Hydrogen sulfide attenuates cardiac dysfunction after heart failure via induction of angiogenesis

Circulation: Heart Failure

Volumn 6, Issue 5, 2013, Pages 1077-1086

  Polhemus, David J ^a,b   Kondo, Kazuhisa ^c   Bhushan, Shashi ^a,b   Bir, Shyamal C ^d   Kevil, Christopher G ^d   Murohara, Toyoaki ^c   Lefer, David J ^a,b   Calvert, John W ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Carlyle Fraser Heart Center   (United States)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Angiogenesis; Diallyl trisulfide; Endothelial nitric oxide synthase; H 2S donor; Nitric oxide

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOSTATIN; DIALLYL TRISULFIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; KI 67 ANTIGEN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; FOLLOW UP; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANGIOGENESIS; DIALLYL TRISULFIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; H2S DONOR; NITRIC OXIDE;

ALLYL COMPOUNDS; ANGIOSTATINS; ANIMALS; DISEASE MODELS, ANIMAL; FIBROSIS; HEART FAILURE; HYDROGEN SULFIDE; KI-67 ANTIGEN; MALE; MICE; MICE, INBRED C57BL; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; SULFIDES; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84887461017     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000299     Document Type: Article

References (49)

1. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600.
2. Foo RS, Mani K, Kitsis RN. Death begets failure in the heart. J Clin Invest. 2005;115:565-571.
3. Cohen-Solal A, Beauvais F, Logeart D. Heart failure and diabetes mellitus: epidemiology and management of an alarming association. J Card Fail. 2008;14:615-625.
4. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, Darley-Usmar VM, Doeller JE, Kraus DW. Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A. 2007;104: 17977-17982.
5. Powolny AA, Singh SV. Multitargeted prevention and therapy of cancer by diallyl trisulfide and related Allium vegetable-derived organosulfur compounds. Cancer Lett. 2008;269:305-314.
6. Mustafa AK, Gadalla MM, Snyder SH. Signaling by gasotransmitters. Sci Signal. 2009;2:re2.
7. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow CW, Lefer DJ. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A. 2007;104:15560-15565.
8. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, Kevil CG, Lefer DJ. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res. 2009;105:365-374.
9. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322:587-590.
10. Calvert JW, Coetzee WA, Lefer DJ. Novel insights into hydrogen sulfide- mediated cytoprotection. Antioxid Redox Signal. 2010;12:1203-1217.
11. Predmore BL, Kondo K, Bhushan S, Zlatopolsky MA, King AL, Aragon JP, Grinsfelder DB, Condit ME, Lefer DJ. The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability. Am J Physiol Heart Circ Physiol. 2012;302:H2410-H2418.
12. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653-660.
13. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, Jeschke MG, Branski LK, Herndon DN, Wang R, Szabó C. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci U S A. 2009;106:21972-21977.
14. Szabó C, Papapetropoulos A. Hydrogen sulphide and angiogenesis: mechanisms and applications. Br J Pharmacol. 2011;164:853-865.
15. Coletta C, Papapetropoulos A, Erdelyi K, Olah G, Módis K, Panopoulos P, Asimakopoulou A, Gerö D, Sharina I, Martin E, Szabo C. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci U S A. 2012;109:9161-9166.
16. Bir SC, Kolluru GK, McCarthy P, Shen X, Pardue S, Pattillo CB, Kevil CG. Hydrogen sulfide stimulates ischemic vascular remodeling through nitric oxide synthase and nitrite reduction activity regulating hypoxiainducible factor-1α and vascular endothelial growth factor-dependent angiogenesis. J Am Heart Assoc. 2012;1:e004093.
17. Calvert JW, Elston M, Nicholson CK, Gundewar S, Jha S, Elrod JW, Ramachandran A, Lefer DJ. Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation. 2010;122:11-19.
18. Elrod JW, Calvert JW, Gundewar S, Bryan NS, Lefer DJ. Nitric oxide promotes distant organ protection: evidence for an endocrine role of nitric oxide. Proc Natl Acad Sci U S A. 2008;105:11430-11435.
19. Lavu M, Gundewar S, Lefer DJ. Gene therapy for ischemic heart disease. J Mol Cell Cardiol. 2011;50:742-750.
20. Calvert JW, Gundewar S, Jha S, Greer JJ, Bestermann WH, Tian R, Lefer DJ. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes. 2008;57:696-705.
21. Koitabashi N, Kass DA. Reverse remodeling in heart failure-mechanisms and therapeutic opportunities. Nat Rev Cardiol. 2012;9:147-157.
22. Solomon SD, Pfeffer MA. The decreasing incidence of left ventricular remodeling following myocardial infarction. Basic Res Cardiol. 1997;92:61-65.
23. Maack C, Kartes T, Kilter H, Schäfers HJ, Nickenig G, Böhm M, Laufs U. Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation. 2003;108:1567-1574.
24. Mishra PK, Tyagi N, Sen U, Givvimani S, Tyagi SC. H2S ameliorates oxidative and proteolytic stresses and protects the heart against adverse remodeling in chronic heart failure. Am J Physiol Heart Circ Physiol. 2010;298:H451-H456.
25. Izumiya Y, Shiojima I, Sato K, Sawyer DB, Colucci WS, Walsh K. Vascular endothelial growth factor blockade promotes the transition from compensatory cardiac hypertrophy to failure in response to pressure overload. Hypertension. 2006;47:887-893.
26. Oshima Y, Ouchi N, Sato K, Izumiya Y, Pimentel DR, Walsh K. Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation. 2008;117:3099-3108.
27. Szabó C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6:917-935.
28. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, Zhu YC. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res. 2007;76:29-40.
29. Qipshidze N, Metreveli N, Mishra PK, Lominadze D, Tyagi SC. Hydrogen sulfide mitigates cardiac remodeling during myocardial infarction via improvement of angiogenesis. Int J Biol Sci. 2012;8:430-441.
30. Villaschi S, Nicosia RF. Angiogenic role of endogenous basic fibroblast growth factor released by rat aorta after injury. Am J Pathol. 1993;143:181-190.
31. Cooke JP. NO and angiogenesis. Atheroscler Suppl. 2003;4:53-60.
32. Minamishima S, Bougaki M, Sips PY, Yu JD, Minamishima YA, Elrod JW, Lefer DJ, Bloch KD, Ichinose F. Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation. 2009;120:888-896.
33. Osipov RM, Robich MP, Feng J, Liu Y, Clements RT, Glazer HP, Sodha NR, Szabo C, Bianchi C, Sellke FW. Effect of hydrogen sulfide in a porcine model of myocardial ischemia-reperfusion: comparison of different administration regimens and characterization of the cellular mechanisms of protection. J Cardiovasc Pharmacol. 2009;54:287-297.
34. Osipov RM, Robich MP, Feng J, Chan V, Clements RT, Deyo RJ, Szabo C, Sellke FW. Effect of hydrogen sulfide on myocardial protection in the setting of cardioplegia and cardiopulmonary bypass. Interact Cardiovasc Thorac Surg. 2010;10:506-512.
35. Shen BQ, Lee DY, Zioncheck TF. Vascular endothelial growth factor governs endothelial nitric-oxide synthase expression via a KDR/ Flk-1 receptor and a protein kinase C signaling pathway. J Biol Chem. 1999;274:33057-33063.
36. Kang KW, Lee SJ, Kim SG. Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal. 2005;7:1664-1673.
37. Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 2004;18:1165-1167.
38. Fisher CD, Augustine LM, Maher JM, Nelson DM, Slitt AL, Klaassen CD, Lehman-McKeeman LD, Cherrington NJ. Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab Dispos. 2007;35:995-1000.
39. Thu VT, Kim HK, Ha SH, Yoo JY, Park WS, Kim N, Oh GT, Han J. Glutathione peroxidase 1 protects mitochondria against hypoxia/reoxygenation damage in mouse hearts. Pflugers Arch. 2010;460:55-68.
40. Ardanaz N, Yang XP, Cifuentes ME, Haurani MJ, Jackson KW, Liao TD, Carretero OA, Pagano PJ. Lack of glutathione peroxidase 1 accelerates cardiac-specific hypertrophy and dysfunction in angiotensin II hypertension. Hypertension. 2010;55:116-123.
41. Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol. 2000;279:L1029-L1037.
42. Wang G, Hamid T, Keith RJ, Zhou G, Partridge CR, Xiang X, Kingery JR, Lewis RK, Li Q, Rokosh DG, Ford R, Spinale FG, Riggs DW, Srivastava S, Bhatnagar A, Bolli R, Prabhu SD. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation. 2010;121:1912-1925.
43. Paul BD, Snyder SH. H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol. 2012;13:499-507.
44. 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.
45. Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barodka VM, Gazi FK, Barrow RK, Wang R, Amzel LM, Berkowitz DE, Snyder SH. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res. 2011;109:1259-1268.
46. Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kim S, Snyder SH. Hydrogen sulfide-linked sulfhydration of NF-κB mediates its antiapoptotic actions. Mol Cell. 2012;45:13-24.
47. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal. 2013;18:1906-1919.
48. Um HC, Jang JH, Kim DH, Lee C, Surh YJ. Nitric oxide activates Nrf2 through S-nitrosylation of Keap1 in PC12 cells. Nitric Oxide. 2011;25:161-168.
49. Li Q, Guo Y, Ou Q, Cui C, Wu WJ, Tan W, Zhu X, Lanceta LB, Sanganalmath SK, Dawn B, Shinmura K, Rokosh GD, Wang S, Bolli R. Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-{kappa} B-dependent pathway. Circulation. 2009;120:1222-1230.