Nitrite therapy improves left ventricular function during heart failure via restoration of nitric oxide-mediated cytoprotective signaling

Circulation Research

Volumn 114, Issue 8, 2014, Pages 1281-1291

  Bhushan, Shashi ^a   Kondo, Kazuhisa ^b   Polhemus, David J ^a   Otsuka, Hiroyuki ^a   Nicholson, Chad K ^c   Tao, Ya Xiong ^e   Huang, Hui ^e   Georgiopoulou, Vasiliki V ^d   Murohara, Toyoaki ^b   Calvert, John W ^c   Butler, Javed ^d   Lefer, David J ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c Carlyle Fraser Heart Center   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e AUBURN UNIVERSITY   (United States)

Author keywords

cardiomyopathy; cyclic GMP; heart failure; hypertrophic; left; nitric oxide; nitric oxide synthase; ventricular function

Indexed keywords

CARDIOMYOPATHY, HYPERTROPHIC; CYCLIC GMP; HEART FAILURE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; VENTRICULAR FUNCTION, LEFT;

AGED; ANIMALS; BIOLOGICAL AVAILABILITY; CYCLIC GMP; CYTOPROTECTION; DISEASE MODELS, ANIMAL; FEMALE; HEART FAILURE; HEMODYNAMICS; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MIDDLE AGED; NITRIC OXIDE; SIGNAL TRANSDUCTION; SODIUM NITRITE; STROKE VOLUME; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84898834966     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.301475     Document Type: Article

References (47)

1. Katholi RE, Couri DM. Left ventricular hypertrophy: major risk factor in patients with hypertension: update and practical clinical applications. Int J Hypertens. 2011;2011:495349.
2. Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol. 2002;53:503-514.
3. Smith CJ, Sun D, Hoegler C, Roth BS, Zhang X, Zhao G, Xu XB, Kobari Y, Pritchard K Jr, Sessa WC, Hintze TH. Reduced gene expression of vascular endothelial NO synthase and cyclooxygenase-1 in heart failure. Circ Res. 1996;78:58-64.
4. Jones SP, Greer JJ, van Haperen R, Duncker DJ, de Crom R, Lefer DJ. Endothelial nitric oxide synthase overexpression attenuates congestive heart failure in mice. Proc Natl Acad Sci USA. 2003;100:4891-4896.
5. Scherrer-Crosbie M, Ullrich R, Bloch KD, Nakajima H, Nasseri B, Aretz HT, Lindsey ML, Vançon AC, Huang PL, Lee RT, Zapol WM, Picard MH. Endothelial nitric oxide synthase limits left ventricular remodeling after myocardial infarction in mice. Circulation. 2001;104:1286-1291.
6. Fraccarollo D, Widder JD, Galuppo P, Thum T, Tsikas D, Hoffmann M, Ruetten H, Ertl G, Bauersachs J. Improvement in left ventricular remodeling by the endothelial nitric oxide synthase enhancer AVE9488 after experimental myocardial infarction. Circulation. 2008;118:818-827.
7. Taylor AL. Nitric oxide modulation as a therapeutic strategy in heart failure. Heart Fail Clin. 2012;8:255-272.
8. Calvert JW, Lefer DJ. Clinical translation of nitrite therapy for cardiovascular diseases. Nitric Oxide. 2010;22:91-97.
9. Dejam A, Hunter CJ, Schechter AN, Gladwin MT. Emerging role of nitrite in human biology. Blood Cells Mol Dis. 2004;32:423-429.
10. Duranski MR, Greer JJ, Dejam A, Jaganmohan S, Hogg N, Langston W, Patel RP, Yet SF, Wang X, Kevil CG, Gladwin MT, Lefer DJ. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest. 2005;115:1232-1240.
11. Hendgen-Cotta UB, Merx MW, Shiva S, Schmitz J, Becher S, Klare JP, Steinhoff HJ, Goedecke A, Schrader J, Gladwin MT, Kelm M, Rassaf T. Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA. 2008;105:10256-10261.
12. Bryan NS, Calvert JW, Elrod JW, Gundewar S, Ji SY, Lefer DJ. Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA. 2007;104:19144-19149.
13. 2S protects against pressure overload-in duced heart failure via upregulation of endothelial nitric oxide synthase. Circulation. 2013;127:1116-1127.
14. Polhemus DJ, Kondo K, Bhushan S, Bir SC, Kevil CG, Murohara T, Lefer DJ, Calvert JW. Hydrogen sulfde attenuates cardiac dysfunction after heart failure via induction of angiogenesis. Circ Heart Fail. 2013;6:1077-1086.
15. Bhushan S, Kondo K, Predmore BL, Zlatopolsky M, King AL, Pearce C, Huang H, Tao YX, Condit ME, Lefer DJ. Selective beta2-adrenoreceptor stimulation attenuates myocardial cell death and preserves cardiac function after ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol. 2012;32:1865-1874
16. Aragón J P, Condit ME, Bhushan S, Predmore BL, Patel SS, Grinsfelder DB, Gundewar S, Jha S, Calvert JW, Barouch LA, Lavu M, Wright HM, Lefer DJ. Beta3-adrenoreceptor stimulation ameliorates myocardial ischemia-reperfusion injury via endothelial nitric oxide synthase and neuro-nal nitric oxide synthase activation. J Am Coll Cardiol. 2011;58:2683-2691.
17. Teng R, Calvert JW, Sibmooh N, Piknova B, Suzuki N, Sun J, Martinez K, Yamamoto M, Schechter AN, Lefer DJ, Noguchi CT. Acute erythropoietin cardioprotection is mediated by endothelial response. Basic Res Cardiol. 2011;106:343-354.
18. Steiner AL, Parker CW, Kipnis DM. Radioimmunoassay for cyclic nucle-otides. I. Preparation of antibodies and iodinated cyclic nucleotides. J Biol Chem. 1972;247:1106-1113.
19. Elrod JW, Greer JJ, Bryan NS, Langston W, Szot JF, Gebregzlabher H, Janssens S, Feelisch M, Lefer DJ. Cardiomyocyte-specifc overexpression of NO synthase-3 protects against myocardial ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol. 2006;26:1517-1523.
20. Dimmeler S, Zeiher AM. Akt takes center stage in angiogenesis signaling. Circ Res. 2000;86:4-5.
21. Calvert JW, Lefer DJ. Clinical translation of nitrite therapy for cardiovascular diseases. Nitric Oxide. 2010;22:91-97.
22. Markou T, Cullingford TE, Giraldo A, Weiss SC, Alsaf A, Fuller SJ, Clerk A, Sugden PH. Glycogen synthase kinases 3alpha and 3beta in cardiac myocytes: regulation and consequences of their inhibition. Cell Signal. 2008;20:206-218.
23. Bueno OF, Molkentin JD. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ Res. 2002;91:776-781.
24. Nishida K, Yamaguchi O, Hirotani S, et al. p38alpha mitogen-activated protein kinase plays a critical role in cardiomyocyte survival but not in cardiac hypertrophic growth in response to pressure overload. Mol Cell Biol. 2004;24:10611-10620.
25. Rose BA, Force T, Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol Rev. 2010;90:1507-1546.
26. Katz SD, Khan T, Zeballos GA, Mathew L, Potharlanka P, Knecht M, Whelan J. Decreased activity of the L-arginine-nitric oxide metabolic pathway in patients with congestive heart failure. Circulation. 1999;99:2113-2117.
27. Janssens S, Pokreisz P, Schoonjans L, Pellens M, Vermeersch P, Tjwa M, Jans P, Scherrer-Crosbie M, Picard MH, Szelid Z, Gillijns H, Van de Werf F, Collen D, Bloch KD. Cardiomyocyte-specifc overexpression of nitric oxide synthase 3 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction. Circ Res. 2004;94:1256-1262.
28. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 1995;377:239-242.
29. Ichinose F, Bloch KD, Wu JC, Hataishi R, Aretz HT, Picard MH, Scherrer-Crosbie M. Pressure overload-induced LV hypertrophy and dysfunction in mice are exacerbated by congenital NOS3 defciency. Am J Physiol Heart Circ Physiol. 2004;286:H1070-H1075.
30. Ozaki M, Kawashima S, Yamashita T, Hirase T, Ohashi Y, Inoue N, Hirata K, Yokoyama M. Overexpression of endothelial nitric oxide synthase attenuates cardiac hypertrophy induced by chronic isoproterenol infusion. Circ J. 2002;66:851-856.
31. Massion PB, Feron O, Dessy C, Balligand JL. Nitric oxide and cardiac function: ten years after, and continuing. Circ Res. 2003;93:388-398.
32. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, Kass DA. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest. 2005;115:1221-1231.
33. Thomas DD, Liu X, Kantrow SP, Lancaster JR Jr. The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA. 2001;98:355-360.
34. Clark AL. Almanac 2011: heart failure. The national society journals present selected research that has driven recent advances in clinical cardiology. Heart. 2011;97:1643-1649.
35. Lewis GD, Shah R, Shahzad K, Camuso JM, Pappagianopoulos PP, Hung J, Tawakol A, Gerszten RE, Systrom DM, Bloch KD, Semigran MJ. Sildenafl improves exercise capacity and quality of life in patients with systolic heart failure and secondary pulmonary hypertension. Circulation. 2007;116:1555-1562.
36. Greer JJ, Kakkar AK, Elrod JW, Watson LJ, Jones SP, Lefer DJ. Low-dose simvastatin improves survival and ventricular function via eNOS in congestive heart failure. Am J Physiol Heart Circ Physiol. 2006;291:H2743-H2751.
37. Prabhu SD. Nitric oxide protects against pathological ventricular remodeling: reconsideration of the role of NO in the failing heart. Circ Res. 2004;94:1155-1157.
38. Chaanine AH, Hajjar RJ. AKT signalling in the failing heart. Eur J Heart Fail. 2011;13:825-829.
39. Shiojima I, Schiekofer S, Schneider JG, Belisle K, Sato K, Andrassy M, Galasso G, Walsh K. Short-term akt activation in cardiac muscle cells improves contractile function in failing hearts. Am J Pathol. 2012;181:1969-1976.
40. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem. 2002;277:22896-22901.
41. Haq S, Choukroun G, Lim H, Tymitz KM, del Monte F, Gwathmey J, Grazette L, Michael A, Hajjar R, Force T, Molkentin JD. Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure. Circulation. 2001;103:670-677.
42. Antos CL, McKinsey TA, Frey N, Kutschke W, McAnally J, Shelton JM, Richardson JA, Hill JA, Olson EN. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc Natl Acad Sci USA. 2002;99:907-912.
43. Hardt SE, Sadoshima J. Glycogen synthase kinase-3beta: a novel regulator of cardiac hypertrophy and development. Circ Res. 2002;90:1055-1063.
44. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, Hewett TE, Jones SP, Lefer DJ, Peng CF, Kitsis RN, Molkentin JD. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J. 2000;19:6341-6350.
45. Lips DJ, Bueno OF, Wilkins BJ, Purcell NH, Kaiser RA, Lorenz JN, Voisin L, Saba-El-Leil MK, Meloche S, Pouysségur J, Pagès G, De Windt LJ, Doevendans PA, Molkentin JD. MEK1-ERK2 signaling pathway protects myocardium from ischemic injury in vivo. Circulation. 2004;109:1938-1941.
46. Gladwin MT, Raat NJ, Shiva S, Dezfulian C, Hogg N, Kim-Shapiro DB, Patel RP. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am J Physiol Heart Circ Physiol. 2006;291:H2026-H2035.
47. Gonzalez FM, Shiva S, Vincent PS, Ringwood LA, Hsu LY, Hon YY, Aletras AH, Cannon RO 3rd, Gladwin MT, Arai AE. Nitrite anion provides potent cytoprotective and antiapoptotic effects as adjunctive therapy to reperfu-sion for acute myocardial infarction. Circulation. 2008;117:2986-2994.