Journal of Molecular and Cellular Cardiology
Volume 47, Issue 2 , Pages 228-237 , August 2009

Metallothionein alleviates oxidative stress-induced endoplasmic reticulum stress and myocardial dysfunction

  • Rui Guo

      Affiliations

    • Department of Biochemistry and Molecular Biology, Hebei University College of Life Sciences, Baoding 071002, China
    • Center for Cardiovascular Research and Alternative Medicine, University of Wyoming College of Health Sciences, Laramie, WY 82071 USA
  • ,
  • Heng Ma

      Affiliations

    • Center for Cardiovascular Research and Alternative Medicine, University of Wyoming College of Health Sciences, Laramie, WY 82071 USA
    • Department of Physiology, Fourth Military Medical University, Xi'an 710032, China
  • ,
  • Feng Gao

      Affiliations

    • Department of Physiology, Fourth Military Medical University, Xi'an 710032, China
  • ,
  • Li Zhong

      Affiliations

    • Department of Biochemistry and Molecular Biology, Hebei University College of Life Sciences, Baoding 071002, China
    • Thoracic Surgery and Lung Cancer Program, City of Hope and Beckman Research Institute, CA 91010, USA
  • ,
  • Jun Ren

      Affiliations

    • Center for Cardiovascular Research and Alternative Medicine, University of Wyoming College of Health Sciences, Laramie, WY 82071 USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 307 766 6131; fax: +1 307 766 2953.

Received 27 December 2008 ,Revised 16 March 2009 ,Accepted 24 March 2009.

References 

  1. Haynes CM, Titus EA, Cooper AA. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell. 2004 Sep 10;15(5):767–776
  2. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 2000 Apr 28;101(3):249–258
  3. Glembotski CC. Endoplasmic reticulum stress in the heart. Circ. Res. 2007 Nov 9;101(10):975–984
  4. Li SY, Ren J. Cardiac overexpression of alcohol dehydrogenase exacerbates chronic ethanol ingestion-induced myocardial dysfunction and hypertrophy: role of insulin signaling and ER stress. J. Mol. Cell. Cardiol. 2008 Jun;44(6):992–1001
  5. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006 Apr 13;440(7086):944–948
  6. Kaneto H, Katakami N, Kawamori D, Miyatsuka T, Sakamoto K, Matsuoka TA, et al. Involvement of oxidative stress in the pathogenesis of diabetes. Antioxid. Redox Signal. 2007 Mar;9(3):355–366
  7. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005 Oct;115(10):2656–2664
  8. Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J. Hypertens. 2000 Jun;18(6):655–673
  9. Malhotra JD, Miao H, Zhang K, Wolfson A, Pennathur S, Pipe SW, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. U. S. A. 2008 Nov 25;105(47):18525–18530
  10. Merksamer PI, Trusina A, Papa FR. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell. 2008 Nov 28;135(5):933–947
  11. Sagrista ML, Garcia AE, Africa De Madariaga M, Mora M. Antioxidant and pro-oxidant effect of the thiolic compounds N-acetyl-l-cysteine and glutathione against free radical-induced lipid peroxidation. Free Radic. Res. 2002 Mar;36(3):329–340
  12. Chakravarthi S, Jessop CE, Bulleid NJ. The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep. 2006 Mar;7(3):271–275
  13. Vaziri ND, Wang XQ, Oveisi F, Rad B. Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. Hypertension. 2000 Jul;36(1):142–146
  14. Ren J, Privratsky JR, Yang X, Dong F, Carlson EC. Metallothionein alleviates glutathione depletion-induced oxidative cardiomyopathy in murine hearts. Crit. Care Med. 2008 Jul;36(7):2106–2116
  15. Jain A, Martensson J, Mehta T, Krauss AN, Auld PA, Meister A. Ascorbic acid prevents oxidative stress in glutathione-deficient mice: effects on lung type 2 cell lamellar bodies, lung surfactant, and skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 1992 Jun 1;89(11):5093–5097
  16. 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. 1997 Sep 15;100(6):1501–1506
  17. Aberle IN, Ren J. Experimental assessment of the role of acetaldehyde in alcoholic cardiomyopathy. Biol. Proced. Online. 2003;5:1–12
  18. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969 Mar;27(3):502–522
  19. Zhang X, Azhar G, Nagano K, Wei JY. Differential vulnerability to oxidative stress in rat cardiac myocytes versus fibroblasts. J. Am. Coll. Cardiol. 2001 Dec;38(7):2055–2062
  20. Robin E, Guzy RD, Loor G, Iwase H, Waypa GB, Marks JD, et al. Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion. J Biol. Chem. 2007 Jun 29;282(26):19133–19143
  21. Denk GU, Hohenester S, Wimmer R, Bohland C, Rust C, Beuers U. Role of mitogen-activated protein kinases in tauroursodeoxycholic acid-induced bile formation in cholestatic rat liver. Hepatol. Res. 2008 Jul;38(7):717–726
  22. Privratsky JR, Wold LE, Sowers JR, Quinn MT, Ren J. AT1 blockade prevents glucose-induced cardiac dysfunction in ventricular myocytes: role of the AT1 receptor and NADPH oxidase. Hypertension. 2003 Aug;42(2):206–212
  23. Li SY, Gomelsky M, Duan J, Zhang Z, Gomelsky L, Zhang X, et al. Overexpression of aldehyde dehydrogenase-2 (ALDH2) transgene prevents acetaldehyde-induced cell injury in human umbilical vein endothelial cells: role of ERK and p38 mitogen-activated protein kinase. J. Biol. Chem. 2004 Mar 19;279(12):11244–11252
  24. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976 May 7;72:248–254
  25. Ren J, Wold LE. Measurement of cardiac mechanical function in isolated ventricular myocytes from rats and mice by computerized video-based imaging. Biol. Proced. Online. 2001 Dec 11;3:43–53
  26. Verma S, Yuen VG, Badiwala M, Anderson TJ, McNeill JH. Working heart function in diabetes is not improved by spironolactone treatment. Can. J. Physiol. Pharmacol. 2003 May;81(5):493–496
  27. Esberg LB, Ren J. The oxygen radical generator pyrogallol impairs cardiomyocyte contractile function via a superoxide and p38 MAP kinase-dependent pathway: protection by anisodamine and tetramethylpyrazine. Cardiovasc. Toxicol. 2004;4(4):375–384
  28. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 2007 Dec;9(12):2277–2293
  29. Holtz WA, Turetzky JM, Jong YJ, O'Malley KL. Oxidative stress-triggered unfolded protein response is upstream of intrinsic cell death evoked by parkinsonian mimetics. J. Neurochem. 2006 Oct;99(1):54–69
  30. Yamamuro A, Yoshioka Y, Ogita K, Maeda S. Involvement of endoplasmic reticulum stress on the cell death induced by 6-hydroxydopamine in human neuroblastoma SH-SY5Y cells. Neurochem. Res. 2006 May;31(5):657–664
  31. Haidara K, Moffatt P, Denizeau F. Metallothionein induction attenuates the effects of glutathione depletors in rat hepatocytes. Toxicol. Sci. 1999 Jun;49(2):297–305
  32. Zhou G, Li X, Hein DW, Xiang X, Marshall JP, Prabhu SD, et al. Metallothionein suppresses angiotensin II-induced nicotinamide adenine dinucleotide phosphate oxidase activation, nitrosative stress, apoptosis, and pathological remodeling in the diabetic heart. J. Am. Coll. Cardiol. 2008 Aug 19;52(8):655–666
  33. Yokouchi M, Hiramatsu N, Hayakawa K, Okamura M, Du S, Kasai A, et al. Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J. Biol. Chem. 2008 Feb 15;283(7):4252–4260
  34. Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007 Dec;18(6):716–731
  35. Morris JA, Dorner AJ, Edwards CA, Hendershot LM, Kaufman RJ. Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J. Biol. Chem. 1997 Feb 14;272(7):4327–4334
  36. Buck TM, Wright CM, Brodsky JL. The activities and function of molecular chaperones in the endoplasmic reticulum. Semin. Cell Dev. Biol. 2007 Dec;18(6):751–761
  37. Waser M, Mesaeli N, Spencer C, Michalak M. Regulation of calreticulin gene expression by calcium. J. Cell Biol. 1997 Aug 11;138(3):547–557
  38. Ihara Y, Kageyama K, Kondo T. Overexpression of calreticulin sensitizes SERCA2a to oxidative stress. Biochem. Biophys. Res. Commun. 2005 Apr 22;329(4):1343–1349

PII: S0022-2828(09)00143-6

doi: 10.1016/j.yjmcc.2009.03.018

Journal of Molecular and Cellular Cardiology
Volume 47, Issue 2 , Pages 228-237 , August 2009