Stabilization of mitochondrial membrane potential prevents doxorubicin-induced cardiotoxicity in isolated rat heart

Toxicology and Applied Pharmacology

Volumn 244, Issue 3, 2010, Pages 300-307

  Montaigne, David ^a   Marechal, Xavier ^a   Baccouch, Riadh ^b   Modine, Thomas ^b   Preau, Sebastien ^a   Zannis, Konstantinos ^b   Marchetti, Philippe ^c   Lancel, Steve ^a   Neviere, Remi ^a  

^a France Institut Pasteur de Lille   (France)

^b LILLE UNIVERSITY HOSPITAL   (France)

^c JEAN PIERRE AUBERT RESEARCH CENTER   (France)

Author keywords

Anthracycline, NADH; Heart failure; Mitochondria; Oxidative phosphorylation

Indexed keywords

CYTOCHROME C OXIDASE; DOXORUBICIN; GLUCOSE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ANTHRACYCLINE; ANTINEOPLASTIC ANTIBIOTIC; CARDIOTOXIN; CYCLOSPORIN;

ANIMAL TISSUE; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; ENZYME ACTIVITY; GLUCOSE TRANSPORT; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE WALL; HEART MITOCHONDRION; HEART MUSCLE CONTRACTILITY; HEART PERFORMANCE; ISOLATED HEART; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION STATE; RAT; ANIMAL; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; ENZYMOLOGY; FLUORESCENCE; FLUOROMETRY; HEART; HEART MUSCLE; IN VITRO STUDY; METABOLISM; OXIDATIVE STRESS; PERMEABILITY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; ANTHRACYCLINES; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOTOXINS; CYCLOSPORINE; DOXORUBICIN; ELECTRON TRANSPORT COMPLEX IV; FLUORESCENCE; FLUOROMETRY; HEART; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MYOCARDIUM; OXIDATIVE STRESS; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; VENTRICULAR DYSFUNCTION, LEFT;

EID: 77950481059     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.01.006     Document Type: Article

References (31)

1. Allen A. The cardiotoxicity of chemotherapeutic drugs. Semin. Oncol. 1992, 19:529-542.
2. Al-Nasser I.A. In vivo prevention of adriamycin cardiotoxicity by cyclosporin A or FK506. Toxicology 1998, 131:175-181.
3. Ashruf J.F., Ince C., Bruining H.A. Regional ischemia in hypertrophic Langendorff-perfused rat hearts. Am. J. Physiol. 1999, 277:H1532-H1539.
4. Berthiaume J.M., Wallace K.B. Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol. Toxicol. 2007, 23:15-25.
5. Boyer P.D. A model for conformational coupling of membrane potential and proton translocation to ATP synthesis and to active transport. FEBS Lett. 1975, 58:1-6.
6. Clarke S.J., McStay G.P., Halestrap A.P. Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J. Biol. Chem. 2002, 277:34793-34799.
7. Cardoso S., Santos R.X., Carvalho C., Correia S., Pereira G.C., Pereira S.S., Oliveira P.J., Santos M.S., Proenca T., Moreira P.I. Doxorubicin increases the susceptibility of brain mitochondria to Ca(2+)-induced permeability transition and oxidative damage. Free Radic. Biol. Med. 2008, 45:1395-1402.
8. Ferreira A.L., Matsubara L.S., Matsubara B.B. Anthracycline-induced cardiotoxicity. Cardiovasc. Hematol. Agents Med. Chem. 2008, 6:278-281.
9. Ganey P.E., Carter L.S., Mueller R.A., Thurman R.G. Doxorubicin toxicity in perfused rat heart. Decreased cell death at low oxygen tension. Circ. Res. 1991, 68:1610-1613.
10. Griffiths E.J., Halestrap A.P. Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol. 1993, 25:1461-1469.
11. Halestrap A.P., Clarke SJ, Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc. Res. 2004, 61:372-385.
12. Hrelia S., Fiorentini D., Maraldi T., Angeloni C., Bordoni A., Biagi P.L., Hakim G. Doxorubicin induces early lipid peroxidation associated with changes in glucose transport in cultured cardiomyocytes. Biochim. Biophys. Acta 2002, 1567:150-156.
13. Jeyaseelan R., Poizat C., Wu H.Y., Kedes L. Molecular mechanisms of doxorubicin-induced cardiomyopathy. Selective suppression of Reiske iron-sulfur protein, ADP/ATP translocase, and phosphofructokinase genes is associated with ATP depletion in rat cardiomyocytes. J. Biol. Chem. 1997, 272:5828-5832.
14. Kato M., Akao M., Matsumoto-Ida M., Makiyama T., Iguchi M., Takeda T., Shimizu S., Kita T. The targeting of cyclophilin D by RNAi as a novel cardioprotective therapy: evidence from two-photon imaging. Cardiovasc. Res. 2009, 83:335-344.
15. Lancel S., Joulin O., Favory R., Goossens J.F., Kluza J., Chopin C., Formstecher P., Marchetti P., Neviere R. Ventricular myocyte caspases are directly responsible for endotoxin-induced cardiac dysfunction. Circulation 2005, 111:2596-2604.
16. Larche J., Lancel S., Hassoun S.M., Favory R., Decoster B., Marchetti P., Chopin C., Neviere R. Inhibition of mitochondrial permeability transition prevents sepsis-induced myocardial dysfunction and mortality. J. Am. Coll. Cardiol. 2006, 48:377-385.
17. Matsumoto-Ida M., Akao M., Takeda T., Kato M., Kita T. Real-time 2-photon imaging of mitochondrial function in perfused rat hearts subjected to ischemia/reperfusion. Circulation 2006, 114:1497-1503.
18. Minotti G., Menna P., Salvatorelli E., Cairo G., Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 2004, 56:185-229.
19. Nicolay K., de Kruijff K.B. Effects of adriamycin on respiratory chain activities in mitochondria from rat liver, rat heart and bovine heart. Evidence for a preferential inhibition of complex III and IV. Biochim. Biophys. Acta 1987, 892:320-330.
20. Niemann C.U., Saeed M., Akbari H., Jacobsen W., Benet L.Z., Christians U., Serkova N. Close association between the reduction in myocardial energy metabolism and infarct size: dose-response assessment of cyclosporine. J. Pharmacol. Exp. Ther. 2002, 302:1123-1128.
21. Oliveira P.J., Wallace K.B. Depletion of adenine nucleotide translocator protein in heart mitochondria from doxorubicin-treated rats-relevance for mitochondrial dysfunction. Toxicology 2006, 220:160-168.
22. Oliveira P.J., Goncalves L., Monteiro P., Providencia L.A., Moreno A.J. Are the antioxidant properties of carvedilol important for the protection of cardiac mitochondria. Curr. Vasc. Pharmacol. 2005, 3:147-158.
23. Reese J.B., Shirhatti V., Singh Y., Krishna G. Daunomycin inhibits the uptake of adenine, amino acids, and glucose into cardiac myocytes. Toxicol. Appl. Pharmacol. 1987, 88:105-112.
24. Riess M.L., Camara A.K., Kevin L.G., An J., Stowe D.F. Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 degrees C ischemia in intact hearts. Cardiovasc. Res. 2004, 61:580-590.
25. Solem L.E., Wallace K.B. Selective activation of the sodium-independent, cyclosporin A-sensitive calcium pore of cardiac mitochondria by doxorubicin. Toxicol. Appl. Pharmacol. 1993, 121:50-57.
26. Solem L.E., Heller L.J., Wallace K.B. Dose-dependent increase in sensitivity to calcium-induced mitochondrial dysfunction and cardiomyocyte cell injury by doxorubicin. J. Mol. Cell. Cardiol. 1996, 28:1023-1032.
27. Tada H., Thompson C.I., Recchia F.A., Loke K.E., Ochoa M., Smith C.J., Shesely E.G., Kaley G., Hintze T.H. Myocardial glucose uptake is regulated by nitric oxide via endothelial nitric oxide synthase in Langendorff mouse heart. Circ. Res. 2000, 86:270-274.
28. Tokarska-Schlattner M., Zaugg M., da S.R., Lucchinetti E., Schaub M.C., Wallimann T., Schlattner U. Acute toxicity of doxorubicin on isolated perfused heart: response of kinases regulating energy supply. Am. J. Physiol. Heart Circ.Physiol. 2005, 289:H37-H47.
29. Tokarska-Schlattner M., Zaugg M., Zuppinger C., Wallimann T., Schlattner U. New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics. J. Mol. Cell. Cardiol. 2006, 41:389-405.
30. Wallace K.B. Adriamycin-induced interference with cardiac mitochondrial calcium homeostasis. Cardiovasc. Toxicol. 2007, 7:101-107.
31. Zhou S., Starkov A., Froberg M.K., Leino R.L., Wallace K.B. Cumulative and irreversible cardiac mitochondrial dysfunction induced by doxorubicin. Cancer Res. 2001, 61:771-777.