Anthracycline-containing chemotherapy causes long-term impairment of mitochondrial respiration and increased reactive oxygen species release in skeletal muscle

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Gouspillou, Gilles ^a,b   Scheede Bergdahl, Celena ^c,d   Spendiff, Sally ^a,d   Vuda, Madhusudanarao ^a   Meehan, Brian ^d,e   Mlynarski, Heather ^c   Archer Lahlou, Elodie ^c   Sgarioto, Nicolas ^a   Purves Smith, Fennigje M ^a,d   Konokhova, Yana ^a,d   Rak, Janusz ^d,e   Chevalier, Stéphanie ^a   Taivassalo, Tanja ^d   Hepple, Russell T ^a,d   Jagoe, R Thomas ^c,d  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE; ANTINEOPLASTIC AGENT; DEXAMETHASONE; DOXORUBICIN; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

ANIMAL; CELL RESPIRATION; DRUG EFFECTS; FEMALE; GENE DELETION; GENETICS; METABOLISM; MITOPHAGY; MOUSE; MUSCLE MITOCHONDRION; MUTATION; OXIDATIVE STRESS; PATHOLOGY; SKELETAL MUSCLE;

ANIMALS; ANTHRACYCLINES; ANTINEOPLASTIC AGENTS; CELL RESPIRATION; DEXAMETHASONE; DNA, MITOCHONDRIAL; DOXORUBICIN; FEMALE; MICE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DEGRADATION; MUSCLE, SKELETAL; MUTATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SEQUENCE DELETION;

EID: 84937012883     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08717     Document Type: Article

References (47)

1. Siegel, R.,Naishadham,D.&Jemal, A. Cancer statistics, 2012. CA Cancer J Clin 62, 10-29 (2012).
2. Zuelzer, W. W. Implications of long-term survival in acute stem cell leukemia of childhood treated with composite cyclical therapy. Blood 24, 477-494 (1964).
3. Hudson, M. M. et al. Clinical ascertainment of health outcomes among adults treated for childhood cancer. JAMA 309, 2371-2381 (2013).
4. Scheede-Bergdahl, C. & Jagoe, R. T. After the chemotherapy: potential mechanisms for chemotherapy-induced delayed skeletal muscle dysfunction in survivors of acute lymphoblastic leukaemia in childhood. Front Pharmacol 4, 49 (2013).
5. Pui, C.-H. & Evans, W. E. Treatment of acute lymphoblastic leukemia. N Engl J Med 354, 166-178 (2006).
6. Ewer, M. S. & Ewer, S. M. Cardiotoxicity of anticancer treatments: what the cardiologist needs to know. Nat Rev Cardiol 7, 564-575 (2010).
7. Peters, J. H., Gordon, G. R., Kashiwase, D. & Acton, E. M. Tissue distribution of doxorubicin and doxorubicinol in rats receiving multiple doses of doxorubicin. Cancer Chemother Pharmacol 7, 65-69 (1981).
8. Octavia, Y. et al. Doxorubicin-induced cardiomyopathy: From molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 52, 1213-1225 (2012).
9. Serrano, J., Palmeira, C. M., Kuehl, D. W. & Wallace, K. B. Cardioselective and cumulative oxidation of mitochondrial DNA following subchronic doxorubicin administration. Biochim Biophys Acta 1411, 201-205 (1999).
10. Adachi, K. et al. A deletion of mitochondrial DNA in murine doxorubicininduced cardiotoxicity. Biochem Biophys Res Commun 195, 945-951 (1993).
11. Lebrecht, D., Setzer, B., Ketelsen, U. P., Haberstroh, J. & Walker, U. A. Timedependent and tissue-specific accumulation of mtDNA and respiratory chain defects in chronic doxorubicin cardiomyopathy. Circulation 108, 2423-2429 (2003).
12. Lebrecht, D. et al. Dexrazoxane prevents doxorubicin-induced long-term cardiotoxicity and protects myocardial mitochondria from genetic and functional lesions in rats. Brit J Pharmacol 151, 771-778 (2007).
13. Lebrecht, D., Kokkori, A., Ketelsen, U.-P., Setzer, B. & Walker, U. A. Tissuespecific mtDNA lesions and radical-associated mitochondrial dysfunction in human hearts exposed to doxorubicin. J Pathol 207, 436-444 (2005).
14. Ito, H. et al. Doxorubicin selectively inhibits muscle gene expression in cardiac muscle cells in vivo and in vitro. Proc Natl Acad Sci USA 87, 4275-4279 (1990).
15. Yamada, K., Sugiyama, S., Kosaka, K., Hayakawa, M. & Ozawa, T. Early appearance of age-associated deterioration in mitochondrial function of diaphragm and heart in rats treated with doxorubicin. Exp Gerontol 30, 581-593 (1995).
16. Gilliam, L. A. A. et al. Doxorubicin acts via mitochondrial ROS to stimulate catabolism in C2C12myotubes.AmJ Physiol Cell Physiol 302, C195-C202 (2012).
17. Gilliam, L. A. A. et al. Doxorubicin acts through tumor necrosis factor receptor subtype 1 to cause dysfunction of murine skeletal muscle. J Appl Physiol 107, 1935-1942 (2009).
18. Batchelor, T. T., Taylor, L. P., Thaler, H. T., Posner, J. B. & DeAngelis, L. M. Steroid myopathy in cancer patients. Neurology 48, 1234-1238 (1997).
19. Mitsui, T. et al. Chronic corticosteroid administration causes mitochondrial dysfunction in skeletal muscle. J Neurol 249, 1004-1009 (2002).
20. Kuznetsov, A. et al. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protocol 3, 965-976 (2008).
21. Gouspillou, G. et al. Increased sensitivity to mitochondrial permeability transition and myonuclear translocation of endonuclease G in atrophied muscle of physically active older humans. The FASEB Journal 28, 1621-1633 (2014).
22. Samuels, D. C., Schon, E. A. & Chinnery, P. F. Two direct repeats cause most human mtDNA deletions. Trends Genet 20, 393-398 (2004).
23. He, L. et al. Detection and quantification of mitochondrial DNA deletions in individual cells by real-time PCR. Nucleic Acids Res 30, e68 (2002).
24. Mordente, A., Meucci, E., Silvestrini, A., Martorana, G. E. & Giardina, B. Anthracyclines and mitochondria. Adv Exp Med Biol 942, 385-419 (2012).
25. Palikaras, K. & Tavernarakis, N. Mitochondrial homeostasis: The interplay between mitophagy and mitochondrial biogenesis. Exp Gerontol (2014).
26. Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nature 12, 119-131 (2010).
27. Sun, Y., Vashisht, A. A., Tchieu, J., Wohlschlegel, J. A. & Dreier, L. Voltagedependent Anion Channels (VDACs) Recruit Parkin to Defective Mitochondria to Promote Mitochondrial Autophagy. J Biol Chem 287, 40652-40660 (2012).
28. Grady, R. M. et al. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90, 729-738 (1997).
29. Trifunovic, A. et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423 (2004).
30. Jansson, J., Hsu, Y.-C., Kuzin, I. I., Campbell, A. & Mullen, C. A. Acute lymphoblastic leukemia cells that survive combination chemotherapy in vivo remain sensitive to allogeneic immune effects. Leuk Res 35, 800-807 (2011).
31. Picard, M. et al. Mitochondrial structure and function are disrupted by standard isolation methods. PLoS ONE 6, e18317 (2011).
32. Anderson, E. J. et al. Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol 54, 1891-1898 (2009).
33. Kuznetsov, A. V. et al. Application of inhibitor titrations for the detection of oxidative phosphorylation defects in saponin-skinned muscle fibers of patients with mitochondrial diseases. Biochim Biophys Acta 1360, 142-150 (1997).
34. Picard, M., Ritchie, D., Thomas, M. M.,Wright, K. J.&Hepple, R. T. Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles. Aging Cell 10, 1047-1055 (2011).
35. Gouspillou, G. & Hepple, R. T. Facts and controversies in our understanding of how caloric restriction impacts the mitochondrion. Exp Gerontol 48, 1075-1084 (2013).
36. Caffin, F. et al. Altered skeletal muscle mitochondrial biogenesis but improved endurance capacity in trained OPA1-deficient mice. J Physiol 591, 6017-6037 (2013).
37. Nielsen, J. et al. Subcellular localization-dependent decrements in skeletal muscle glycogen and mitochondria content following short-term disuse in young and old men. Am J Physiol Endocrinol Metab 299, E1053-E1060 (2010).
38. Wagatsuma, A. et al. Mitochondrial adaptations in skeletal muscle to hindlimb unloading. Mol Cell Biochem 350, 1-11 (2010).
39. Min, K. et al.Mitochondrial-targeted antioxidants protect skeletal muscle against immobilization-induced muscle atrophy. J Appl Physiol 111, 1459-1466 (2011).
40. Yan, L. J., Levine, R. L. & Sohal, R. S. Oxidative damage during aging targets mitochondrial aconitase. Proc Natl Acad Sci USA 94, 11168-11172 (1997).
41. Yan, L. J. & Sohal, R. S. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc Natl Acad Sci USA 95, 12896-12901 (1998).
42. Hammerling, B. C. & Gustafsson, Ã.B. Mitochondrial quality control in the myocardium: cooperation between protein degradation andmitophagy. JMol Cell Cardiol 75, 122-130 (2014).
43. Picard, M. et al.Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 9, 1032-1046 (2010).
44. Old, S. L. & Johnson, M. A. Methods of microphotometric assay of succinate dehydrogenase and cytochrome c oxidase activities for use on human skeletal muscle. Histochem. J. 21, 545-555 (1989).
45. Murphy, J. L. et al. Cytochrome c oxidase-intermediate fibres: importance in understanding the pathogenesis and treatment of mitochondrial myopathy. Neuromuscul Disord 22, 690-698 (2012).
46. Cree, L. M. et al. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 40, 249-254 (2008).
47. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, 1-10 (2002).