Carvedilol inhibits mitochondrial complex I and induces resistance to H2O2-mediated oxidative insult in H9C2 myocardial cells

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1767, Issue 3, 2007, Pages 222-232

  Sgobbo, Paola ^a   Pacelli, Consiglia ^a   Grattagliano, Ignazio ^a   Villani, Gaetano ^a   Cocco, Tiziana ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Carvedilol; Complex I; Glutathione; Mitochondria; Oxidative stress; Respiratory chain

Indexed keywords

CARVEDILOL; GLUTATHIONE; HYDROGEN PEROXIDE; MITOCHONDRIAL COMPLEX I; MITOCHONDRIAL ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; ROTENONE; THIOL; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BIOENERGY; CELL METABOLISM; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; DRUG MECHANISM; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; HEART MUSCLE CELL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; RAT;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; ANTIOXIDANTS; CARBAZOLES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT COMPLEX I; EMBRYO; FREE RADICALS; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PROPANOLAMINES; RATS; SULFHYDRYL COMPOUNDS; TIME FACTORS;

EID: 33947138770     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2007.01.023     Document Type: Article

References (51)

1. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 115 (2005) 500-508
2. Sam F., Kerstetter D.L., Pimental D.R., Mulukutla S., Tabaee A., Bristow M.R., Colucci W.S., and Sawyer D.B. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J. Card. Fail. 11 (2005) 473-480
3. Lefer D.J., and Granger D.N. Oxidative stress and cardiac disease. Am. J. Med. 109 (2000) 315-323
4. McMurray J., Chopra M., Abdullah I., Smith W.E., and Dargie H.J. Evidence of oxidative stress in chronic heart failure in humans. Eur. Heart J. 14 (1993) 1493-1498
5. Bandyopadhyay D., Chattopadhyay A., Ghosh G., and Datta A.G. Oxidative stress-induced ischemic heart disease: protection by antioxidants. Curr. Med. Chem. 11 (2004) 369-387
6. Nakamura K., Kusano K., Nakamura Y., Kakishita M., Ohta K., Nagase S., Yamamoto M., Miyaji K., Saito H., Morita H., Emori T., Matsuhara H., Toyokuni S., and Ohe T. Carvedilol decreases elevated oxidative stress in human failing myocardium. Circulation 105 (2002) 2867-2871
7. Feuerstein G.Z., and Ruffolo Jr. R.R. Carvedilol, a novel multiple action antihypertensive agent with antioxidant activity and the potential for myocardial and vascular protection. Eur. Heart J. 16 (1995) 38-42
8. Colucci W.S., Packer M., Bristow M.R., Gilbert E.M., Cohn J.N., Fowler M.B., Krueger S.K., Hershberger R., Uretsky B.F., Bowers J.A., Sackner-Bernstein J.D., Young S.T., Holcslaw T.L., and Lukas M.A. Carvedilol inhibits clinical progression in patients with mild symptoms of heart failure. US Carvedilol Heart Failure Study Group. Circulation 94 (1996) 2800-2806
9. McMurray J., Kober L., Robertson M., Dargie H., Colucci W., Lopez-Sendon J., Remme W., Sharpe D.N., and Ford I. Antiarrhythmic effect of carvedilol after acute myocardial infarction: results of the Carvedilol Post-Infarct Survival Control in Left Ventricular Dysfunction (CAPRICORN) trial. J. Am. Coll. Cardiol. 45 (2005) 525-530
10. Monteiro P., Duarte A.I., Moreno A., Goncalves L.M., and Providencia L.A. Carvedilol improves energy production during acute global myocardial ischaemia. Eur. J. Pharmacol. 482 (2003) 245-253
11. Yue T.L., Cheng H.Y., Lysko P.G., McKenna P.J., Feuerstein R., Gu J.L., Lysko K.A., Davis L.L., and Feuerstein G. Carvedilol, a new vasodilator and beta adrenoceptor antagonist, is an antioxidant and free radical scavenger. J. Pharmacol. Exp. Ther. 263 (1992) 92-98
12. Feuerstein G.Z., Bril A., and Ruffolo Jr. R.R. Protective effects of carvedilol in the myocardium. Am. J. Cardiol. Am. J. Cardiol. 80 (1997) 41-45
13. Feuerstein G., Liu G.L., Yue T.L., Cheng H.Y., Hieble J.P., Arch J.R., Ruffolo Jr. R.R., and Ma X.L. Comparison of metoprolol and carvedilol pharmacology and cardioprotection in rabbit ischemia and reperfusion model. Eur. J. Pharmacol. 351 (1998) 341-350
14. Lysko P.G., Webb C.L., Gu J.L., Ohlstein E.H., Ruffolo Jr. R.R., and Yue T.L.A. A comparison of carvedilol and metoprolol antioxidant activities in vitro. J. Cardiovasc. Pharmacol. 36 (2000) 277-281
15. Flesch M., Maack C., Cremers B., Baumer A.T., Sudkamp M., and Bohm M. Effect of beta-blockers on free radical-induced cardiac contractile dysfunction. Circulation 100 (1999) 346-353
16. Koitabashi N., Arai M., Tomaru K., Takizawa T., Watanabe A., Niwano K., Yokoyama T., Wuytack F., Periasamy M., Nagai R., and Kurabayashi M. Carvedilol effectively blocks oxidative stress-mediated downregulation of sarcoplasmic reticulum Ca2+-ATPase 2 gene transcription through modification of Sp1 binding. Biochem. Biophys. Res. Commun. 328 (2005) 116-124
17. Cargnoni A., Ceconi C., Bernocchi P., Boraso A., Parrinello G., Curello S., and Ferrari R. Reduction of oxidative stress by carvedilol: role in maintenance of ischaemic myocardium viability. Cardiovasc. Res. 47 (2000) 556-566
18. Oliveira P.J., Rolo A.P., Monteiro P., Goncalves L., Palmeira C.M., and Moreno A.J. Impact of carvedilol on the mitochondrial damage induced by hypoxanthine and xantine oxidase-what role in myocardial ischemia and reperfusion?. Rev. Port. Cardiol. 21 (2002) 1447-1455
19. Yue T.L., McKenna P.J., Gu J.L., Cheng H.Y., Ruffolo Jr. R.E., and Feuerstein G.Z. Carvedilol, a new vasodilating beta adrenoceptor blocker antihypertensive drug, protects endothelial cells from damage initiated by xanthine-xanthine oxidase and neutrophils. Cardiovasc. Res. 28 (1994) 400-406
20. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
21. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
22. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J. Biol. Chem. 276 (2001) 2571-2575
23. Oliveira P.J., Esteves T., Rolo A.P., Palmeira C.M., and Moreno A.J. Carvedilol inhibits the mitochondrial permeability transition by an antioxidant mechanism. Cardiovasc. Toxicol. 4 (2004) 11-20
24. Cocco T., Cutecchia G., Montedoro G., and Lorusso M. The antihypertensive drug carvedilol inhibits the activity of mitochondrial NADH-ubiquinone oxidoreductase. J. Bioenerg. Biomembr. 34 (2002) 251-258
25. Oliveira P.J., Goncalves L., Monteiro P., Providencia L.A., and Moreno A.J. Are the antioxidant properties of carvedilol important for the protection of cardiac mitochondria?. Curr. Vasc. Pharmacol. 3 (2005) 147-158
26. Kimes B.W., and Brandt B.L. Properties of a clonal muscle cell line from rat heart. Exp. Cell Res. 98 (1976) 367-381
27. Villani G., and Attardi G. In vivo measurements of respiration control by cytochrome c oxidase and in situ analysis of oxidative phosphorylation. Methods Cell. Biol. 65 (2001) 119-131
28. Cocco T., Sgobbo P., Clemente M., Lopriore B., Grattagliano I., Di Paola M., and Villani G. Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic. Biol. Med. 38 (2005) 796-805
29. McLennan H.R., and Degli Esposti M. The contribution of mitochondrial respiratory complexes to the production of reactive oxygen species. J. Bioenerg. Biomembr. 32 (2000) 153-162
30. Grattagliano I., Vendemiale G., Sabba C., Buonamico P., and Altomare E. Oxidation of circulating proteins in alcoholics: role of acetaldehyde and xanthine oxidase. J. Hepatol. 25 (1996) 28-36
31. 2. Free Radic. Biol. Med. 37 (2004) 1272-1281
32. Oliveira P.J., Marques M.P., Batista de Carvalho L.A., and Moreno A.J. Effects of carvedilol on isolated heart mitochondria: evidence for a protonophoretic mechanism. Biochem. Biophys. Res. Commun. 276 (2000) 82-87
33. Abreu R.M., Santos D.J., and Moreno A.J. Effects of carvedilol and its analog BM-910228 on mitochondrial function and oxidative stress. J. Pharmacol. Exp. Ther. 295 (2000) 1022-1030
34. Santos D.J., and Moreno A.J. Inhibition of heart mitochondrial lipid peroxidation by non-toxic concentrations of carvedilol and its analog BM-910228. Biochem. Pharmacol. 61 (2001) 155-164
35. Spallarossa P., Garibaldi S., Altieri P., Fabbi P., Manca V., Nasti S., Rossettin P., Ghigliotti G., Ballestrero A., Patrone F., Barsotti A., and Brunelli C. Carvedilol prevents doxorubicin-induced free radical release and apoptosis in cardiomyocytes in vitro. J. Mol. Cell. Cardiol. 37 (2004) 837-846
36. Yue T.L., McKenna P.J., Lysko P.G., Ruffolo Jr. R.R., and Feuerstein G.Z. Carvedilol, a new antihypertensive, prevents oxidation of human low density lipoprotein by macrophages and copper. Atherosclerosis 97 (1992) 209-216
37. Cheng H.Y., Randall C.S., Holl W.W., Constantinides P.P., Yue T.L., and Feuerstein G.Z. Carvedilol-liposome interaction: evidence for strong association with the hydrophobic region of the lipid bilayers. Biochim. Biophys. Acta 1284 (1996) 20-28
38. Oliveira P.J., Bjork J.A., Santos M.S., Leino R.L., Froberg M.K., Moreno A.J., and Wallace K.B. Carvedilol-mediated antioxidant protection against doxorubicin-induced cardiac mitochondrial toxicity. Toxicol. Appl. Pharmacol. 200 (2004) 159-168
39. Santos D.L., Moreno A.J., Leino R.L., Froberg M.K., and Wallace K.B. Carvedilol protects against doxorubicin-induced mitochondrial cardiomyopathy. Toxicol. Appl. Pharmacol. 185 (2002) 218-227
40. Vanden Hoek T.L., Shao Z., Li C., Schumacker P.T., and Becker L.B. Mitochondrial electron transport can become a significant source of oxidative injury in cardiomyocytes. J. Mol. Cell Cardiol. 29 (1997) 2441-2450
41. Tsutsui H., Ide T., Hayashidani S., Suematsu N., Utsumi H., Nakamura R., Egashira K., and Takeshita A. Greater susceptibility of failing cardiac myocytes to oxygen free radical-mediated injury. Cardiovasc. Res. 49 (2001) 103-109
42. Hajek P., Villani G., and Attardi G. Rate-limiting step preceding cytochrome c release in cells primed for Fas-mediated apoptosis revealed by analysis of cellular mosaicism of respiratory changes. J. Biol. Chem. 276 (2001) 606-615
43. Huang X., Zhai D., and Huang Y. Dependence of permeability transition pore opening and cytochrome c release from mitochondria on mitochondria energetic status. Mol. Cell Biochem. 224 (2001) 1-7
44. Wolvetang E.J., Johnson K.L., Krauer K., Ralph S.J., and Linnane A.W. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 339 (1994) 40-44
45. Bautista J., Corpas R., Ramos R., Cremades O., Gutierrez J.F., and Alegre S. Brain mitochondrial complex I inactivation by oxidative modification. Biochem. Biophys. Res. Commun. 275 (2000) 890-894
46. Murray C.E., Jennings R.B., and Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74 (1986) 1124-1136
47. De Zeeuw S., Van Den Doel M.A., Duncker D.J., and Verdouw P.D. New insights into cardioprotection by ischemic preconditioning and other forms of stress. Ann. N. Y. Acad. Sci. 874 (1999) 179-191
48. Verdouw P.D., Gho B.C., Koning M.M.G., Schoemaker R.G., and Duncker D.J. Cardioprotection by ischemic and nonischemic myocardial stress and ischemia in remote organs. Implications for the concept of ischemic preconditioning. Ann. N. Y. Acad. Sci. 793 (1996) 27-42
49. Han H., Wang H., Long H., Nattel S., and Wang Z. Oxidative preconditioning and apoptosis in L-cells. Roles of protein kinase B and mitogen-activated protein kinases. J. Biol. Chem. 276 (2001) 26357-26364
50. Vanden Hoek T., Becker L.B., Shao Z.H., Li C.Q., and Schumacker P.T. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ. Res. 86 (2000) 541-548
51. Kowaltowski A.J., Fenton R.G., and Fiskum G. Bcl-2 family proteins regulate mitochondrial reactive oxygen production and protect against oxidative stress. Free Radic. Biol. Med. 37 (2004) 1845-1853