Diesterified Nitrone Rescues Nitroso-Redox Levels and Increases Myocyte Contraction Via Increased SR Ca2+ Handling

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Traynham, Christopher J ^a   Roof, Steve R ^a   Wang, Honglan ^a   Prosak, Robert A ^b   Tang, Lifei ^a   Viatchenko Karpinski, Serge ^a   Ho, Hsiang Ting ^b   Racoma, Ira O ^b   Catalano, Dominic J ^a   Huang, Xin ^a   Han, Yongbin ^b   Kim, Shang U ^b   Gyorke, Sandor ^a   Billman, George E ^a   Villamena, Frederick A ^b   Ziolo, Mark T ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 ETHOXY 2 OXOETHYL) 2 (ETHOXYCARBONYL) 3,4 DIHYDRO 2H PYRROLE 1 OXIDE; CALCIUM ION; LUCIGENIN; NITRONE; PHOSPHOLAMBAN; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; CELL FUNCTION; CELL ISOLATION; CHEMOLUMINESCENCE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; HEART INFARCTION; INCUBATION TIME; MOUSE; MUSCLE FIBER CONTRACTION; NONHUMAN; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; WESTERN BLOTTING;

ANIMALS; CALCIUM; ESTERIFICATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITROGEN OXIDES; OXIDATION-REDUCTION; SARCOPLASMIC RETICULUM; SPIN LABELS; SUPEROXIDES;

MUS;

EID: 84871659588     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052005     Document Type: Article

References (51)

1. Taylor AL, Ziesche S, Yancy C, Carson P, D'Agostino R Jr, et al. (2004) Combination of isosorbide dinitrate and hydralazine in blacks with heart failure. N Engl J Med 351: 2049-2057.
2. Hare JM, (2004) Nitroso-redox balance in the cardiovascular system. N Engl J Med 351: 2112-2114.
3. Cappola TP, Kass DA, Nelson GS, Berger RD, Rosas GO, et al. (2001) Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104: 2407-2411.
4. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, et al. (1999) Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 85: 357-363.
5. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, et al. (2003) Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41: 2164-2171.
6. Sam F, Kerstetter DL, Pimental DR, Mulukutla S, Tabaee A, et al. (2005) Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J Card Fail 11: 473-480.
7. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, et al. (2005) Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115: 1221-1231.
8. Ambrosio G, Zweier JL, Duilio C, Kuppusamy P, Santoro G, et al. (1993) Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem 268: 18532-18541.
9. Hare JM, Mangal B, Brown J, Fisher C Jr, Freudenberger R, et al. (2008) Impact of oxypurinol in patients with symptomatic heart failure. Results of the OPT-CHF study. J Am Coll Cardiol 51: 2301-2309.
10. Nediani C, Raimondi L, Borchi E, Cerbai E, (2010) Nitric oxide/reactive oxygen species generation and nitroso/redox imbalance in heart failure: from molecular mechanisms to therapeutic implications. Antioxid Redox Signal 14: 289-331.
11. Ziolo MT, Maier LS, Piacentino V, 3rd, Bossuyt J, Houser SR, et al (2004) Myocyte nitric oxide synthase 2 contributes to blunted beta-adrenergic response in failing human hearts by decreasing Ca2+ transients. Circulation 109: 1886-1891.
12. Damy T, Ratajczak P, Shah AM, Camors E, Marty I, et al. (2004) Increased neuronal nitric oxide synthase-derived NO production in the failing human heart. Lancet 363: 1365-1367.
13. Wildhirt SM, Weismueller S, Schulze C, Conrad N, Kornberg A, et al. (1999) Inducible nitric oxide synthase activation after ischemia/reperfusion contributes to myocardial dysfunction and extent of infarct size in rabbits: evidence for a late phase of nitric oxide-mediated reperfusion injury. Cardiovasc Res 43: 698-711.
14. Zuo L, Chen YR, Reyes LA, Lee HL, Chen CL, et al. (2009) The radical trap 5,5-dimethyl-1-pyrroline N-oxide exerts dose-dependent protection against myocardial ischemia-reperfusion injury through preservation of mitochondrial electron transport. J Pharmacol Exp Ther 329: 515-523.
15. Locigno EJ, Zweier JL, Villamena FA, (2005) Nitric oxide release from the unimolecular decomposition of the superoxide radical anion adduct of cyclic nitrones in aqueous medium. Org Biomol Chem 3: 3220-3227.
16. Floyd RA, Hensley K, (2000) Nitrone inhibition of age-associated oxidative damage. Ann N Y Acad Sci 899: 222-237.
17. Inanami O, Kuwabara M, (1995) a-Phenyl N-tert-butyl nitrone (PBN) increases the cortical cerebral blood flow by inhibiting the breakdown of nitric oxide in anesthetized rats. Free Radical Res 23: 33-39.
18. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, et al. (2002) Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416: 337-339.
19. Khan SA, Skaf MW, Harrison RW, Lee K, Minhas KM, et al. (2003) Nitric oxide regulation of myocardial contractility and calcium cycling: independent impact of neuronal and endothelial nitric oxide synthases. Circ Res 92: 1322-1329.
20. Gonzalez DR, Beigi F, Treuer AV, Hare JM, (2007) Deficient ryanodine receptor S-nitrosylation increases sarcoplasmic reticulum calcium leak and arrhythmogenesis in cardiomyocytes. Proc Natl Acad Sci U S A 104: 20612-20617.
21. Wang H, Kohr MJ, Traynham CJ, Wheeler DG, Janssen PM, et al. (2008) Neuronal nitric oxide synthase signaling within cardiac myocytes targets phospholamban. Am J Physiol Cell Physiol 294: C1566-1575.
22. Wang H, Viatchenko-Karpinski S, Sun J, Gyorke I, Benkusky NA, et al. (2010) Regulation of myocyte contraction via neuronal nitric oxide synthase: role of ryanodine receptor S-nitrosylation. J Physiol 588: 2905-2917.
23. Sears CE, Bryant SM, Ashley EA, Lygate CA, Rakovic S, et al. (2003) Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ Res 92: e52-59.
24. Zhang YH, Zhang MH, Sears CE, Emanuel K, Redwood C, et al. (2008) Reduced phospholamban phosphorylation is associated with impaired relaxation in left ventricular myocytes from neuronal NO synthase-deficient mice. Circ Res 102: 242-249.
25. Kinugawa S, Huang H, Wang Z, Kaminski PM, Wolin MS, et al. (2005) A defect of neuronal nitric oxide synthase increases xanthine oxidase-derived superoxide anion and attenuates the control of myocardial oxygen consumption by nitric oxide derived from endothelial nitric oxide synthase. Circ Res 96: 355-362.
26. Zhang YH, Dingle L, Hall R, Casadei B, (2009) The role of nitric oxide and reactive oxygen species in the positive inotropic response to mechanical stretch in the mammalian myocardium. Biochim Biophys Acta 1787: 811-817.
27. Khan SA, Lee K, Minhas KM, Gonzalez DR, Raju SV, et al. (2004) Neuronal nitric oxide synthase negatively regulates xanthine oxidoreductase inhibition of cardiac excitation-contraction coupling. Proc Natl Acad Sci U S A 101: 15944-15948.
28. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC, (1993) Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75: 1273-1286.
29. Billman GE, (2006) A comprehensive review and analysis of 25 years of data from an in vivo canine model of sudden cardiac death: implications for future anti-arrhythmic drug development. Pharmacol Ther 111: 808-835.
30. Belevych AE, Terentyev D, Viatchenko-Karpinski S, Terentyeva R, Sridhar A, et al. (2009) Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc Res 84: 387-395.
31. Ambrosio G, Zweier JL, Duilio C, Kuppusamy P, Santoro G, et al. (1993) Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem 268: 18532-18541.
32. Zima AV, Blatter LA, (2006) Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 71: 310-321.
33. Kuster GM, Lancel S, Zhang J, Communal C, Trucillo MP, et al. (2010) Redox-mediated reciprocal regulation of SERCA and Na+-Ca2+ exchanger contributes to sarcoplasmic reticulum Ca2+ depletion in cardiac myocytes. Free Radic Biol Med 48: 1182-1187.
34. Kogler H, Fraser H, McCune S, Altschuld R, Marban E, (2003) Disproportionate enhancement of myocardial contractility by the xanthine oxidase inhibitor oxypurinol in failing rat myocardium. Cardiovasc Res 59: 582-592.
35. Liu Y, Huang H, Xia W, Tang Y, Li H, et al. (2010) NADPH oxidase inhibition ameliorates cardiac dysfunction in rabbits with heart failure. Mol Cell Biochem 343: 143-153.
36. Saavedra WF, Paolocci N, St John ME, Skaf MW, Stewart GC, et al. (2002) Imbalance between xanthine oxidase and nitric oxide synthase signaling pathways underlies mechanoenergetic uncoupling in the failing heart. Circ Res 90: 297-304.
37. Gonzalez DR, Treuer AV, Castellanos J, Dulce RA, Hare JM (2010.) Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 285: 28938-28945.
38. Hare JM, Stamler JS, (2005) NO/redox disequilibrium in the failing heart and cardiovascular system. J Clin Invest 115: 509-517.
39. Villamena FA, (2010) Superoxide Radical Anion Adduct of 5,5-Dimethyl-1-pyrroline N-Oxide. 6: Redox Properties. J Phys Chem A 114: 1153-1160.
40. Villamena FA, Hadad CM, Zweier JL, (2005) Comparative DFT Study of the Spin Trapping of Methyl, Mercapto, Hydroperoxy, Superoxide, and Nitric Oxide Radicals by Various Substituted Cyclic Nitrones. J Phys Chem A 109: 1662-1674.
41. Villamena FA, (2009) Superoxide radical anion adduct of 5,5-dimethyl-1-pyrroline N-oxide. 5. Thermodynamics and kinetics of unimolecular decomposition. J Phys Chem A 113: 6398-6403.
42. Dawson D, Lygate CA, Zhang MH, Hulbert K, Neubauer S, et al. (2005) nNOS gene deletion exacerbates pathological left ventricular remodeling and functional deterioration after myocardial infarction. Circulation 112: 3729-3737.
43. Saraiva RM, Minhas KM, Raju SV, Barouch LA, Pitz E, et al. (2005) Deficiency of neuronal nitric oxide synthase increases mortality and cardiac remodeling after myocardial infarction: role of nitroso-redox equilibrium. Circulation 112: 3415-3422.
44. Zhang GX, Kimura S, Nishiyama A, Shokoji T, Rahman M, et al. (2005) Cardiac oxidative stress in acute and chronic isoproterenol-infused rats. Cardiovasc Res 65: 230-238.
45. Xie H, Zhu PH, (2006) Biphasic modulation of ryanodine receptors by sulfhydryl oxidation in rat ventricular myocytes. Biophys J 91: 2882-2891.
46. Kohr MJ, Kaludercic N, Tocchetti CG, Dong Gao W, Kass DA, et al. (2010) Nitroxyl enhances myocyte Ca2+ transients by exclusively targeting SR Ca2+-cycling. Front Biosci 2: 614-626.
47. Kohr MJ, Traynham CJ, Roof SR, Davis JP, Ziolo MT, (2010) cAMP-independent activation of protein kinase A by the peroxynitrite generator SIN-1 elicits positive inotropic effects in cardiomyocytes. J Mol Cell Cardiol 48: 645-648.
48. Roof SR, Biesiadecki BJ, Davis JP, Janssen PM, Ziolo MT (2012) Effects of increased systolic Ca(2+) and beta-adrenergic stimulation on Ca(2+) transient decline in NOS1 knockout cardiac myocytes. Nitric Oxide: In Press.
49. Roof SR, Shannon TR, Janssen PM, Ziolo MT, (2011) Effects of increased systolic Ca2+ and phospholamban phosphorylation during beta-adrenergic stimulation on Ca2+ transient kinetics in cardiac myocytes. Am J Physiol Heart Circ Physiol 301: H1570-1578.
50. Layland J, Li JM, Shah AM, (2002) Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes. J Physiol 540: 457-467.
51. Campbell DL, Stamler JS, Strauss HC, (1996) Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol 108: 277-293.