Mitochondrial topoisomerase i (Top1mt) is a novel limiting factor of doxorubicin cardiotoxicity

Clinical Cancer Research

Volumn 20, Issue 18, 2014, Pages 4873-4881

  Khiati, Salim ^a   Rosa, Ilaria Dalla ^a   Sourbier, Carole ^b   Ma, Xuefei ^c   Rao, V Ashutosh ^d   Neckers, Leonard M ^b   Zhang, Hongliang ^a   Pommier, Yves ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; DNA TOPOISOMERASE; DOXORUBICIN; MITOCHONDRIAL DNA;

ANIMAL; CARDIOTOXICITY; DRUG EFFECTS; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; HEART MITOCHONDRION; KNOCKOUT MOUSE; METABOLISM; MOUSE; WESTERN BLOTTING;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLOTTING, WESTERN; CARDIOTOXICITY; DNA TOPOISOMERASES, TYPE I; DNA, MITOCHONDRIAL; DOXORUBICIN; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART;

EID: 84907883735     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-3373     Document Type: Article

References (50)

1. DoroshowJH. Anthraycyclines and anthracenediones. In:Chabner BA, Longo DL, editors. Cancer chemotherapy and biotherapy. 2nd ed. Philadelphia:Lippincott-Raven; 1996. p. 409-34.
2. Wang AH, Ughetto G, Quigley GJ, Rich A. Interactions between an anthracycline antibiotic and DNA: molecular structure of daunomycin complexed to d(CpGpTpApCpG) at 1.2-A resolution. Biochemistry 1987;26:1152-63.
3. Ross WE, Glaubiger DL, Kohn KW. Protein-associated DNA breaks in cells treated with adriamycin or ellipticine. Biochim Biophys Acta 1978;519:23-30.
4. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 1984;226:466-8.
5. Capranico G, Kohn KW, Pommier Y. Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin. Nucleic Acids Res 1990;18:6611-9.
6. Pommier Y, Marchand C. Interfacial inhibitors: targeting macromolecular complexes. Nat Rev Drug Discov 2012;11:25-36.
7. Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chem Biol 2013;8:82-95.
8. Nitiss JL. Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 2009;9:338-50.
9. McClendon AK, Osheroff N. DNA topoisomerase II, genotoxicity, and cancer. Mutat Res 2007;623:83-97.
10. Kremer LC, Caron HN. Anthracycline cardiotoxicity in children. N Engl J Med 2004;351:120-1.
11. Weiss RB. The anthracyclines: will we ever find a better doxorubicin? Semin Oncol 1992;19:670-86.
12. Capranico G, Tinelli S, Austin CA, Fisher ML, Zunino F. Different patterns of gene expression of topoisomerase II isoforms in differentiated tissues during murine development. Biochim Biophys Acta 1992;1132:43-8.
13. Jarvinen TA, Liu ET. Simultaneous amplification of HER-2 (ERBB2) and topoisomerase IIalpha (TOP2A) genes-molecular basis for combination chemotherapy in cancer. Curr Cancer Drug Target 2006;6:579-602.
14. Kumar S, Marfatia R, Tannenbaum S, Yang C, Avelar E. Doxorubicininduced cardiomyopathy 17 years after chemotherapy. Tex Heart Inst J 2012;39:424-7.
15. Blanco JG, Sun CL, Landier W, Chen L, Esparza-Duran D, Leisenring W, et al. Anthracycline-related cardiomyopathy after childhood cancer: role of polymorphisms in carbonyl reductase genes-A report from the Children's Oncology Group. J Clin Oncol 2012;30: 1415-21.
16. Xu MF, Tang PL, Qian ZM, Ashraf M. Effects by doxorubicin on the myocardium are mediated by oxygen free radicals. Life Sci 2001;68: 889-901.
17. Berthiaume JM, Wallace KB. Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol 2007;23:15-25.
18. Van Vleet JF, Ferrans VJ, Weirich WE. Cardiac disease induced by chronic adriamycin administration in dogs and an evaluation of vitamin E and selenium as cardioprotectants. Am J Pathol 1980;99:13-42.
19. Unverferth DV, Leier CV, Balcerzak SP, Hamlin RL. Usefulness of a free radical scavenger in preventing doxorubicin-induced heart failure in dogs. Am J Cardiol 1985;56:157-61.
20. Dorr RT. Cytoprotective agents for anthracyclines. Semin Oncol 1996;23:23-34.
21. Doroshow JH, Locker GY, Myers CE. Enzymatic defenses of the mouse heart against reactive oxygen metabolites: alterations produced by doxorubicin. J Clin Invest 1980;65:128-35.
22. Zhang S, Liu X, Bawa-Khalfe T, Lu LS, Lyu YL, Liu LF, et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med 2012;18:1639-42.
23. Jung K, Reszka R. Mitochondria as subcellular targets for clinically useful anthracyclines. Adv Drug Deliv Rev 2001;49:87-105.
24. Adachi K, Fujiura Y, Mayumi F, Nozuhara A, Sugiu Y, Sakanashi T, et al. A deletion of mitochondrial DNA in murine doxorubicin-induced cardiotoxicity. Biochem Biophys Res Commun 1993;195:945-51.
25. Lebrecht D, Setzer B, Ketelsen UP, Haberstroh J, Walker UA. Timedependent and tissue-specific accumulation ofmtDNA and respiratory chain defects in chronic doxorubicin cardiomyopathy. Circulation 2003;108:2423-9.
26. Lebrecht D, Kokkori A, Ketelsen UP, Setzer B, Walker UA. Tissuespecific mtDNA lesions and radical-associated mitochondrial dysfunction in human hearts exposed to doxorubicin. J Pathol 2005; 207:436-44.
27. Ashley N, Poulton J. MitochondrialDNA is a direct target of anti-cancer anthracycline drugs. BiochemBiophys ResCommun2009;378:450-5.
28. Kolesnikov AA, Gerasimov ES. Diversity of mitochondrial genome organization. Biochemistry Biokhimiia 2012;77:1424-35.
29. Zhang H, Barcelo JM, Lee B, Kohlhagen G, Zimonjic DB, Popescu NC, et al. Human mitochondrial topoisomerase I. Proc Natl Acad Sci U S A 2001;98:10608-13.
30. Low RL, Orton S, Friedman DB. A truncated form of DNA topoisomerase IIbeta associates with the mtDNA genome in mammalian mitochondria. Eur J Biochem/FEBS 2003;270:4173-86.
31. Wang Y, Lyu YL, Wang JC. Dual localization of human DNA topoisomerase IIIalpha to mitochondria and nucleus. Proc Natl Acad Sci U S A 2002;99:12114-9.
32. Douarre C, Sourbier C, Dalla Rosa I, Brata Das B, Redon CE, Zhang H, et al. Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism. PLoS ONE 2012;7: e41094.
33. Zhang H, Pommier Y. Mitochondrial topoisomerase I sites in the regulatory D-loop region of mitochondrial DNA. Biochemistry 2008;47: 11196-203.
34. Rogers GW, Brand MD, Petrosyan S, Ashok D, Elorza AA, Ferrick DA, et al. High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS ONE 2011;6: e21746.
35. Hunter SE, Jung D, Di Giulio RT, Meyer JN. The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number. Methods 2010;51:444-51.
36. Nicolay K, de Kruijff 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;892:320-30.
37. Goormaghtigh E, Brasseur R, Ruysschaert JM. Adriamycin inactivates cytochrome c oxidase by exclusion of the enzyme from its cardiolipin essential environment. Biochem Biophys Res Commun 1982;104: 314-20.
38. Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J physiol Heart Circ physiol 2011;301:H2181-90.
39. Mari M, Morales A, Colell A, Garcia-Ruiz C, Fernandez-Checa JC. Mitochondrial glutathione, a key survival antioxidant. Antiox Redox Signal 2009;11:2685-700.
40. Lebrecht D, Walker UA. Role of mtDNA lesions in anthracycline cardiotoxicity. Cardiovasc Toxicol 2007;7:108-13.
41. Das BB, Dexheimer TS, Maddali K, Pommier Y. Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria. Proc Natl Acad Sci U S A 2010;107:19790-5.
42. Chazotte B. Labeling membrane glycoproteins or glycolipids with fluorescent wheat germ agglutinin. Cold Spring Harb Protoc 2011; 2011:pdb prot5623.
43. Chen QM, Tu VC, Purdon S, Wood J, Dilley T. Molecular mechanisms of cardiac hypertrophy induced by toxicants. Cardiovasc Toxicol 2001;1:267-83.
44. Kubli DA, Zhang X, Lee Y,HannaRA, QuinsayMN, Nguyen CK, et al. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 2013;288: 915-26.
45. Ellis CN, Ellis MB, Blakemore WS. Effect of adriamycin on heart mitochondrial DNA. Biochem J 1987;245:309-12.
46. Palmeira CM, Serrano J, Kuehl DW, Wallace KB. Preferential oxidation of cardiac mitochondrial DNA following acute intoxication with doxorubicin. Biochim Biophys Acta 1997;1321:101-6.
47. van Ekeren GJ, Stadhouders AM, Egberink GJ, Sengers RC, Daniels O, Kubat K. Hereditary mitochondrial hypertrophic cardiomyopathy with mitochondrial myopathy of skeletal muscle, congenital cataract and lactic acidosis. Virchows Arch A Pathol Anat Histopathol 1987;412: 47-52.
48. Chandran K, Aggarwal D, Migrino RQ, Joseph J, McAllister D, Konorev EA, et al. Doxorubicin inactivates myocardial cytochrome c oxidase in rats: cardioprotection by Mito-Q. Biophys J 2009;96:1388-98.
49. Dhanasekaran A, Kotamraju S, Kalivendi SV, Matsunaga T, Shang T, Keszler A, et al. Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis. J Biol Chem 2004;279: 37575-87.
50. Dickey JS, Gonzalez Y, Aryal B, Mog S, Nakamura AJ, Redon CE, et al. Mito-tempol and dexrazoxane exhibit cardioprotective and chemotherapeutic effects through specific protein oxidation and autophagy in a syngeneic breast tumor preclinical model. PLoS ONE 2013;8: e70575.