Enhanced toxicity and ROS generation by doxorubicin in primary cultures of cardiomyocytes from neonatal metallothionein-I/II null mice

Toxicology in Vitro

Volumn 24, Issue 6, 2010, Pages 1584-1591

  Fu, Ze ^a   Guo, Jiabin ^a   Jing, Li ^a   Li, Ruisheng ^b   Zhang, Tingfen ^a   Peng, Shuangqing ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b BEIJING 302 HOSPITAL   (China)

Author keywords

Cardiomyocytes; Doxorubicin; Metallothionein; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; DOXORUBICIN; GLUTATHIONE; LACTATE DEHYDROGENASE; METALLOTHIONEIN I; METALLOTHIONEIN II; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARDIOTOXICITY; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; HEART MUSCLE CELL; MOUSE; NEWBORN; NONHUMAN;

ANIMALS; ANIMALS, NEWBORN; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; CELLS, CULTURED; DOXORUBICIN; L-LACTATE DEHYDROGENASE; METALLOTHIONEIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; REACTIVE OXYGEN SPECIES; TUMOR STEM CELL ASSAY;

MUS;

EID: 77956172973     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2010.06.009     Document Type: Article

References (48)

1. Bernuzzi F., Recalcati S., Alberghini A., Cairo G. Reactive oxygen species-independent apoptosis in doxorubicin-treated H9c2 cardiomyocytes: role for heme oxygenase-1 down-modulation. Chem. Biol. Interact. 2009, 177(1):12-20.
2. Buyukokuroglu M.E., Taysi S., Buyukavci M., Bakan E. Prevention of acute adriamycin cardiotoxicity by dantrolene in rats. Hum. Exp. Toxicol. 2004, 23(5):251-256.
3. DiSilvestro R.A., Liu J., Klaassen C.D. Transgenic mice overexpressing metallothionein are not resistant to adriamycin cardiotoxicity. Res. Commun. Mol. Pathol. Pharmacol. 1996, 93(2):163-170.
4. Eaton D.L., Cherian M.G. Determination of metallothionein in tissues by cadmium-hemoglobin affinity assay. Methods Enzymo. 1991, 205:83-88.
5. Feng W., Benz F.W., Cai J., Pierce W.M., Kang Y.J. Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J. Biol. Chem. 2006, 281(2):681-687.
6. Futakawa N., Kondoh M., Ueda S., Higashimoto M., Takiguchi M., Suzuki S., Sato M. Involvement of oxidative stress in the synthesis of metallothionein induced by mitochondrial inhibitors. Biol. Pharm. Bull. 2006, 29(10):2016-2020.
7. 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. 1999, 57(7):727-741.
8. Guo J.B., Chen L.J., Yan C.H., Yang H.Y., Peng S.Q. Metallothionein protection against doxorubicin-induced cardiac oxidative injuries. J. Toxicol. 2006, 6(20):364-366.
9. Kalyanaraman B., Joseph J., Kalivendi S., Wang S., Konorev E., Kotamraju S. Doxorubicin-induced apoptosis: implications in cardiotoxicity. Mol. Cell. Biochem. 2002, 234-235(1-2):119-124.
10. Kang Y.J., Chen Y., Yu A., Voss-McCowan M., Epstein P.N. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J. Clin. Invest. 1997, 100(6):1501-1506.
11. Kang Y.J., Li Y., Sun X., Sun X. Antiapoptotic effect and inhibition of ischemia/reperfusion-induced myocardial injury in metallothionein-overexpressing transgenic mice. Am. J. Pathol. 2003, 163(4):1579-1586.
12. Kang Y.J. Antioxidant defense against anthracycline cardiotoxicity by metallothionein. Cardiovasc. Toxicol. 2007, 7(2):95-100.
13. Kern J.C., Kehrer J.P. Free radicals and apoptosis: relationships with glutathione, thioredoxin, and the BCL family of proteins. Front. Biosci. 2005, 10:1727-1738.
14. Kimura T., Fujita I., Itoh N., Muto N., Nakanishi T., Takahashi K., Azuma J., Tanaka K. Metallothionein acts as a cytoprotectant against doxorubicin toxicity. J. Pharmacol. Exp. Ther. 2000, 292(1):299-302.
15. Klaassen C.D., Liu J., Diwan B.A. Metallothionein protection of cadmium toxicity. Toxicol. Appl. Pharmacol. 2009, 238(3):215-220.
16. Kotamraju S., Konorev E.A., Joseph J., Kalyanaraman B. Doxorubicin-induced apoptosis in endothelial cells and cardiomyocytes is ameliorated by nitrone spin traps and ebselen. Role of reactive oxygen and nitrogen species. J. Biol. Chem. 2000, 275(43):33585-33592.
17. Lebrecht D., Geist A., Ketelsen U.P., Haberstroh J., Setzer B., Walker U.A. Dexrazoxane prevents doxorubicin-induced long-term cardiotoxicity and protects myocardial mitochondria from genetic and functional lesions in rats. Br. J. Pharmacol. 2007, 151(6):771-778.
18. Li Q., Peng S., Sheng Z., Wang Y. Ofloxacin induces oxidative damage to joint chondrocytes of juvenile rabbit: excessive production of reactive oxygen species, lipid peroxidation and DNA damage. Eur. J. Pharmacol. 2010, 626(2-3):146-153.
19. Li T., Danelisen I., Bello-Klein A., Singal P.K. Effects of probucol on changes of antioxidant enzymes in adriamycin-induced cardiomyopathy in rats. Cardiovasc. Res. 2000, 46(3):523-530.
20. Licata S., Saponiero A., Mordente A., Minotti G. Doxorubicin metabolism and toxicity in human myocardium: role of cytoplasmic deglycosidation and carbonyl reduction. Chem. Res. Toxicol. 2000, 13(5):414-420.
21. Liu J.B., Wang Y.M., Peng S.Q., Han G., Dong Y.S., Yang H.Y., Yan C.H., Wang G.Q. Toxic effects of fusarium mycotoxin butenolide on rat myocardium and primary culture of cardiac myocytes. Toxicon 2007, 50(3):357-364.
22. Maret M. The function of zinc metallothionein: a link between cellular zinc and redox state. J. Nutr. 2000, 130:1455s-1458s.
23. McAuliffe J.J., Joseph B., Hughes E., Miles L., Vorhees .C.V. Metallothionein I, II deficient mice do not exhibit significantly worse long-term behavioral outcomes following neonatal hypoxia-ischemia: MT-I, II deficient mice have inherent behavioral impairments. Brain Res. 2008, 1190:175-185.
24. Menna P., Salvatorelli E., Minotti G. Cardiotoxicity of antitumor drugs. Chem. Res. Toxicol. 2008, 2(5):978-989.
25. 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(2):185-229.
26. Muller T., Schuckelt R., Jaenicke L. Evidence for radical species as intermediates in cadmium/zinc-metallothionein-dependent DNA damage in vitro. Environ. Health Perspect. 1994, 3:27-29.
27. Ngu T.T., Stillman M.J. Metalation of metallothioneins. IUBMB Life 2009, 61(4):438-446.
28. Olson R.D., Mushlin P.S. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 1990, 4(13):3076-3086.
29. Park E.S., Kim S.D., Lee M.H., Lee H.S., Lee I.S., Sung J.K., Yoon Y.S. Protective effects of N-acetylcysteine and selenium against doxorubicin toxicity in rats. J. Vet. Sci. 2003, 4(2):129-136.
30. 2 with sulfhydryl groups in HL-60 cells: zinc-metallothionein and other sites. Arch. Biochem. Biophys. 1996, 334(2):241-250.
31. Quiles J.L., Huertas J.R., Battino M., Mataix J., Ramirez-Tortosa M.C. Antioxidant nutrients and adriamycin toxicity. Toxicology 2002, 180(1):79-95.
32. Romero-Isart N., Vasak M. Advances in the structure and chemistry of metallothioneins. J. Inorg. Biochem. 2002, 88(3-4):388-396.
33. Sato M., Kondoh M. Recent studies on metallothionein: protection against toxicity of heavy metals and oxygen free radicals. Tohoku J. Exp. Med. 2002, 196(1):9-22.
34. Shibuya K., Nishimura N., Suzuki J.S., Tohyama C., Naganuma A., Satoh M. Role of metallothionein as a protective factor against radiation carcinogenesis. J. Toxicol. Sci. 2008, 33(5):651-655.
35. Shi R., Huang C.C., Aronstam R.S., Ercal N., Martin A., Huang Y.W. N-acetylcysteine amide decreases oxidative stress but not cell death induced by doxorubicin in H9c2 cardiomyocytes. BMC Pharmacol. 2009, 9:7.
36. Shuai Y., Guo J.B., Peng S.Q., Zhang L.S. Metallothionein inhibited Dox-induced cardiac apoptosis in mice. J. Sichuan Univ. (Med. Sci. Edi.) 2007, 38(4):620-623.
37. Simunek T., Sterba M., Popelova O., Adamcova M., Hrdina R., Gersl V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol. Rep. 2009, 61(1):154-171.
38. Singal P.K., Iliskovic N. Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 1998, 339(13):900-905.
39. Singal P.K., Li T., Kumar D., Danelisen I., Iliskovic N. Adriamycin-induced heart failure: mechanism and modulation. Mol. Cell. Biochem. 2000, 207(1-2):77-86.
40. Sun X., Zhou Z., Kang Y.J. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res. 2001, 61(8):3382-3387.
41. Takemura G., Fujiwara H. Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog. Cardiovasc. Dis. 2007, 49(5):330-352.
42. Thirumoorthy N., Manisenthil Kumar K.T., Shyam Sundar A., Panayappan L., Chatterjee M. Metallothionein: an overview. World J. Gastroenterol. 2007, 13(7):993-996.
43. Tokarska-Schlattner M., Wallimann T., Schlattner U. Alterations in myocardial energy metabolism induced by the anti-cancer drug doxorubicin. C. R. Biol. 2006, 329(9):657-668.
44. Umlauf J., Horky M. Molecular biology of doxorubicin-induced cardiomyopathy. Exp. Clin. Cardiol. 2002, 7(1):35-39.
45. 2 toxicity. Am. J. Physiol. 1999, 276(1 pt 2):167-175.
46. Wallace K.B. Doxorubicin induced cardiac mitochondrionopathy. Pharmacol. Toxicol. 2003, 93(3):105-115.
47. Xu M.F., Ho S., Qian Z.M., Tang P.L. Melatonin protects against cardiac toxicity of doxorubicin in rat. J. Pineal Res. 2001, 31(4):301-307.
48. Zhou Z., Sun X., Lambert J.C., Saari J.T., Kang Y.J. Metallothionein-independent zinc protection from alcoholic liver injury. Am. J. Pathol. 2002, 160(6):2267-2274.