387
Views
29
CrossRef citations to date
0
Altmetric
Research Article

Ascorbic acid and N-acetyl cysteine prevent uncoupling of nitric oxide synthase and increase tolerance to ischemia/reperfusion injury in diabetic rat heart

, , , , &
Pages 1173-1183 | Received 19 May 2011, Accepted 11 Jul 2011, Published online: 10 Aug 2011

References

  • Stone PH, Muller JE, Hartwell T, . The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: contribution of both coronary disease and diastolic left ventricular dysfunction to the adverse prognosis. The MILIS Study Group. J Am Coll Cardiol 1989;14:49–57.
  • Lago RM, Nesto RW. Type 2 diabetes and coronary heart disease: focus on myocardial infarction. Curr Diab Rep 2009; 9:73–78.
  • Liu X, Wei J, Peng DH, Layne MD, Yet SF. Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 2005;54:778–784.
  • Luan R, Liu S, Yin T, . High glucose sensitizes adult cardiomyocytes to ischaemia/reperfusion injury through nitrative thioredoxin inactivation. Cardiovasc Res 2009;83: 294–302.
  • Bitar MS, Wahid S, Mustafa S, Al-Saleh E, Dhaunsi GS, Al-Mulla F. Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes. Eur J Pharmacol 2005;511:53–64.
  • Sasaki N, Yamashita T, Takaya T, . Augmentation of vascular remodeling by uncoupled endothelial nitric oxide synthase in a mouse model of diabetes mellitus. Arterioscler Thromb Vasc Biol 2008;28:1068–1076.
  • Landmesser U, Dikalov S, Price SR, . Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003; 111:1201–1209.
  • Mayer B, Hemmens B. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 1997;22:477–481.
  • Stuehr D, Pou S, Rosen GM. Oxygen reduction by nitric-oxide synthases. J Biol Chem 2001;276:14533–14536.
  • Otani H. The role of nitric oxide in myocardial repair and remodeling. Antioxid Redox Signal 2009;11:1913–1928.
  • Moens AL, Kass DA. Tetrahydrobiopterin and cardiovascular disease. Arterioscler Thromb Vasc Biol 2006;26: 2439–2444.
  • Soliman H, Craig GP, Nagareddy P, . Role of inducible nitric oxide synthase in induction of RhoA expression in hearts from diabetic rats. Cardiovasc Res 2008;79:322–330.
  • Okazaki T, Otani H, Shimazu T, . Reversal of inducible nitric oxide synthase uncoupling unmasks tolerance to ischemia/reperfusion injury in the diabetic rat heart. J Mol Cell Cardiol 2011;50:534–544.
  • Sun F, Iwaguchi K, Shudo R, . Change in tissue concentrations of lipid hydroperoxides, vitamin C and vitamin E in rats with streptozotocin-induced diabetes. Clin Sci (Lond) 1999;96:185–190.
  • Gumieniczek A, Hopkala H, Wojtowicz Z, Nikolajuk J. Changes in antioxidant status of heart muscle tissue in experimental diabetes in rabbits. Acta Biochim Pol 2002;49: 529–535.
  • Gumieniczek A. Modification of cardiac oxidative stress in alloxan-induced diabetic rabbits with repaglinide treatment. Life Sci 2005;78:259–263.
  • Xia Z, Nagareddy PR, Guo Z, Zhang W, McNeill JH. Antioxidant N-acetylcysteine restores systemic nitric oxide availability and corrects depressions in arterial blood pressure and heart rate in diabetic rats. Free Radic Res 2006;40:175–184.
  • Fiordaliso F, Bianchi R, Staszewsky L, . Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J Mol Cell Cardiol 2004;37:959–968.
  • Kido M, Otani H, Kyoi S, . Ischemic preconditioning-mediated restoration of membrane dystrophin during reperfusion correlates with protection against contraction-induced myocardial injury. Am J Physiol Heart Circ Physiol 2004;287:H81–H90.
  • Gao F, Yao CL, Gao E, . Enhancement of glutathione cardioprotection by ascorbic acid in myocardial reperfusion injury. J Pharmacol Exp Ther 2002;301:543–550.
  • Saini-Chohan HK, Dhalla NS. Attenuation of ischemia-reperfusion-induced alterations in intracellular Ca2+ in cardiomyocytes from hearts treated with N-acetylcysteine and N-mercaptopropionylglycine. Can J Physiol Pharmacol 2009; 87:1110–1119.
  • Hattori R, Otani H, Maulik N, Das DK. Pharmacological preconditioning with resveratrol: role of nitric oxide. Am J Physiol Heart Circ Physiol 2002;282:H1988–H1995.
  • Akita Y, Otani H, Matsuhisa S, . Exercise-induced activation of cardiac sympathetic nerve triggers cardioprotection via redox-sensitive activation of eNOS and upregulation of iNOS. Am J Physiol Heart Circ Physiol 2007;292: H2051–H2059.
  • Masano T, Kawashima S, Toh R, . Beneficial effects of exogenous tetrahydrobiopterin on left ventricular remodeling after myocardial infarction in rats: the possible role of oxidative stress caused by uncoupled endothelial nitric oxide synthase. Circ J 2008;72:1512–1519.
  • Jobgen WS, Jobgen SC, Li H, Meininger CJ, Wu G. Analysis of nitrite and nitrate in biological samples using high-performance liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 2007;851:71–82.
  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131–138.
  • Wang S, Xu J, Song P, Viollet B, Zou MH. In vivo activation of AMP-activated protein kinase attenuates diabetes-enhanced degradation of GTP cyclohydrolase I. Diabetes 2009;58: 1893–1901.
  • Xu J, Wu Y, Song P, Zhang M, Wang S, Zou MH. Proteasome-dependent degradation of guanosine 5′-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation 2007;116:944–953.
  • Jo H, Otani H, Jo F, . Inhibition of Nitric Oxide Synthase Uncoupling by Sepiapterin Improves Left Ventricular Function in Streptozotocin-induced Diabetic Mice. Clin Exp Pharmacol Physiol 2011;38:485–493.
  • Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001; 357:593–615.
  • Haramaki N, Stewart DB, Aggarwal S, Kawabata T, Packer L. Role of ascorbate in protection by nitecapone against cardiac ischemia-reperfusion injury. Biochem Pharmacol 1995;50: 839–843.
  • Sicard P, Oudot A, Guilland JC, Moreau D, Vergely C, Rochette L. Dissociation between vascular oxidative stress and cardiovascular function in Wistar Kyoto and spontaneously hypertensive rats. Vascul Pharmacol 2006;45:112–121.
  • Ferrari R, Ceconi C, Curello S, . Oxygen free radicals and myocardial damage: protective role of thiol-containing agents. Am J Med 1991;91:95S–105S.
  • Chen W, Gabel S, Steenbergen C, Murphy E. A redox-based mechanism for cardioprotection induced by ischemic preconditioning in perfused rat heart. Circ Res 1995;77:424–429.
  • Penna C, Rastaldo R, Mancardi D, . Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K+ channel and protein kinase C activation. Basic Res Cardiol 2006;101:180–189.
  • Otani H. Ischemic preconditioning: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2008;10:207–247.
  • Davis KL, Martin E, Turko IV, Murad F. Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 2001;41:203–236.
  • Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 1998;356:1–11.
  • Balafanova Z, Bolli R, Zhang J, . Nitric oxide (NO) induces nitration of protein kinase Cepsilon (PKCepsilon ), facilitating PKCepsilon translocation via enhanced PKCepsilon -RACK2 interactions: a novel mechanism of no-triggered activation of PKCepsilon. J Biol Chem 2002; 277:15021–15027.
  • Gray MO, Karliner JS, Mochly-Rosen D. A selective epsilon-protein kinase C antagonist inhibits protection of cardiac myocytes from hypoxia-induced cell death. J Biol Chem 1997;272:30945–30951.
  • Liu GS, Cohen MV, Mochly-Rosen D, Downey JM. Protein kinase C-epsilon is responsible for the protection of preconditioning in rabbit cardiomyocytes. J Mol Cell Cardiol 1999; 31:1937–1948.
  • Kukreja RC, Salloum F, Das A, . Pharmacological preconditioning with sildenafil: Basic mechanisms and clinical implications. Vascul Pharmacol 2005;42:219–232.
  • Handy DE, Loscalzo J. Nitric oxide and posttranslational modification of the vascular proteome: S-nitrosation of reactive thiols. Arterioscler Thromb Vasc Biol 2006;26:1207–1214.
  • Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005;6:150–166.
  • Martinez-Ruiz A, Lamas S. S-nitrosylation: a potential new paradigm in signal transduction. Cardiovasc Res 2004;62: 43–52.
  • Sun J, Steenbergen C, Murphy E. S-nitrosylation: NO-related redox signaling to protect against oxidative stress. Antioxid Redox Signal 2006;8:1693–1705.
  • Zimmet JM, Hare JM. Nitroso-redox interactions in the cardiovascular system. Circulation 2006;114:1531–1544.
  • Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, Murphy E. Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 2006;98: 403–411.
  • Sun J, Murphy E. Protein S-nitrosylation and cardioprotection. Circ Res;2010;106:285–296.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.