Reduced creatine-stimulated respiration in doxorubicin challenged mitochondria: Particular sensitivity of the heart

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1767, Issue 11, 2007, Pages 1276-1284

  Tokarska Schlattner, Malgorzata ^a,d   Dolder, Max ^b   Gerber, Isabelle ^a   Speer, Oliver ^c   Wallimann, Theo ^a   Schlattner, Uwe ^a,d  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^d INSERM   (France)

Author keywords

Anthracycline; Cardiotoxicity; Creatine kinase; Creatine simulated respiration; Isolated mitochondria

Indexed keywords

ADENOSINE DIPHOSPHATE; CARDIOLIPIN; CREATINE KINASE; CREATININE; DOXORUBICIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CHEMOSENSITIVITY; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; ENZYME ACTIVITY; ENZYME BINDING; HEART MITOCHONDRION; MEMBRANE BINDING; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROVOCATION TEST; RAT;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; CATTLE; CREATINE; CREATINE KINASE; DOXORUBICIN; ELECTRON TRANSPORT; ELECTROPHORESIS, POLYACRYLAMIDE GEL; IMMUNOBLOTTING; ISOENZYMES; KINETICS; MITOCHONDRIA; MITOCHONDRIA, HEART; OXYGEN; RATS;

EID: 35549010278     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2007.08.006     Document Type: Article

References (47)

1. Tokarska-Schlattner M., Zaugg M., Zuppinger C., Wallimann T., and Schlattner U. New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics. J. Mol. Cell. Cardiol. 41 (2006) 389-405
2. Saks V.A., Ventura-Clapier R., and Aliev M.K. Metabolic control and metabolic capacity: two aspects of creatine kinase functioning in the cells. Biochim. Biophys. Acta 1274 (1996) 81-88
3. Schlattner U., Tokarska-Schlattner M., and Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim. Biophys. Acta 1762 (2006) 164-180
4. Schlattner U., and Wallimann T. In: Lennarz W.J., and Lane M.D. (Eds). Encyclopedia of Biological Chemistry (2004), Academic Press, New York, USA 646-651
5. Saks V., Dzeja P., Schlattner U., Vendelin M., Terzic A., and Wallimann T. Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J. Physiol. 571 (2006) 253-273
6. Tokarska-Schlattner M., Wallimann T., and Schlattner U. Multiple interference of anthracyclines with mitochondrial creatine kinases: preferential damage of the cardiac isoenzyme and its implications for drug cardiotoxicity. Mol. Pharmacol. 61 (2002) 516-523
7. Epand R.F., Tokarska-Schlattner M., Schlattner U., Wallimann T., and Epand R.M. Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J. Mol. Biol. 365 (2007) 968-980
8. Brdiczka D., Beutner G., Ruck A., Dolder M., and Wallimann T. The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition. Biofactors 8 (1998) 235-242
9. Tokarska-Schlattner M., Zaugg M., da Silva R., Lucchinetti E., Schaub M.C., Wallimann T., and Schlattner U. Acute toxicity of doxorubicin on isolated perfused heart: response of kinases regulating energy supply. Am. J. Physiol. Heart Circ. Physiol. 289 (2005) H37-H47
10. Wyss M., Smeitink J., Wevers R.A., and Wallimann T. Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism. Biochim. Biophys. Acta 1102 (1992) 119-166
11. Jacobus W.E. Respiratory control and the integration of heart high-energy phosphate metabolism by mitochondrial creatine kinase. Annu. Rev. Physiol. 47 (1985) 707-725
12. Boveris A., Oshino N., and Chance B. The cellular production of hydrogen peroxide. Biochem. J. 128 (1972) 617-630
13. Meyer L.E., Machado L.B., Santiago A.P., da-Silva W.S., De Felice F.G., Holub O., Oliveira M.F., and Galina A. Mitochondrial creatine kinase activity prevents reactive oxygen species generation: antioxidant role of mitochondrial kinase-dependent ADP re-cycling activity. J. Biol. Chem. 281 (2006) 37361-37371
14. Dolder M., Walzel B., Speer O., Schlattner U., and Wallimann T. Inhibition of the mitochondrial permeability transition by creatine kinase substrates. Requirement for microcompartmentation. J. Biol. Chem. 278 (2003) 17760-17766
15. Cheneval D., Carafoli E., Powell G.L., and Marsh D. A spin-label electron spin resonance study of the binding of mitochondrial creatine kinase to cardiolipin. Eur. J. Biochem. 186 (1989) 415-419
16. Cheneval D., Muller M., Toni R., Ruetz S., and Carafoli E. Adriamycin as a probe for the transversal distribution of cardiolipin in the inner mitochondrial membrane. J. Biol. Chem. 260 (1985) 13003-13007
17. Vacheron M.J., Clottes E., Chautard C., and Vial C. Mitochondrial creatine kinase interaction with phospholipid vesicles. Arch. Biochem. Biophys. 344 (1997) 316-324
18. Minotti G., Menna P., Salvatorelli E., Cairo G., and Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 56 (2004) 185-229
19. Dolder M., Wendt S., and Wallimann T. Mitochondrial creatine kinase in contact sites: interaction with porin and adenine nucleotide translocase, role in permeability transition and sensitivity to oxidative damage. Biol. Signals Recept. 10 (2001) 93-111
20. Koufen P., Ruck A., Brdiczka D., Wendt S., Wallimann T., and Stark G. Free radical-induced inactivation of creatine kinase: influence on the octameric and dimeric states of the mitochondrial enzyme (Mib-CK). Biochem. J. 344 Pt 2 (1999) 413-417
21. Mihm M.J., Yu F., Weinstein D.M., Reiser P.J., and Bauer J.A. Intracellular distribution of peroxynitrite during doxorubicin cardiomyopathy: evidence for selective impairment of myofibrillar creatine kinase. Br. J. Pharmacol. 135 (2002) 581-588
22. Soboll S., Brdiczka D., Jahnke D., Schmidt A., Schlattner U., Wendt S., Wyss M., and Wallimann T. Octamer-dimer transitions of mitochondrial creatine kinase in heart disease. J. Mol. Cell. Cardiol. 31 (1999) 857-866
23. Stachowiak O., Dolder M., Wallimann T., and Richter C. Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J. Biol. Chem. 273 (1998) 16694-16699
24. Wendt S., Schlattner U., and Wallimann T. Differential effects of peroxynitrite on human mitochondrial creatine kinase isoenzymes. Inactivation, octamer destabilization, and identification of involved residues. J. Biol. Chem. 278 (2003) 1125-1130
25. Toleikis A.I., Kal'venas A.A., Dzheia P.P., Prashkiavichius A.K., and Iasaitis A.A. Functional changes in the mitochondrial site of adenylate kinase and creatine kinase systems of energy transport induced by myocardial ischemia and adriablastin. Biokhimiia 53 (1988) 649-654
26. Jacobus W.E., and Lehninger A.L. Creatine kinase of rat heart mitochondria. Coupling of creatine phosphorylation to electron transport. J. Biol. Chem. 248 (1973) 4803-4810
27. Schlattner U., Eder M., Dolder M., Khuchua Z.A., Strauss A.W., and Wallimann T. Divergent enzyme kinetics and structural properties of the two human mitochondrial creatine kinase isoenzymes. Biol. Chem. 381 (2000) 1063-1070
28. Wyss M., Schlegel J., James P., Eppenberger H.M., and Wallimann T. Mitochondrial creatine kinase from chicken brain. Purification, biophysical characterization, and generation of heterodimeric and heterooctameric molecules with subunits of other creatine kinase isoenzymes. J. Biol. Chem. 265 (1990) 15900-15908
29. Schlattner U., Mockli N., Speer O., Werner S., and Wallimann T. Creatine kinase and creatine transporter in normal, wounded, and diseased skin. J. Invest. Dermatol. 118 (2002) 416-423
30. Schlattner U., and Wallimann T. Octamers of mitochondrial creatine kinase isoenzymes differ in stability and membrane binding. J. Biol. Chem. 275 (2000) 17314-17320
31. Gosalvez M., Blanco M., Hunter J., Miko M., and Chance B. Effects of anticancer agents on the respiration of isolated mitochondria and tumor cells. Eur. J. Cancer 10 (1974) 567-574
32. Muhammed H., Ramasarma T., and Kurup C.K. Inhibition of mitochondrial oxidative phosphorylation by adriamycin. Biochim. Biophys. Acta 722 (1983) 43-50
33. Bianchi C., Bagnato A., Paggi M.G., and Floridi A. Effect of adriamycin on electron transport in rat heart, liver, and tumor mitochondria. Exp. Mol. Pathol. 46 (1987) 123-135
34. Gewirtz D.A. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57 (1999) 727-741
35. In: Saks V. (Ed). Molecular Systems Bioenergetics-Energy for Life (2007), Wiley-VCH, Weinheim
36. Saks V., Aliev M., Guzun R., Beraud N., Monge C., Anmann T., Kuznetsov A.V., and Seppet E. Biophysics of the organized metabolic networks in muscle and brain cells. Recent Res. Devel. Biophysics 5 (2006) 1-49
37. Ventura-Clapier R., Kuznetsov A., Veksler V., Boehm E., and Anflous K. Functional coupling of creatine kinases in muscles: species and tissue specificity. Mol. Cell. Biochem. 184 (1998) 231-247
38. Anflous K., Veksler V., Mateo P., Samson F., Saks V., and Ventura-Clapier R. Mitochondrial creatine kinase isoform expression does not correlate with its mode of action. Biochem. J. 322 Pt 1 (1997) 73-78
39. Khuchua Z.A., Qin W., Boero J., Cheng J., Payne R.M., Saks V.A., and Strauss A.W. Octamer formation and coupling of cardiac sarcomeric mitochondrial creatine kinase are mediated by charged N-terminal residues. J. Biol. Chem. 273 (1998) 22990-22996
40. Pelikan P.C., Gerstenblith G., Vandegaer K., and Jacobus W.E. Absence of acute doxorubicin-induced dysfunction of heart mitochondrial oxidative phosphorylation and creatine kinase activities. Proc. Soc. Exp. Biol. Med. 188 (1988) 7-16
41. Miura T., Muraoka S., and Fujimoto Y. Inactivation of creatine kinase by adriamycin during interaction with horseradish peroxidase. Biochem. Pharmacol. 60 (2000) 95-99
42. Miura T., Muraoka S., and Ogiso T. Adriamycin-Fe(3+)-induced inactivation of rat heart mitochondrial creatine kinase: sensitivity to lipid peroxidation. Biol. Pharm. Bull. 17 (1994) 1220-1223
43. Yen H.C., Oberley T.D., Gairola C.G., Szweda L.I., and St Clair D.K. Manganese superoxide dismutase protects mitochondrial complex I against adriamycin-induced cardiomyopathy in transgenic mice. Arch. Biochem. Biophys. 362 (1999) 59-66
44. Speer O., Back N., Buerklen T., Brdiczka D., Koretsky A., Wallimann T., and Eriksson O. Octameric mitochondrial creatine kinase induces and stabilizes contact sites between the inner and outer membrane. Biochem. J. 385 (2005) 445-450
45. Epand R.F., Schlattner U., Wallimann T., Lacombe M.L., and Epand R.M. Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys. J. 92 (2007) 126-137
46. Wallace K.B. Doxorubicin-induced cardiac mitochondrionopathy. Pharmacol. Toxicol. 93 (2003) 105-115
47. Braith R.W. Role of exercise in rehabilitation of cancer survivors. Pediatr. Blood Cancer 44 (2005) 595-599