Hydrogen sulfide and cardioprotection - Mechanistic insights and clinical translatability

Pharmacology and Therapeutics

Volumn 152, Issue , 2015, Pages 11-17

  Salloum, Fadi N ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute myocardial infarction; Angiogenesis; Apoptosis; Heart failure; Hydrogen sulfide; Inflammation

Indexed keywords

DOXORUBICIN; GASOTRANSMITTER; HYDROGEN SULFIDE; CARDIOTONIC AGENT;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; CARDIOVASCULAR DISEASE; HEART ARREST; HEART FAILURE; HEART HYPERTROPHY; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; MYOCARDITIS; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; RESUSCITATION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; HEART; HEART DISEASES; METABOLISM; PHYSIOLOGY;

ANIMALS; CARDIOTONIC AGENTS; HEART; HEART DISEASES; HUMANS; HYDROGEN SULFIDE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84933677721     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.04.004     Document Type: Review

References (81)

1. L.A. Barr, and J.W. Calvert Discoveries of hydrogen sulfide as a novel cardiovascular therapeutic Circ J 78 2014 2111 2118
2. G.A. Benavides, G.L. Squadrito, R.W. Mills, H.D. Patel, T.S. Isbell, and R.P. Patel Hydrogen sulfide mediates the vasoactivity of garlic Proc Natl Acad Sci U S A 104 2007 17977 17982
3. S.C. Bir, G.K. Kolluru, P. McCarthy, X. Shen, S. Pardue, and C.B. Pattillo Hydrogen sulfide stimulates ischemic vascular remodeling through nitric oxide synthase and nitrite reduction activity regulating hypoxia-inducible factor-1alpha and vascular endothelial growth factor-dependent angiogenesis J Am Heart Assoc 1 2012 e004093
4. E. Blackstone, M. Morrison, and M.B. Roth H2S induces a suspended animation-like state in mice Science 308 2005 518
5. E. Boelke, M. Storck, K. Buttenschoen, D. Berger, and A. Hannekum Endotoxemia and mediator release during cardiac surgery Angiology 51 2000 743 749
6. Z. Cai, and G.L. Semenza PTEN activity is modulated during ischemia and reperfusion: involvement in the induction and decay of preconditioning Circ Res 97 2005 1351 1359
7. W.J. Cai, M.J. Wang, P.K. Moore, H.M. Jin, T. Yao, and Y.C. Zhu The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation Cardiovasc Res 76 2007 29 40
8. G. Caliendo, G. Cirino, V. Santagada, and J.L. Wallace Synthesis and biological effects of hydrogen sulfide (H2S): development of H2S-releasing drugs as pharmaceuticals J Med Chem 53 2010 6275 6286
9. J.W. Calvert, M. Elston, C.K. Nicholson, S. Gundewar, S. Jha, and J.W. Elrod Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice Circulation 122 2010 11 19
10. S.R. Case, R.J. Martin, D. Jiang, M.N. Minor, and H.W. Chu MicroRNA-21 inhibits toll-like receptor 2 agonist-induced lung inflammation in mice Exp Lung Res 37 2011 500 508
11. Y. Chen, J. Chen, H. Wang, J. Shi, K. Wu, and S. Liu HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1 PLoS Pathog 9 2013 e1003248
12. M.W. Donnino, L.W. Andersen, T. Giberson, D.F. Gaieski, B.S. Abella, and M.A. Peberdy Initial lactate and lactate change in post-cardiac arrest: a multicenter validation study Crit Care Med 42 2014 1804 1811
13. J.W. Elrod, J.W. Calvert, J. Morrison, J.E. Doeller, D.W. Kraus, and L. Tao Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function Proc Natl Acad Sci U S A 104 2007 15560 15565
14. L. Franchi, T. Eigenbrod, R. Munoz-Planillo, and G. Nunez The inflammasome: A caspase-1-activation platform that regulates immune responses and disease pathogenesis Nat Immunol 10 2009 241 247
15. N.G. Frangogiannis, C.W. Smith, and M.L. Entman The inflammatory response in myocardial infarction Cardiovasc Res 53 2002 31 47
16. S. Frantz, A. Ducharme, D. Sawyer, L.E. Rohde, L. Kobzik, and R. Fukazawa Targeted deletion of caspase-1 reduces early mortality and left ventricular dilatation following myocardial infarction J Mol Cell Cardiol 35 2003 685 694
17. B. Geng, J. Yang, Y. Qi, J. Zhao, Y. Pang, and J. Du H2S generated by heart in rat and its effects on cardiac function Biochem Biophys Res Commun 313 2004 362 368
18. S. Givvimani, C. Munjal, R. Gargoum, U. Sen, N. Tyagi, and J.C. Vacek Hydrogen sulfide mitigates transition from compensatory hypertrophy to heart failure J Appl Physiol 110 2011 1093 1100
19. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, and M.J. Blaha Heart disease and stroke statistics - 2014 update: A report from the American Heart Association Circulation 129 2014 e28 e292
20. R. Guo, J. Lin, W. Xu, N. Shen, L. Mo, and C. Zhang Hydrogen sulfide attenuates doxorubicin-induced cardiotoxicity by inhibition of the p38 MAPK pathway in H9c2 cells Int J Mol Med 31 2013 644 650
21. S.J. Hanssen, J.P. Derikx, I.C. Vermeulen Windsant, J.H. Heijmans, T.A. Koeppel, and G.W. Schurink Visceral injury and systemic inflammation in patients undergoing extracorporeal circulation during aortic surgery Ann Surg 248 2008 117 125
22. D.J. Hausenloy, and D.M. Yellon Myocardial ischemia-reperfusion injury: A neglected therapeutic target J Clin Invest 123 2013 92 100
23. Y. Ji, Q.F. Pang, G. Xu, L. Wang, J.K. Wang, and Y.M. Zeng Exogenous hydrogen sulfide postconditioning protects isolated rat hearts against ischemia-reperfusion injury Eur J Pharmacol 587 2008 1 7
24. H.L. Jiang, H.C. Wu, Z.L. Li, B. Geng, and C.S. Tang Changes of the new gaseous transmitter H2S in patients with coronary heart disease Di 1 jun yi da xue xue bao Acad J First Med Coll PLA 25 2005 951 954
25. J. Kan, W. Guo, C. Huang, G. Bao, Y. Zhu, and Y.Z. Zhu S-propargyl-cysteine, a novel water-soluble modulator of endogenous hydrogen sulfide, promotes angiogenesis through activation of signal transducer and activator of transcription 3 Antioxid Redox Signal 20 2014 2303 2316
26. M. Kawaguchi, M. Takahashi, T. Hata, Y. Kashima, F. Usui, and H. Morimoto Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury Circulation 123 2011 594 604
27. A.L. King, D.J. Polhemus, S. Bhushan, H. Otsuka, K. Kondo, and C.K. Nicholson Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent Proc Natl Acad Sci U S A 111 2014 3182 3187
28. K. Kondo, S. Bhushan, A.L. King, S.D. Prabhu, T. Hamid, and S. Koenig H(2)S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase Circulation 127 2013 1116 1127
29. D. Kovacic, N. Glavnik, M. Marinsek, P. Zagozen, K. Rovan, and T. Goslar Total plasma sulfide in congestive heart failure J Card Fail 18 2012 541 548
30. W.W. Kuo, W.J. Wang, C.Y. Tsai, C.L. Way, H.H. Hsu, and L.M. Chen Diallyl trisufide (DATS) suppresses high glucose-induced cardiomyocyte apoptosis by inhibiting JNK/NFkappaB signaling via attenuating ROS generation Int J Cardiol 168 2013 270 280
31. J.P. Lambert, C.K. Nicholson, H. Amin, S. Amin, and J.W. Calvert Hydrogen sulfide provides cardioprotection against myocardial/ischemia reperfusion injury in the diabetic state through the activation of the RISK pathway Med Gas Res 4 2014 20
32. L. Li, M. Whiteman, Y.Y. Guan, K.L. Neo, Y. Cheng, and S.W. Lee Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide Circulation 117 2008 2351 2360
33. F. Liu, D.D. Chen, X. Sun, H.H. Xie, H. Yuan, and W. Jia Hydrogen sulfide improves wound healing via restoration of endothelial progenitor cell functions and activation of angiopoietin-1 in type 2 diabetes Diabetes 63 2014 1763 1778
34. Z. Liu, Y. Han, L. Li, H. Lu, G. Meng, and X. Li The hydrgen sulfide donor, GYY4137, exhibits anti-atherosclerotic activity in high fat fed apolipoprotein E(-/-) mice Br J Pharmacol 169 2013 1795 1809
35. F. Lu, J. Xing, X. Zhang, S. Dong, Y. Zhao, and L. Wang Exogenous hydrogen sulfide prevents cardiomyocyte apoptosis from cardiac hypertrophy induced by isoproterenol Mol Cell Biochem 381 2013 41 50
36. H.F. Luan, Z.B. Zhao, Q.H. Zhao, P. Zhu, M.Y. Xiu, and Y. Ji Hydrogen sulfide postconditioning protects isolated rat hearts against ischemia and reperfusion injury mediated by the JAK2/STAT3 survival pathway Braz J Med Biol Res 45 2012 898 905
37. I.R.B. Mc, J.G. Timpa, A.R. Kurundkar, D.W. Holt, D.R. Kelly, and Y.E. Hartman Plasma concentrations of inflammatory cytokines rise rapidly during ECMO-related SIRS due to the release of preformed stores in the intestine Lab Investig 90 2010 128 139
38. B. McNally, R. Robb, M. Mehta, K. Vellano, A.L. Valderrama, and P.W. Yoon Out-of-hospital cardiac arrest surveillance - Cardiac Arrest Registry to Enhance Survival (CARES), United States, October 1, 2005-December 31, 2010 Morb Mortal Wkly Rep Surveill Summ 60 2011 1 19
39. S. Merkle, S. Frantz, M.P. Schon, J. Bauersachs, M. Buitrago, and R.J. Frost A role for caspase-1 in heart failure Circ Res 100 2007 645 653
40. E. Mezzaroma, S. Toldo, D. Farkas, I.M. Seropian, B.W. Van Tassell, and F.N. Salloum The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse Proc Natl Acad Sci U S A 108 2011 19725 19730
41. S. Minamishima, M. Bougaki, P.Y. Sips, J.D. Yu, Y.A. Minamishima, and J.W. Elrod Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice Circulation 120 2009 888 896
42. B.F. Moody, and J.W. Calvert Emergent role of gasotransmitters in ischemia-reperfusion injury Med Gas Res 1 2011 3
43. S.K. Ohri Systemic inflammatory response and the splanchnic bed in cardiopulmonary bypass Perfusion 11 1996 200 212
44. B. Ostadal, I. Ostadalova, and N.S. Dhalla Development of cardiac sensitivity to oxygen deficiency: Comparative and ontogenetic aspects Physiol Rev 79 1999 635 659
45. H. Pan, D. Chen, B. Liu, X. Xie, J. Zhang, and G. Yang Effects of sodium hydrosulfide on intestinal mucosal injury in a rat model of cardiac arrest and cardiopulmonary resuscitation Life Sci 93 2013 24 29
46. L.L. Pan, X.H. Liu, Q.H. Gong, and Y.Z. Zhu S-Propargyl-cysteine (SPRC) attenuated lipopolysaccharide-induced inflammatory response in H9c2 cells involved in a hydrogen sulfide-dependent mechanism Amino Acids 41 2011 205 215
47. T.T. Pan, K.L. Neo, L.F. Hu, Q.C. Yong, and J.S. Bian H2S preconditioning-induced PKC activation regulates intracellular calcium handling in rat cardiomyocytes Am J Physiol Cell Physiol 294 2008 C169 C177
48. A. Papapetropoulos, A. Pyriochou, Z. Altaany, G. Yang, A. Marazioti, and Z. Zhou Hydrogen sulfide is an endogenous stimulator of angiogenesis Proc Natl Acad Sci U S A 106 2009 21972 21977
49. B.F. Peake, C.K. Nicholson, J.P. Lambert, R.L. Hood, H. Amin, and S. Amin Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner Am J Physiol Heart Circ Physiol 304 2013 H1215 H1224
50. H.M. Piper, D. Garcia-Dorado, and M. Ovize A fresh look at reperfusion injury Cardiovasc Res 38 1998 291 300
51. D.J. Polhemus, K. Kondo, S. Bhushan, S.C. Bir, C.G. Kevil, and T. Murohara Hydrogen sulfide attenuates cardiac dysfunction after heart failure via induction of angiogenesis Circ Heart Fail 6 2013 1077 1086
52. D.J. Polhemus, and D.J. Lefer Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease Circ Res 114 2014 730 737
53. N. Qipshidze, N. Metreveli, P.K. Mishra, D. Lominadze, and S.C. Tyagi Hydrogen sulfide mitigates cardiac remodeling during myocardial infarction via improvement of angiogenesis Int J Biol Sci 8 2012 430 441
54. J.R. Rivers, A. Badiei, and M. Bhatia Hydrogen sulfide as a therapeutic target for inflammation Expert Opin Ther Targets 16 2012 439 449
55. R. Ross Atherosclerosis - An inflammatory disease N Engl J Med 340 1999 115 126
56. M. Rossi, G. Sganga, M. Mazzone, V. Valenza, S. Guarneri, and G. Portale Cardiopulmonary bypass in man: role of the intestine in a self-limiting inflammatory response with demonstrable bacterial translocation Ann Thorac Surg 77 2004 612 618
57. F.N. Salloum, V.Q. Chau, N.N. Hoke, A. Abbate, A. Varma, and R.A. Ockaili Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase g-dependent generation of hydrogen sulfide Circulation 120 2009 S31 S36
58. F.N. Salloum, A. Das, A. Samidurai, N.N. Hoke, V.Q. Chau, and R.A. Ockaili Cinaciguat, a novel activator of soluble guanylate cyclase, protects against ischemia/reperfusion injury: Role of hydrogen sulfide Am J Physiol Heart Circ Physiol 302 2012 H1347 H1354
59. F.N. Salloum, G.R. Sturz, C. Yin, S. Rehman, N.N. Hoke, and R.C. Kukreja Beetroot juice reduces infarct size and improves cardiac function following ischemia-reperfusion injury: Possible involvement of endogenous H2S Exp Biol Med 2014 pii: 1535370214558024
60. O. Sandanger, T. Ranheim, L.E. Vinge, M. Bliksoen, K. Alfsnes, and A.V. Finsen The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischaemia-reperfusion injury Cardiovasc Res 99 2013 164 174
61. F.J. Sheedy, E. Palsson-McDermott, E.J. Hennessy, C. Martin, J.J. O'Leary, and Q. Ruan Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21 Nat Immunol 11 2010 141 147
62. S. Shi, Q.S. Li, H. Li, L. Zhang, M. Xu, and J.L. Cheng Anti-apoptotic action of hydrogen sulfide is associated with early JNK inhibition Cell Biol Int 33 2009 1095 1101
63. A. Sivarajah, M. Collino, M. Yasin, E. Benetti, M. Gallicchio, and E. Mazzon Anti-apoptotic and anti-inflammatory effects of hydrogen sulfide in a rat model of regional myocardial I/R Shock 31 2009 267 274
64. P.M. Snijder, A.S. Frenay, R.A. de Boer, A. Pasch, J. Hillebrands, and H.G. Leuvenink Exogenous administration of thiosulfate, a donor of hydrogen sulfide, attenuates Angiotensin II-induced hypertensive heart disease in rats Br J Pharmacol 172 2014 1494 1504
65. N.R. Sodha, R.T. Clements, J. Feng, Y. Liu, C. Bianchi, and E.M. Horvath Hydrogen sulfide therapy attenuates the inflammatory response in a porcine model of myocardial ischemia/reperfusion injury J Thorac Cardiovasc Surg 138 2009 977 984
66. Y.W. Su, C. Liang, H.F. Jin, X.Y. Tang, W. Han, and L.J. Chai Hydrogen sulfide regulates cardiac function and structure in adriamycin-induced cardiomyopathy Circ J 73 2009 741 749
67. W.H. Sun, F. Liu, Y. Chen, and Y.C. Zhu Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion Biochem Biophys Res Commun 421 2012 164 169
68. C. Szabo, and A. Papapetropoulos Hydrogen sulphide and angiogenesis: Mechanisms and applications Br J Pharmacol 164 2011 853 865
69. S. Toldo, A. Das, E. Mezzaroma, V.Q. Chau, C. Marchetti, and D. Durrant Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice Circ - Cardiovasc Gene 7 2014 311 320
70. R. Wang Physiological implications of hydrogen sulfide: A whiff exploration that blossomed Physiol Rev 92 2012 791 896
71. X.Y. Wang, C.T. Yang, D.D. Zheng, L.Q. Mo, A.P. Lan, and Z.L. Yang Hydrogen sulfide protects H9c2 cells against doxorubicin-induced cardiotoxicity through inhibition of endoplasmic reticulum stress Mol Cell Biochem 363 2012 419 426
72. Y. Wang, X. Zhao, H. Jin, H. Wei, W. Li, and D. Bu Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice Arterioscler Thromb Vasc Biol 29 2009 173 179
73. D. Wu, Q. Hu, X. Liu, L. Pan, Q. Xiong, and Y.Z. Zhu Hydrogen sulfide protects against apoptosis under oxidative stress through SIRT1 pathway in H9c2 cardiomyocytes Nitric Oxide Biol Chem 46 2015 204 212
74. S. Xu, Z. Liu, and P. Liu Targeting hydrogen sulfide as a promising therapeutic strategy for atherosclerosis Int J Cardiol 172 2014 313 317
75. L.L. Yao, X.W. Huang, Y.G. Wang, Y.X. Cao, C.C. Zhang, and Y.C. Zhu Hydrogen sulfide protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis by preventing GSK-3beta-dependent opening of mPTP Am J Physiol Heart Circ Physiol 298 2010 H1310 H1319
76. X. Yao, G. Tan, C. He, Y. Gao, S. Pan, and H. Jiang Hydrogen sulfide protects cardiomyocytes from myocardial ischemia-reperfusion injury by enhancing phosphorylation of apoptosis repressor with caspase recruitment domain Tohoku J Exp Med 226 2012 275 285
77. Q.C. Yong, S.W. Lee, C.S. Foo, K.L. Neo, X. Chen, and J.S. Bian Endogenous hydrogen sulphide mediates the cardioprotection induced by ischemic postconditioning Am J Physiol Heart Circ Physiol 295 2008 H1330 H1340
78. X. Zhou, X. Lu, W. Xu, and J. Chen Protective effects of hydrogen sulfide against chronic alcohol intake-induced left ventricular remodeling in rats Cardiovasc Drugs Ther 27 2013 221 227
79. X.Y. Zhu, S.J. Liu, Y.J. Liu, S. Wang, and X. Ni Glucocorticoids suppress cystathionine gamma-lyase expression and H2S production in lipopolysaccharide-treated macrophages Cell Mol Life Sci 67 2010 1119 1132
80. X. Zhu, Z. Tang, B. Cong, J. Du, C. Wang, and L. Wang Estrogens increase cystathionine-gamma-lyase expression and decrease inflammation and oxidative stress in the myocardium of ovariectomized rats Menopause 20 2013 1084 1091
81. Z.R. Zunnunov Efficacy and safety of hydrogen sulfide balneotherapy in ischemic heart disease the arid zone Ter Arkh 76 2004 15 18