Nitric oxide and excitation-contraction coupling

Journal of Molecular and Cellular Cardiology

Volumn 35, Issue 7, 2003, Pages 719-729

  Hare, Joshua M ^a  

^a JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM CHANNEL L TYPE; CELL SURFACE RECEPTOR; ISOPROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RYANODINE RECEPTOR;

BIOCHEMISTRY; CALCIUM TRANSPORT; CAVEOLA; CELL COMPARTMENTALIZATION; CELL METABOLISM; ENZYME LOCALIZATION; EVIDENCE BASED MEDICINE; EXCITATION CONTRACTION COUPLING; HEART MITOCHONDRION; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION;

EID: 0037785375     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2828(03)00143-3     Document Type: Review

References (116)

1. Bers D.M. Cardiac excitation-contraction coupling. Nature. 415:2002;198-205.
2. Bers D.M. Calcium and cardiac rhythms: physiological and pathophysiological. Circ Res. 90:(1):2002;14-17.
3. Hobai I.A., O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation. 103:2001;1577-1584.
4. Hobai I.A., O'Rourke B. Enhanced Ca(2+)-activated Na(+)-Ca(2+) exchange activity in canine pacing-induced heart failure. Circ Res. 87:2000;690-698.
5. Schuh K., Uldrijan S., Telkamp M., Rothlein N., Neyses L. The plasmamembrane calmodulin-dependent calcium pump: a major regulator of nitric oxide synthase I. J Cell Biol. 155:(2):2001;201-205.
6. Michel T., Feron O. Nitric oxide synthases: which, where, how and why? J Clin Invest. 100:1997;2146-2152.
7. Xu K.Y., Huso D.L., Dawson T., Bredt D.S., Becker L.C. NO synthase in cardiac sarcoplasmic reticulum. Proc Natl Acad Sci USA. 96:1999;657-662.
8. DeBelder A.J., Radomski M., Why H.J.F., Richardson P.J., Bucknall C.A., Salas E., et al. Nitric oxide synthase activities in human myocardium. Lancet. 341:1993;84-85.
9. Balligand J.-L., Kobzik L., Han X., Kaye D.M., Belhassen L., O'Hara D.S., et al. Nitric oxide-dependent parasympathetic signaling is due to activation of constitutive endothelial (type III) nitric oxide synthase in cardiac myocytes. J Biol Chem. 270:1995;14582-14586.
10. Balligand J.-L., Ungureanu-Longrois D., Simmons W.W., Pimental D., Malinski T.A., Kapturczak M., et al. Cytokine-inducible nitric-oxide synthase (iNOS) expression in cardiac myocytes: characterization and regulation of iNOS expression and detection of iNOS activity in single cardiac myocytes in vitro. J Biol Chem. 269:1994;27580-27588.
11. Senzaki H., Smith C.J., Juang G.J., Isoda T., Mayer S.P., Ohler A., et al. Cardiac phosphodiesterase 5 (cGMP-specific) modulates beta-adrenergic signaling in vivo and is down-regulated in heart failure. FASEB J. 15:2001;1718-1726.
12. Stamler J.S., Lamas S., Fang F.C. Nitrosylation. The prototypic redox-based signaling mechanism. Cell. 106:2001;675-683.
13. Wink D.A., Mitchell J.B. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Rad Biol M. 25:1998;434-456.
14. Layland J., Li J.M., Shah A.M. Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes. J Physiol. (Pt 2 VI):2002;457-467.
15. Campbell D.L., Stamler J.S., Strauss H.C. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol. 108:1996;277-293.
16. Sun J., Xin C., Eu J.P., Stamler J.S., Meissner G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc Natl Acad Sci USA. 98:(20):2001;11158-11162.
17. Wink D.A., Cook J.A., Kim S.Y., Vodovotz Y., Pacelli R., Krishna M.C., et al. Superoxide modulates the oxidation and nitrosation of thiols by nitric oxide-derived reactive intermediates. J Biol Chem. 272:1997;11147-11151.
18. Scharfstein J.S., Keaney J.F. Jr, Slivka A., Welch G.N., Vita J., Stamler J.S., et al. In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J Clin Invest. 94:1994;1432-1439.
19. Stamler J.S., Jaraki O., Osborne J., Simon D.I., Keaney J.F. Jr, Vita J., et al. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA. 89:1992;7674-7677.
20. Simon D.I., Mullins M.E., Jia L., Gaston B., Singel D.J., Stamler J.S. Polynitrosylated proteins: characterization, bioactivity, and functional consequences. Proc Natl Acad Sci USA. 93:1996;4736-4741.
21. Xu L., Eu J.P., Meissner G., Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science. 279:1998;234-237.
22. 2 sensor and NO signaling functions. Cell. 102:2000;499-509.
23. Sun J., Xin C., Eu J.P., Stamler J.S., Meissner G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc Natl Acad Sci USA. 98:2001;11158-11162.
24. Liu L., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature. 410:2001;490-494.
25. Chesnais J.M., Fischmeister R., Mery P.F. Positive and negative inotropic effects of NO donors in atrial and ventricular fibres of the frog heart. J Physiol. 518:(Pt 2):1999;449-461.
26. Paolocci N., Ekelund U.E.G., Isoda T., Ozaki M., Vandegaer K., Georgakopoulos D., et al. cGMP-independent inotropic effect of nitric oxide and peroxynitirite donors: potential role for S-nitrosylation. Am J Physiol. 279:2000;H1982-H1988.
27. Muller-Strahl G., Kottenberg K., Zimmer H.G., Noack E., Kojda G. Inhibition of nitric oxide synthase augments the positive inotropic effect of nitric oxide donors in the rat heart. J Physiol. 522:(Pt 2):2000;311-320.
28. Preckel B., Kojda G., Schlack W., Ebel D., Kottenberg K., Noack E., et al. Inotropic effects of glyceryl trinitrate and spontaneous NO donors in the dog heart. Circulation. 96:1997;2675-2682.
29. Hare J.M., Colucci W.S. Role of nitric oxide in the regulation of myocardial function. Prog Cardiovasc Dis. 38:(2):1995;155-166.
30. Hare J.M., Stamler J.S. NOS: modulator, not mediator of cardiac performance. Nat M. 5:1999;273-274.
31. Hare J.M., Loh E., Creager M.A., Colucci W.S. Nitric oxide inhibits the contractile response to β-adrenergic stimulation in humans with left ventricular dysfunction. Circulation. 92:1995;2198-2203.
32. Hare J.M., Lofthouse R.A., Juang G.J., Colman L., Ricker K.M., Kim B., et al. Contribution of caveolin protein abundance to augmented nitric oxide signaling in conscious dogs with pacing-induced heart failure. Circ Res. 86:2000;1085-1092.
33. 2+ in intact cardiac myocytes. Circ Res. 74:1994;970-978.
34. Zieman S.J., Gerstenblith G., Lakatta E.G., Rosas G.O., Vandegaer K., Ricker K.M., et al. Upregulation of the nitric oxide-cGMP pathway in aged myocardium: physiological response to L-arginine. Circ Res. 88:2001;97-102.
35. Recchia F.A., McConnell P.I., Bernstein R.D., Vogel T.R., Xu X., Hintze T.H. Reduced nitric oxide production and altered myocardial metabolism during the decompensation of pacing-induced heart failure in the conscious dog. Circ Res. 83:1998;969-979.
36. Saavedra W.F., Paolocci N., St John M.E., Skaf M.W., Stewart G.C., Xie J.S., et al. Imbalance between xanthine oxidase and nitric oxide synthase signaling pathways underlies mechanoenergetic uncoupling in the failing heart. Circ Res. 90:(3):2002;297-304.
37. Clementi E., Brown G.C., Feelisch M., Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA. 95:1998;7631-7636.
38. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 377:1995;239-242.
39. Gyurko R., Kuhlencordt P., Fishman M.C., Huang P.L. Modulation of mouse cardiac function in vivo by eNOS and ANP. Am J Physiol Heart Circ Physiol. 278:2000;H971-H981.
40. Varghese P., Harrison R.W., Lofthouse R.A., Georgakopoulos D., Berkowitz D.E., Hare J.M. Beta(3)-adrenoceptor deficiency blocks nitric oxide-dependent inhibition of myocardial contractility. J Clin Invest. 106:2000;697-703.
41. Keaney J.F. Jr, Hare J.M., Kelly R.A., Loscalzo J., Smith T.W., Colucci W.S. Inhibition of nitric oxide synthase potentiates the positive inotropic response to β-adrenergic stimulation in normal dogs. Am J Physiol. 271:1996;H2646-H2652.
42. Pinsky D., Patton S., Mesaros S., Brovkovych V., Kubaszewski E., Grunfeld S., et al. Mechanical transduction of nitric oxide synthesis in the beating heart. Circ Res. 81:1997;372-379.
43. Kanai A.J., Mesaros S., Finkel M.S., Oddis C.V., Birder L.A., Malinski T. Beta-adrenergic regulation of constitutive nitric oxide synthase in cardiac myocytes. Am J Physiol. 273:(4Pt 1):1997;C1371-C1377.
44. Kojda G., Kottenberg K., Nix P., Schluter K.D., Piper H.M., Noack E. Low increase in cGMP induced by organic nitrates and nitrovasodilators improves contractile response of rat ventricular myocytes. Circ Res. 78:1996;91-101.
45. Brady A.J.B., Warren J.B., Poole-Wilson P.A., Williams T.J., Harding S.E. Nitric oxide attenuates cardiac myocyte contraction. Am J Physiol. 265:1993;H176-H182.
46. 2+ current is preserved in mice lacking endothelial nitric oxide synthase. Nat M. 5:1999;331-334.
47. Mohan P., Brutsaert D.L., Paulus W.J. Myocardial contractile response to nitric oxide and cGMP. Circulation. 93:1996;1223-1229.
48. Ziolo M.T., Katoh H., Bers D.M. Positive and negative effects of nitric oxide on Ca(2+) sparks: influence of beta-adrenergic stimulation. Am J Physiol Heart Circ Physiol. 281:(6):2001;H2295-H2303.
49. Hare J.M., Kim B., Flavahan N.A., Ricker K.M., Peng X., Colman L., et al. Pertussis toxin-sensitive G proteins influence nitric oxide synthase III activity and protein levels in rat heart. J Clin Invest. 101:1998;1424-1431.
50. Barouch L.A., Harrison R.W., Skaf M.W., Rosas G.O., Cappola T.P., Kobeissi Z.A., et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 416:2002;337-340.
51. Feron O., Smith T.W., Michel T., Kelly R.A. Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J Biol Chem. 272:1997;17744-17748.
52. Feron O., Saldana F., Michel J.B., Michel T. The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem. 273:1998;3125-3128.
53. Fulton D., Gratton J.P., McCabe T.J., Fontana J., Fujio Y., Walsh K., et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt [published erratum appears in Nature 1999 August 19;400(6746):792]. Nature. 399:1999 June 10;597-601.
54. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R., Zeiher A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 399:1999;601-605.
55. George W.J., Wilkerson R.D., Kadowitz P.J. Influence of acetylcholine on contractile force and cyclic nucleotide levels in the isolated perfused rat heart. J Pharmacol Exp Ther. 184:1973;228-235.
56. Shah A.M., Lewis M.J., Henderson A.H. Effects of 8-bromo-cyclic GMP on contraction and on inotropic response of ferret cardiac muscle. J Mol Cell Cardiol. 23:1991;55-64.
57. Han X., Shimoni Y., Giles W.R. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J Physiol. 476:(2):1994;309-314.
58. Han X., Shimoni Y., Giles W.R. A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J Gen Physiol. 106:1995;45-65.
59. Ca by carbachol and sodium nitroprusside. Pflugers Arch. 426:1994;419-426.
60. Kobzik L., Reid M.B., Bredt D.S., Stamler J.S. Nitric oxide in skeletal muscle. Nature. 372:1994;546-548.
61. Bredt D., Snyder S. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA. 87:1990;682-685.
62. Gonzalez-Cadavid N.F., Burnett A.L., Magee T.R., Zeller C.B., Vernet D., Smith N., et al. Expression of penile neuronal nitric oxide synthase variants in the rat and mouse penile nerves. Biol Reprod. 63:2000;704-714.
63. Stamler J.S., Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev. 81:2001;209-237.
64. Wang Y., Newton D.C., Robb G.B., Kau C.L., Miller T.L., Cheung A.H., et al. RNA diversity has profound effects on the translation of neuronal nitric oxide synthase. Proc Natl Acad Sci USA. 96:1999;12150-12155.
65. Wang Y., Newton D.C., Marsden P.A. Neuronal NOS: gene structure, mRNA diversity, and functional relevance. Crit Rev Neurobiol. 13:1999;21-43.
66. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santillano D.R., et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell. 84:1996;757-767.
67. Jaffrey S.R., Snyder S.H. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science. 274:1996;774-777.
68. Silvagno F., Xia H., Bredt D.S. Neuronal nitric-oxide synthase-μ, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem. 271:1996;11204-11208.
69. Cotton J.M., Kearney M.T., MacCarthy P.A., Grocott-Mason R.M., McClean D.R., Heymes C., et al. Effects of nitric oxide synthase inhibition on basal function and the force-frequency relationship in the normal and failing human heart in vivo. Circulation. 104:(19):2001;2318-2323.
70. Sears C., Bryant S.M., Ashley E., Lygate C.A., Rakovic S., Wallis H.L., et al. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ Res. 92:2003;e52-e59.
71. Henning R.J., Khalil I.R., Levy M.N. Vagal stimulation attenuates sympathetic enhancement of left ventricular function. Am J Physiol. 258:1990;H1470-H1475.
72. Watanabe A.M., Besch H.R. Jr. Interaction between cyclic adenosine monophosphate and cyclic guanosine monophosphate in guinea pig ventricular myocardium. Circ Res. 37:1975;309-317.
73. 3-adrenoreceptor stimulation is mediated by activation of a nitric oxide synthase pathway in human ventricle. J Clin Invest. 102:1998;1377-1384.
74. Moniotte S., Kobzik L., Feron O., Trochu J.N., Gauthier C., Balligand J.L. Upregulation of beta(3)-adrenoceptors and altered contractile response to inotropic amines in human failing myocardium. Circulation. 103:2001;1649-1655.
75. 3-adrenoceptor in the human heart. J Clin Invest. 98:(2):1998;556-562.
76. 3-adrenoreceptor agonists. J Pharmacol Exp Ther. 290:1999;687-693.
77. Cheng H.J., Zhang Z.S., Onishi K., Ukai T., Sane D.C., Cheng C.P. Upregulation of functional beta(3)-adrenergic receptor in the failing canine myocardium. Circ Res. 89:2001;599-606.
78. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc Natl Acad Sci USA. 88:1991;1197-1201.
79. 2+ current in single heart cells. Nature. 323:1986;273-275.
80. 2+ current. Involvement of cGMP-inhibited and cGMP-stimulated phosphodiesterases through guanylyl cyclase activity. J Biol Chem. 268:1993;26286-26295.
81. Ca-L is absent in mice with targeted disruption of endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 95:1998;6510-6515.
82. Feron O., Dessy C., Opel D.J., Arstall M.A., Kelly R.A., Michel T. Modulation of endothelial nitric-oxide synthase-caveolin interaction in cardiac myocytes. J Biol Chem. 273:1998;30249-30254.
83. Mohan R.M., Heaton D.A., Danson E.J., Krishnan S.P., Cai S., Channon K.M., et al. Neuronal nitric oxide synthase gene transfer promotes cardiac vagal gain of function. Circ Res. 91:2002;1089-1091.
84. Surks H.K., Mochizuki N., Kasai Y., Georgescu S.P., Tang K.M., Ito M., et al. Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase Ialpha. Science. 286:1999;1583-1587.
85. Bates T.E., Loesch A., Burnstock G., Clark J.B. Mitochondrial nitric oxide synthase: a ubiquitous regulator of oxidative phosphorylation? Biochem Biophys Res Comm. 218:1996;40-44.
86. Xie Y.-W., Shen W., Zhao G., Xu X., Wolin M.S., Hintze T.H. Role of endothelium-derived nitric oxide in the modulation of canine myocardial mitochondrial respiration in vitro. Implications for the development of heart failure. Circ Res. 79:1996;381-387.
87. Suto N., Mikuniya A., Okubo T., Hanada H., Shinozaki N., Okumura K. Nitric oxide modulates cardiac contractility and oxygen consumption without changing contractile efficiency. Am J Physiol. 275:1998;H41-H49.
88. Kanai A.J., Pearce L.L., Clemens P.R., Birder L.A., VanBibber M.M., Choi S.Y., et al. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc Natl Acad Sci USA. 98:(24):2001;14126-14131.
89. Khan S.A., Skaf M.W., Harrison R.W., Lee K., Minhas K.M., Kumar A., Fradley M., Shoukas A.A., Berkowitz D.E., Hare J.M. Nitric oxide regulation of myocardial contractility and calcium cycling: Independent impact of neuronal and endothelial nitric oxide synthases. Circ Res. 2003;. (in press).
90. 2+ release in cardiomyocytes. Nat Cell Biol. 3:(10):2001;867-873.
91. Ashley E., Sears C., Bryant S., Watkins H., Casadei B. Cardiac nitric oxide synthase 1 regulates basal and β-adrenergic contractility in murine ventricular myoyctes. Circulation. 105:2002;3011-3016.
92. (2+)-ATPase of rabbit skeletal muscle sarcoplasmic reticulum: identification of sites labeled with aryl isothiocyanates and thiol-directed conformational probes. Biochim Biophys Acta. 1203:1993;60-70.
93. 2+ ATPase activity by hypochlorous acid: reversal by dithiothreitol. Can J Physiol Pharmacol. 69:1991;1677-1685.
94. Stamler J.S., Hausladen A. Oxidative modifications in nitrosative stress. Nat Struct Biol. 5:1998;247-249.
95. Stojanovic M.O., Ziolo M.T., Wahler G.M., Wolska B.M. Anti-adrenergic effects of nitric oxide donor SIN-1 in rat cardiac myocytes. Am J Physiol Cell Physiol. 281:(1):2001;C342-C349.
96. Cornwell T.L., Pryzwansky K.B., Wyatt T.A., Lincoln T.M. Regulation of sarcoplasmic reticulum protein phosphorylation by localized cyclic GMP-dependent protein kinase in vascular smooth muscle cells. Mol Pharmacol. 40:(6):1991;923-931.
97. Zeitz O., Maass A.E., Van Nguyen P., Hensmann G., Kogler H., Moller K., et al. Hydroxyl radical-induced acute diastolic dysfunction is due to calcium overload via reverse-mode Na(+)-Ca(2+) exchange. Circ Res. 90:(9):2002;988-995.
98. Hare J.M., Givertz M.M., Creager M.A., Colucci W.S. Increased sensitivity to nitric oxide synthase inhibition in patients with heart failure: Potentiation of β-adrenergic inotropic responsiveness. Circulation. 97:1998;161-166.
99. Barry W.H. Mechanisms of immune-mediated myocyte injury. Circulation. 89:1994;2421-2432.
100. Yang X., Chowdhury N., Cai B., Brett J., Marboe C., Sciacca R.R., et al. Induction of myocardial nitric oxide synthase by cardiac allograft rejection. J Clin Invest. 94:1994;714-721.
101. Levine B., Kalman J., Mayer L., Fillit H.M., Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. New Engl J M. 323:1990;236-241.
102. Torre-Amione G., Kapadia S., Benedict C., Oral H., Young J.B., Mann D.L. Proinflammatory cytokine levels in patients with depressed left ventricular ejection fraction: a report from the studies of left ventricular dysfunction (SOLVD). J Am Coll Cardiol. 27:1996;1201-1206.
103. Torre-Amione G., Kapadia S., Lee J., Durand J.-B., Bies R.D., Young J.B., et al. Tumor necrosis factor-α and tumor necrosis factor receptors in the failing human heart. Circulation. 93:1996;704-711.
104. Nathan C. Inducible nitric oxide synthase: what difference does in make? J Clin Invest. 100:1997;2417-2423.
105. Haywood G.A., Tsao P.S., von der Leyen H.E., Mann M.J., Keeling P.J., Trindade P.T., et al. Expression of inducible nitric oxide synthase in human heart failure. Circulation. 93:1996;1087-1094.
106. DeBelder A.J., Radomski M.W., Why H.J., Richardson P.J., Martin J.F. Myocardial calcium-independent nitric oxide synthase activity is present in dilated cardiomyopathy, myocarditis, and postpartum cardiomyopathy but not in ischaemic or valvar heart disease. Br Heart J. 74:1995;426-430.
107. Habib F.M., Springall D.R., Davies G.J., Oakley C.M., Yacoub M.H., Polak J.M. Tumor necrosis factor and inducible nitric oxide synthase in dilated cardiomyopathy. Lancet. 347:1996;1151-1155.
108. Theones M., Forstermann U., Tracey W.R., Bleese N.M., Nussler A.K., Scholz H., et al. Expression of inducible nitric oxide synthase in failing and non-failing human heart. J Mol Cell Cardiol. 28:1996;165-169.
109. Ziolo M.T., Katoh H., Bers D.M. Expression of inducible nitric oxide synthase depresses beta-adrenergic-stimulated calcium release from the sarcoplasmic reticulum in intact ventricular myocytes. Circulation. 104:2001;2961-2966.
110. Barouch L.A., Harrison R.W., Cappola T.P., Skaf M.W., Crone J.K., Rodriguez E.R., et al. Combined loss of cardiac neuronal and endothelial nitric oxide synthase causes premature mortality and age-associated hypertropic cardiac remodeling in mice. J Mol Cell Cardiol. 35:2003;637-644.
111. Hare J.M. Oxidative stress and apoptosis in heart failure progression. Circ Res. 89:(3):2001;198-200.
112. 2+ channel. Mol Pharmacol. 53:(3):1998;497-503.
113. Beltran B., Mathur A., Duchen M.R., Erusalimsky J.D., Moncada S. The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc Natl Acad Sci USA. 97:2000;14602-14607.
114. Geng Y.J., Hansson G.K., Holme E. Interferon-γ and tumor necrosis factor synergize to induce nitric oxide production and inhibit mitochondrial respiration in vascular smooth muscle cells. Circ Res. 71:1992;1268-1276.
115. Ekelund U.E.G., Harrison R.W., Shokek O., Thakkar R.N., Tunin R.S., Senzaki H., et al. Intravenous allopurinol decreases myocardial oxygen consumption and increases mechanical efficiency in dogs with pacing-induced heart failure. Circ Res. 85:1999;437-445.
116. Cappola T.P., Kass D.A., Nelson G.S., Berger R.D., Rosas G.O., Kobeissi Z.A., et al. Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation. 104:(20):2001;2407-2411.