Zinc inhibits doxorubicin-activated calcineurin signal transduction pathway in H9c2 embryonic rat cardiac cells

Experimental Biology and Medicine

Volumn 232, Issue 5, 2007, Pages 682-689

  Merten, Kevyn E ^a   Jiang, Youchun ^a   Kang, Y James ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Calcineurin; Doxorubicin; H9c2 cells; Hypertrophy; Metallothionein; Zinc

Indexed keywords

CALCINEURIN; CYCLOSPORIN A; DOXORUBICIN; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; TACROLIMUS; TRANSCRIPTION FACTOR NFAT; ZINC; ZINC ION;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; EMBRYO CELL; HEART MUSCLE CELL; HYPERTROPHY; NONHUMAN; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CALCINEURIN; CELL LINE; CELL SIZE; CELL SURVIVAL; CHELATING AGENTS; CHLORIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; ETHYLENEDIAMINES; LUCIFERASES; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; RATS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; ZINC; ZINC COMPOUNDS;

RATTUS;

EID: 34247593860     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. Kang YJ, Chen Y, Yu A, Voss-McCowan M, Epstein PN. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J Clin Invest 100:1501-1506, 1997.
2. Kang YJ, Zhou ZX, Wang GW, Buridi A, Klein JB. Suppression by metallothionein of doxorubicin-induced cardiomyocyte apoptosis through inhibition of p38 mitogen-activated protein kinases. J Biol Chem 275:13690-13698, 2000.
3. Wang GW, Klein JB, Kang YJ. Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J Pharmacol Exp Ther 298:461-468, 2001.
4. Sun X, Zhou Z, Kang YJ. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res 61:3382-3387, 2001.
5. Ferrans VJ. Overview of cardiac pathology in relation to anthracycline cardiotoxicity. Cancer Treat Rep 62:955-961, 1978.
6. Kang YJ, Chen Y, Epstein PN. Suppression of doxorubicin cardiotoxicity by overexpression of catalase in the heart of transgenic mice. J Biol Chem 271:12610-12616, 1996.
7. Myers CE, McGuire WP, Liss RH, Ifrim I, Grotzinger K, Young RC. Adriamycin: the role of lipid peroxidation in cardiac toxicity and tumor response. Science 197:165-167, 1977.
8. Bachur NR, Gordon SL, Gee MV. A general mechanism for microsomal activation of quinone anticancer agents to free radicals. Cancer Res 38:1745-1750, 1978.
9. Davies KJ, Doroshow JH. Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem 261:3060-3067, 1986.
10. Jung K, Reszka R. Mitochondria as subcellular targets for clinically useful anthracyclines. Adv Drug Deliv Rev 49:87-105, 2001.
11. Kalyanaraman B, Sealy RC, Sinha BK. An electron spin resonance study of the reduction of peroxides by anthracycline semiquinones. Biochim Biophys Acta 799:270-275, 1984.
12. Hamer DH. Metallothionein. Annu Rev Biochem 55:913-951, 1986.
13. Thornalley PJ, Vasak M. Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim Biophys Acta 827:36-44, 1985.
14. Cai L, Klein JB, Kang YJ. Metallothionein inhibits peroxynitrite-induced DNA and lipoprotein damage. J Biol Chem 275:38957-38960, 2000.
15. Wang GW, Kang YJ. Inhibition of doxorubicin toxicity in cultured neonatal mouse cardiomyocytes with elevated metallothionein levels. J Pharmacol Exp Ther 288:938-944, 1999.
16. Kang YJ, Li G, Saari JT. Metallothionein inhibits ischemia-reperfusion injury in mouse heart. Am J Physiol 276:H993-H997, 1999.
17. Wu HY, Kang YJ. Inhibition of buthionine sulfoximine-enhanced doxorubicin toxicity in metallothionein overexpressing transgenic mouse heart. J Pharmacol Exp Ther 287:515-520, 1998.
18. Kang YJ. Metallothionein redox cycle and function. Exp Biol Med (Maywood) 231:1459-1467, 2006.
19. Maret W, Vallee BL. Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci U S A 95:3478-3482, 1998.
20. Hansson A. Extracellular zinc ions induces mitogen-activated protein kinase activity and protein tyrosine phosphorylation in bombesin-sensitive Swiss 3T3 fibroblasts. Arch Biochem Biophys 328:233-238, 1996.
21. Samet JM, Graves LM, Quay J, Dailey LA, Devlin RB, Ghio AJ, Wu W, Bromberg PA, Reed W. Activation of MAPKs in human bronchial epithelial cells exposed to metals. Am J Physiol 275:L551-L558, 1998.
22. Korichneva I, Hoyos B, Chua R, Levi E, Hammerling U. Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J Biol Chem 277:44327-44331, 2002.
23. Beyersmann D, Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 14:331-341, 2001.
24. Haase H, Maret W. Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Exp Cell Res 291:289-298, 2003.
25. Samet JM, Silbajoris R, Wu W, Graves LM. Tyrosine phosphatases as targets in metal-induced signaling in human airway epithelial cells. Am J Respir Cell Mol Biol 21:357-364, 1999.
26. Lengyel I, Fieuw-Makaroff S, Hall AL, Sim AT, Rostas JA, Dunkley PR. Modulation of the phosphorylation and activity of calcium/calmodulin-dependent protein kinase II by zinc. J Neurochem 75:594-605, 2000.
27. Kim S, Jung Y, Kim D, Koh H, Chung J. Extracellular zinc activates p70 S6 kinase through the phosphatidylinositol 3-kinase signaling pathway. J Biol Chem 275:25979-25984, 2000.
28. Takahashi K, Akaishi E, Abe Y, Ishikawa R, Tanaka S, Hosaka K, Kubohara Y. Zinc inhibits calcineurin activity in vitro by competing with nickel. Biochem Biophys Res Commun 307:64-68, 2003.
29. Wilkins BJ, Molkentin JD. Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem Biophys Res Commun 322:1178-1191, 2004.
30. Kalivendi SV, Konorev EA, Cunningham S, Vanamala SK, Kaji EH, Joseph J, Kalyanaraman B. Doxorubicin activates nuclear factor of activated T-lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium. Biochem J 389:527-539, 2005.
31. Merten KE, Jiang Y, Feng W, Kang YJ. Calcineurin activation is not necessary for doxorubicin-induced hypertrophy in H9c2 embryonic rat cardiac cells: involvement of the phosphoinositide 3-kinase-Akt pathway. J Pharmacol Exp Ther 319:934-940, 2006.
32. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228, 1998.
33. Truong-Tran AQ, Carter J, Ruffin RE, Zalewski PD. The role of zinc in caspase activation and apoptotic cell death. Biometals 14:315-330, 2001.
34. Maret W. Zinc coordination environments in proteins as redox sensors and signal transducers. Antioxid Redox Signal 8:1419-1441, 2006.
35. Malaiyandi LM, Dineley KE, Reynolds IJ. Divergent consequences arise from metallothionein overexpression in astrocytes: zinc buffering and oxidant-induced zinc release. Glia 45:346-353, 2004.
36. St Croix CM, Wasserloos KJ, Dineley KE, Reynolds IJ, Levitan ES, Pitt BR. Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. Am J Physiol Lung Cell Mol Physiol 282:L185-L192, 2002.
37. Krinks MH, Manalan AS, Klee CB. Calcineurin: a calmodulin regulated protein phosphatase. Fed Proc 42:2026, 1983.
38. Tanaka S, Akaishi E, Hosaka K, Okamura S, Kubohara Y. Zinc ions suppress mitogen-activated interleukin-2 production in Jurkat cells. Biochem Biophys Res Commun 335:162-167, 2005.
39. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94:110-118, 2004.
40. Koizumi S, Nakazawa K, Inoue K. Inhibition by Zn of uridine 5′-triphosphate-induced Ca-influx but not Ca-mobilization in rat phaechromocytoma cells. Br J Pharmacol 115:1502-1508, 1995.
41. Lambert JC, Wang GW, Kang YJ. Zinc inhibition of caspase-3 activation does not protect HeLa cells from apoptotic cell death. Toxicol Appl Pharmacol 175:89-93, 2001.
42. Youn HJ, Kim HS, Jeon MH, Lee JH, Seo YJ, Lee YJ, Lee JH. Induction of caspase-independent apoptosis in H9c2 cardiomyocytes by adriamycin treatment. Mol Cell Biochem 270:13-19, 2005.
43. Feng W, Cai J, Pierce WM, Franklin RB, Maret W, Benz FW, Kang YJ. Metallothionein transfers zinc to mitochondrial aconitase through a direct interaction in mouse hearts. Biochem Biophys Res Commun 332:853-858, 2005.
44. Merten KE, Feng W, Zhang L, Pierce W, Cai J, Klein JB, Kang YJ. Modulation of cytochrome C oxidase-va is possibly involved in metallothionein protection from doxorubicin cardiotoxicity. J Pharmacol Exp Ther 315:1314-1319, 2005.