:1397-1402.