Journal of Molecular and Cellular Cardiology
Volume 49, Issue 1 , Pages 41-47 , July 2010

The critical role of intracellular zinc in adenosine A2 receptor activation induced cardioprotection against reperfusion injury

  • Rachel McIntosh

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • These authors contributed equally to this work.
    • ,
  • SungRyul Lee

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • These authors contributed equally to this work.
    • ,
  • Andrew J. Ghio

      Affiliations

    • Human Studies Division, US Environmental Protection Agency, Chapel Hill, NC 27599, USA
    • These authors contributed equally to this work.
    • ,
  • Jinkun Xi

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • ,
  • Min Zhu

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • ,
  • Xiangjun Shen

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • ,
  • Guillaume Chanoit

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • ,
  • David A. Zvara

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • ,
  • Zhelong Xu

      Affiliations

    • Department of Anesthesiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 919 843 4174.

Received 14 October 2009 ,Revised 26 January 2010 ,Accepted 1 February 2010.

References 

  1. Zhao Z-Q, Sato H, Williams MW, Fernandez AZ, Vinten-Johansen J. Adenosine A2-receptor activation inhibits neutrophil-mediated injury to coronary endothelium. Am J Physiol. 1996;271:H1456–H1464
  2. Jordan JE, Zhao Z-Q, Sato H, Taft S, Vinten-Johansen J. Adenosine A2 receptor activation attenuates reperfusion injury by inhibiting neutrophil accumulation, superoxide generation and coronary endothelial adherence. J Pharmacol Exp Ther. 1997;280:301–309
  3. Philipp S, Yang X-M, Cui L, Davis AM, Downey JM, Cohen MV. Postconditioning protects rabbit hearts through a protein kinase C-adenosine A2b receptor cascade. Cardiovasc Res. 2006;70:308–314
  4. Kuno A, Critz SD, Cui L, Solodushko V, Yang X-M, Krahn T, et al. Protein kinase C protects preconditioned rabbit hearts by increasing sensitivity of adenosine A2b-dependent signaling during early reperfusion. J Mol Cell Cardiol. 2007;43:262–271
  5. Berg JM, Shi Y. The galvanization of biology: a growing appreciation for the roles of zinc. Science. 1996;271:1081–1085
  6. Barthel A, Ostrakhovitch EA, Walter PL, Kampkötter A, Klotz L-O. Stimulation of phosphoinositide 3-kinase/Akt signaling by copper and zinc ions: mechanisms and consequences. Arch Biochem Biophys. 2007;463:175–182
  7. An W-L, Pei J-J, Nishimura T, Winblad B, Cowburn RF. Zinc-induced anti-apoptotic effects in SH-SY5Y neuroblastoma cells via the extracellular signal-regulated kinase 1/2. Brain Res Mol Brain Res. 2005;135:40–47
  8. Ilouz R, Kaidanovich O, Gurwitz D, Eldar-Finkelman H. Inhibition of glycogen synthase kinase-3β by bivalent zinc ions: insight into the insulin-mimetic action of zinc. Biochem Biophys Res Commun. 2002;295:102–106
  9. Chanoit G, Lee S, Xi J, Zhu M, McIntosh RA, Mueller RA, et al. Exogenous zinc protects cardiac cells from reperfusion injury by targeting mitochondrial permeability transition pore through inactivation of glycogen synthase kinase-3β. Am J Physiol. 2008;295:H1227–H1233
  10. Lee S, Chanoit G, McIntosh RA, Zvara DA, Xu Z. The molecular mechanism underlying Akt activation in zinc-induced cardioprotection. Am J Physiol. 2009;297:H569–H575
  11. Jang Y, Wang H, Xi J, Mueller RA, Norfleet EA, Xu Z. NO mobilizes intracellular Zn2+ via cGMP/PKG signaling pathway and prevents mitochondrial oxidant damage in cardiomyocytes. Cardiovasc Res. 2007;75:426–433
  12. Karagulova G, Yue Y, Moreyra A, Boutjdir M, Korichneva I. Protective role of intracellular zinc in myocardial ischemia/reperfusion is associated with preservation of protein kinase C isoforms. J Pharmacol Exp Ther. 2007;321:517–525
  13. Xu Z, Park SS, Mueller RA, Bagnell RC, Patterson C, Boysen PG. Adenosine produces nitric oxide and prevents mitochondrial oxidant damage in rat cardiomyocytes. Cardiovasc Res. 2005;65:803–812
  14. Baines CP, Zhang J, Wang GW, Zheng YT, Xiu JX, Cardwell EM, et al. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon–MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res. 2002;90:390–397
  15. Deng Z, Dailey L, Soukup J, Stonehuerner J, Richards J, Callaghan K, et al. Zinc transport by respiratory epithelial cells and interaction with iron homeostasis. BioMetals. 2009;
  16. Wang G, Liem DA, Vondriska TM, Honda HM, Korge P, Pantaleon DM, et al. Nitric oxide donors protect the murine myocardium against infarction via modulation of mitochondrial permeability transition. Am J Physiol. 2005;288:H1290–H1295
  17. Viola HM, Arthur PG, Hool LC. Evidence for regulation of mitochondrial function by the L-type Ca2+ channel in ventricular myocytes. J Mol Cell Cardiol. 2009;46:1016–1026
  18. Yang XM, Krieg T, Cui L, Downey JM, Cohen MV. NECA and bradykinin at reperfusion reduce infarction in rabbit hearts by signaling through PI3K, ERK, and NO. J Mol Cell Cardiol. 2004;36:411–421
  19. Förster K, Paul I, Solenkova N, Staudt A, Cohen M, Downey J, et al. NECA at reperfusion limits infarction and inhibits formation of the mitochondrial permeability transition pore by activating p70S6 kinase. Basic Res Cardiol. 2006;101:319–326
  20. Xu Z, Downey JM, Cohen MV. AMP 579 reduces contracture and limits infarction in rabbit heart by activating adenosine A2 receptors. J Cardiovasc Pharmacol. 2001;38:474–481
  21. Kuno A, Solenkova NV, Solodushko V, Dost T, Liu Y, Yang X-M, et al. Infarct limitation by a protein kinase G activator at reperfusion in rabbit hearts is dependent on sensitizing the heart to A2b agonists by protein kinase C. Am J Physiol. 2008;295:H1288–H1295
  22. Xi J, McIntosh RA, Shen X, Lee S, Chanoit G, Criswell H, et al. Adenosine A2A and A2B receptors work in concert to induce a strong protection against reperfusion injury in rat hearts. J Mol Cell Cardiol. 2009;47:684–690
  23. Morrison RR, Tan XL, Ledent C, Mustafa SJ, Hofmann PA. Targeted deletion of A2A adenosine receptors attenuates the protective effects of myocardial postconditioning. Am J Physiol. 2007;293:H2523–H2529
  24. Rork TH, Wallace KL, Kennedy DP, Marshall MA, Lankford AR, Linden J. Adenosine A2A receptor activation reduces infarct size in the isolated, perfused mouse heart by inhibiting resident cardiac mast cell degranulation. Am J Physiol. 2008;295:H1825–H1833
  25. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia–reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res. 2004;61:448–460
  26. Beyersmann D, Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals. 2001;14:331–341
  27. Liuzzi JP, Cousins RJ. Mammalian zinc transporters. Annu Rev Nutr. 2004;24:151–172
  28. Masaaki M, Toshio H. Intracellular zinc homeostasis and zinc signaling. Cancer Sci. 2008;99:1515–1522
  29. Powell SR, Hall D, Aiuto L, Wapnir RA, Teichberg S, Tortolani AJ. Zinc improves postischemic recovery of isolated rat hearts through inhibition of oxidative stress. Am J Physiol. 1994;266:H2497–H2507
  30. Sensi SL, Ton-That D, Sullivan PG, Jonas EA, Gee KR, Kaczmarek LK, et al. Modulation of mitochondrial function by endogenous Zn2+ pools. Proc Natl Acad Sci USA. 2003;100:6157–6162
  31. Korichneva I. Zinc dynamics in the myocardial redox signaling network. Antioxid Redox Signal. 2006;8:1707–1721
  32. Nishihara M, Miura T, Miki T, Tanno M, Yano T, Naitoh K, et al. Modulation of the mitochondrial permeability transition pore complex in GSK-3β-mediated myocardial protection. J Mol Cell Cardiol. 2007;43:564–570
  33. Brown AM, Kristal BS, Effron MS, Shestopalov AI, Ullucci PA, Sheu KFR, et al. Zn2+ inhibits alpha-ketoglutarate-stimulated mitochondrial respiration and the isolated alpha-ketoglutarate dehydrogenase complex. J Biol Chem. 2000;275:13441–13447
  34. Michele L, Tiziana C, Anna Maria S, Michele M, Francesco B, Sergio P. Interaction of Zn2+ with the bovine-heart mitochondrial bc1 complex. Eur J Biochem. 1991;197:555–561
  35. Sharpley MS, Hirst J. The inhibition of mitochondrial complex I (NADH:ubiquinone oxidoreductase) by Zn2+. J Biol Chem. 2006;281:34803–34809

PII: S0022-2828(10)00035-0

doi: 10.1016/j.yjmcc.2010.02.001

Journal of Molecular and Cellular Cardiology
Volume 49, Issue 1 , Pages 41-47 , July 2010

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