Chronic anthracycline Cardiotoxicity: Molecular and functional analysis with focus on nuclear factor erythroid 2-related factor 2 and mitochondrial biogenesis pathways

Journal of Pharmacology and Experimental Therapeutics

Volumn 343, Issue 2, 2012, Pages 468-478

  Jirkovský, Eduard ^a   Popelová, Olga ^a   Křiváková Staňková, Pavla ^a   Vávrová, Anna ^b   Hroch, Miloš ^a   Hašková, Pavlína ^a,b   Brčáková Doleželová, Eva ^a,b   Mičuda, Stanislav ^a   Adamcová, Michaela ^a   Šimůnek, Tomáš ^a,b   Červinková, Zuzana ^a   Geršl, Vladimír ^a   Štěrba, Martin ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b Charles University in Prague Faculty of Pharmacy   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

DAUNORUBICIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEME OXYGENASE 1; MANGANESE SUPEROXIDE DISMUTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CARDIOTOXICITY; CHRONIC TOXICITY; CONGESTIVE HEART FAILURE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; GENE TARGETING; HEART DILATATION; HEART LEFT VENTRICLE FAILURE; LIPID PEROXIDATION; LONG TERM CARE; MALE; MITOCHONDRIAL GENE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN METABOLISM; RABBIT; REPEATED DRUG DOSE; TREATMENT DURATION; UPREGULATION;

EID: 84867608210     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.112.198358     Document Type: Article

References (49)

1. Asensio-López MC, Lax A, Pascual-Figal DA, Valdés M, and Sánchez-Más J (2011) Metformin protects against doxorubicin-induced cardiotoxicity: involvement of the adiponectin cardiac system. Free Radic Biol Med 51:1861-1871.
2. Ashour AE, Sayed-Ahmed MM, Abd-Allah AR, Korashy HM, Maayah ZH, Alkhalidi H, Mubarak M, and Alhaider A (2012) Metformin rescues the myocardium from doxorubicin-induced energy starvation and mitochondrial damage in rats. Oxid Med Cell Longev 2012:434195.
3. Baird L and Dinkova-Kostova AT (2011) The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 85:241-272.
4. Bernuzzi F, Recalcati S, Alberghini A, and Cairo G (2009) Reactive oxygen species-independent apoptosis in doxorubicin-treated H9c2 cardiomyocytes: role for heme oxygenase-1 down-modulation. Chem Biol Interact 177:12-20.
5. Berthiaume JM, Oliveira PJ, Fariss MW, and Wallace KB (2005) Dietary vitamin E decreases doxorubicin-induced oxidative stress without preventing mitochondrial dysfunction. Cardiovasc Toxicol 5:257-267. (Pubitemid 41506867)
6. Berthiaume JM and Wallace KB (2007) Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol 23:15-25. (Pubitemid 44950185)
7. Choi EH, Lee N, Kim HJ, Kim MK, Chi SG, Kwon DY, and Chun HS (2008) Schisandra fructus extract ameliorates doxorubicin-induce cytotoxicity in cardiomyocytes: altered gene expression for detoxification enzymes. Genes Nutr 2:337-345. (Pubitemid 351447709)
8. Davies KJ and Doroshow JH (1986) Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem 261:3060-3067. (Pubitemid 17204909)
9. De Sousa E, Veksler V, Minajeva A, Kaasik A, Mateo P, Mayoux E, Hoerter J, Bigard X, Serrurier B, and Ventura-Clapier R (1999) Subcellular creatine kinase alterations. Implications in heart failure. Circ Res 85:68-76. (Pubitemid 29321043)
10. Dhar SK and St Clair DK (2012) Manganese superoxide dismutase regulation and cancer. Free Radic Biol Med 52:2209-2222.
11. Dignam JD, Martin PL, Shastry BS, and Roeder RG (1983) Eukaryotic gene transcription with purified components. Methods Enzymol 101:582-598. (Pubitemid 13071071)
12. Ewer MS and Suter TM (2010) Diagnostic aspects of cardiovascular toxicity of antitumor drugs, in Cardiotoxicity of Non-Cardiovascular Drugs (Minotti G ed) pp 201-221, John Wiley & Son Ltd, Padstow, UK.
13. Gianni L, Herman EH, Lipshultz SE, Minotti G, Sarvazyan N, and Sawyer DB (2008) Anthracycline cardiotoxicity: from bench to bedside. J Clin Oncol 26:3777-3784.
14. Institute of Laboratory Animal Resources (1996) Guide for the Care and Use of Laboratory Animals 7th ed. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, Washington, DC.
15. Kand'ár R, Záková P, Lotková H, Kucera O, and Cervinková Z (2007) Determination of reduced and oxidized glutathione in biological samples using liquid chromatography with fluorimetric detection. J Pharm Biomed Anal 43:1382-1387.
16. Keizer HG, Pinedo HM, Schuurhuis GJ, and Joenje H (1990) Doxorubicin (adriamycin): a critical review of free radical-dependent mechanisms of cytotoxicity. Pharmacol Ther 47:219-231. (Pubitemid 20228581)
17. Kwok JC and Richardson DR (2003) Anthracyclines induce accumulation of iron in ferritin in myocardial and neoplastic cells: inhibition of the ferritin iron mobilization pathway. Mol Pharmacol 63:849-861. (Pubitemid 36368992)
18. Kwok JC and Richardson DR (2004) Examination of the mechanism(s) involved in doxorubicin-mediated iron accumulation in ferritin: studies using metabolic inhibitors, protein synthesis inhibitors, and lysosomotropic agents. Mol Pharmacol 65:181-195. (Pubitemid 38113899)
19. Lebrecht D, Kirschner J, Geist A, Haberstroh J, and Walker UA (2010) Respiratory chain deficiency precedes the disrupted calcium homeostasis in chronic doxorubicin cardiomyopathy. Cardiovasc Pathol 19:e167-174.
20. Lebrecht D, Setzer B, Ketelsen UP, Haberstroh J, and Walker UA (2003) Time-dependent and tissue-specific accumulation of mtDNA and respiratory chain defects in chronic doxorubicin cardiomyopathy. Circulation 108:2423-2429. (Pubitemid 37413552)
21. Lebrecht D and Walker UA (2007) Role of mtDNA lesions in anthracycline cardiotoxicity. Cardiovasc Toxicol 7:108-113. (Pubitemid 47339856)
22. Li T and Singal PK (2000) Adriamycin-induced early changes in myocardial antioxidant enzymes and their modulation by probucol. Circulation 102:2105-2110.
23. Lim CC, Zuppinger C, Guo X, Kuster GM, Helmes M, Eppenberger HM, Suter TM, Liao R, and Sawyer DB (2004) Anthracyclines induce calpain-dependent titin proteolysis and necrosis in cardiomyocytes. J Biol Chem 279:8290-8299. (Pubitemid 38294721)
24. Lipshultz SE, Alvarez JA, and Scully RE (2008) Anthracycline associated cardiotoxicity in survivors of childhood cancer. Heart 94:525-533. (Pubitemid 351441417)
25. Long J, Ma J, Luo C, Mo X, Sun L, Zang W, and Liu J (2009) Comparison of two methods for assaying complex I activity in mitochondria isolated from rat liver, brain and heart. Life Sci 85:276-280.
26. Marechal X, Montaigne D, Marciniak C, Marchetti P, Hassoun SM, Beauvillain JC, Lancel S, and Neviere R (2011) Doxorubicin-induced cardiac dysfunction is attenuated by ciclosporin treatment in mice through improvements in mitochondrial bioenergetics. Clin Sci 121:405-413.
27. Menna P, Paz OG, Chello M, Covino E, Salvatorelli E, and Minotti G (2012) Anthracycline cardiotoxicity. Expert Opin Drug Saf 11 (Suppl 1):S21-S36.
28. Minotti G, Menna P, Salvatorelli E, Cairo G, and Gianni L (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229. (Pubitemid 38720829)
29. Miyagawa K, Emoto N, Widyantoro B, Nakayama K, Yagi K, Rikitake Y, Suzuki T, and Hirata K (2010) Attenuation of doxorubicin-induced cardiomyopathy by endothelin-converting enzyme-1 ablation through prevention of mitochondrial biogenesis impairment. Hypertension 55:738-746.
30. Ohkura K, Lee JD, Shimizu H, Nakano A, Uzui H, Horikoshi M, Fujibayashi Y, Yonekura Y, and Ueda T (2003) Mitochondrials complex I activity is reduced in latent adriamycin-induced cardiomyopathy of rat. Mol Cell Biochem 248:203-208. (Pubitemid 36833661)
31. Peers C and Steele DS (2012) Carbon monoxide: a vital signalling molecule and potent toxin in the myocardium. J Mol Cell Cardiol 52:359-365.
32. Piantadosi CA, Carraway MS, Babiker A, and Suliman HB (2008) Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 103:1232-1240.
33. Piantadosi CA and Suliman HB (2006) Mitochondrial transcription factor A induction by redox activation of nuclear respiratory factor 1. J Biol Chem 281:324-333. (Pubitemid 43671192)
34. Pilz J, Meineke I, and Gleiter CH (2000) Measurement of free and bound malondialdehyde in plasma by high-performance liquid chromatography as the 2,4-dinitrophenylhydrazine derivative. J Chromatogr B Biomed Sci Appl 742:315-325. (Pubitemid 30331049)
35. Popelová O, Štěrba M, Hasková P, Šimůnek T, Hroch M, Guncová I, Nachtigal P, Adamcová M, Geršl V, and Mazurová Y (2009) Dexrazoxane-afforded protection against chronic anthracycline cardiotoxicity in vivo: effective rescue of cardiomyocytes from apoptotic cell death. Br J Cancer 101:792-802.
36. Richard C, Ghibu S, Delemasure-Chalumeau S, Guilland JC, Des Rosiers C, Zeller M, Cottin Y, Rochette L, and Vergely C (2011) Oxidative stress and myocardial gene alterations associated with doxorubicin-induced cardiotoxicity in rats persist for 2 months after treatment cessation. J Pharmacol Exp Ther 339:807-814.
37. Rimbaud S, Garnier A, and Ventura-Clapier R (2009) Mitochondrial biogenesis in cardiac pathophysiology. Pharmacol Rep 61:131-138.
38. Sardão VA, Oliveira PJ, Holy J, Oliveira CR, and Wallace KB (2009) Doxorubicin-induced mitochondrial dysfunction is secondary to nuclear p53 activation in H9c2 cardiomyoblasts. Cancer Chemother Pharmacol 64:811-827.
39. Šimůnek T, Klimtová I, Kaplanová J, Mazurová Y, Adamcová M, Štěrba M, Hrdina R, and Gersl V (2004) Rabbit model for in vivo study of anthracycline-induced heart failure and for the evaluation of protective agents. Eur J Heart Fail 6:377-387. (Pubitemid 38746579)
40. Šimůnek T, Štěrba M, Popelová O, Adamcová M, Hrdina R, and Geršl V (2009) Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 61:154-171.
41. Soni H, Pandya G, Patel P, Acharya A, Jain M, and Mehta AA (2011) Beneficial effects of carbon monoxide-releasing molecule-2 (CORM-2) on acute doxorubicin cardiotoxicity in mice: role of oxidative stress and apoptosis. Toxicol Appl Pharmacol 253:70-80.
42. Štěrba M, Popelová O, Lenčo J, Fučíková A, Brčáková E, Mazurová Y, Jirkovský E, Šimůnek T, Adamcová M, Mičuda S, et al. (2011) Proteomic insights into chronic anthracycline cardiotoxicity. J Mol Cell Cardiol 50:849-862.
43. Suliman HB, Carraway MS, Ali AS, Reynolds CM, Welty-Wolf KE, and Piantadosi CA (2007) The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy. J Clin Invest 117:3730-3741. (Pubitemid 350224084)
44. Tokarska-Schlattner M, Zaugg M, Zuppinger C, Wallimann T, and Schlattner U (2006) New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics. J Mol Cell Cardiol 41:389-405. (Pubitemid 44362995)
45. Vávrová A, Popelová O, Štěrba M, Jirkovský E, Hašková P, Mertlíková- Kaiserová H, Geršl V, and Šimůnek T (2011) In vivo and in vitro assessment of the role of glutathione antioxidant system in anthracycline-induced cardiotoxicity. Arch Toxicol 85:525-535.
46. Velez JM, Miriyala S, Nithipongvanitch R, Noel T, Plabplueng CD, Oberley T, Jungsuwadee P, Van Remmen H, Vore M, and St Clair DK (2011) p53 regulates oxidative stress-mediated retrograde signaling: a novel mechanism for chemotherapy-induced cardiac injury. PLoS One 6:e18005.
47. Ventura-Clapier R, Garnier A, and Veksler V (2008) Transcriptional control of mitochondrial biogenesis: the central role of PGC-1α. Cardiovasc Res 79:208-217. (Pubitemid 351951611)
48. Wallace KB (2003) Doxorubicin-induced cardiac mitochondrionopathy. Pharmacol Toxicol 93:105-115.
49. Wallace KB (2007) Adriamycin-induced interference with cardiac mitochondrial calcium homeostasis. Cardiovasc Toxicol 7:101-107.