A tale of two gases: NO and H2S, foes or friends for life?

Redox Biology

Volumn 1, Issue 1, 2013, Pages 313-318

  Kolluru, Gopi K ^a   Shen, Xinggui ^a   Kevil, Christopher G ^a,b  

^a Louisiana State University School of Medicine Shreveport   (United States)

^b Department of Neurosurgery LSU Health Shreveport   (United States)

Author keywords

Cardiovascular disease; Chemistry; Redox biology; Thiol; Vascular biology

Indexed keywords

HYDROGEN SULFIDE; NITROGEN OXIDE; NITRIC OXIDE;

CARDIOVASCULAR SYSTEM; DISEASES; HUMAN; IMMUNE SYSTEM; MOLECULAR INTERACTION; NERVOUS TISSUE; NONHUMAN; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; METABOLISM;

HYDROGEN SULFIDE; NITRIC OXIDE; SIGNAL TRANSDUCTION;

EID: 84879584067     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.05.001     Document Type: Review

References (63)

1. Marsh N., Marsh A. A short history of nitroglycerine and nitric oxide in pharmacology and physiology. Clinical and Experimental Pharmacology and Physiology 2000, 27:313-319.
2. Kolluru G.K., Siamwala J.H., Chatterjee S. eNOS phosphorylation in health and disease. Biochimie 2010, 92:1186-1198.
3. Lundberg J.O., Weitzberg E., Gladwin M.T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nature Reviews Drug Discovery 2008, 7:156-167.
4. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews 1991, 43:109-142.
5. Li L., Rose P., Moore P.K. Hydrogen sulfide and cell signaling. Annual Review of Pharmacology and Toxicology 2011, 51:169-187.
6. Szabo C., Papapetropoulos A. Hydrogen sulphide and angiogenesis: mechanisms and applications. British Journal of Pharmacology 2011, 164:853-865.
7. Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiological Reviews 2012, 92:791-896.
8. 2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation 2013, 127:1116-1127.
9. Wang M.J., Cai W.J., Li N., Ding Y.J., Chen Y., Zhu Y.C. The hydrogen sulfide donor NaHS promotes angiogenesis in a rat model of hind limb ischemia. Antioxidants and Redox Signaling 2010, 12:1065-1077.
10. Cai W.J., Wang M.J., Moore P.K., Jin H.M., Yao T., Zhu Y.C. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovascular Research 2007, 76:29-40.
11. Kubo S., Kurokawa Y., Doe I., Masuko T., Sekiguchi F., Kawabata A. Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 2007, 241:92-97.
12. Li X.H., Du J.B., Bu D.F., Tang X.Y., Tang C.S. Sodium hydrosulfide alleviated pulmonary vascular structural remodeling induced by high pulmonary blood flow in rats. Acta Pharmacologica Sinica 2006, 27:971-980.
13. Prathapasinghe G.A., Siow Y.L., Xu Z., O K. Inhibition of cystathionine-beta-synthase activity during renal ischemia-reperfusion: role of pH and nitric oxide. American Journal of Physiology-Renal Physiology 2008, 295:F912-F922.
14. Wang Y.F., Mainali P., Tang C.S., Shi L., Zhang C.Y., Yan H., Liu X.Q., Du J.B. Effects of nitric oxide and hydrogen sulfide on the relaxation of pulmonary arteries in rats. Chinese Medical Journal (England) 2008, 121:420-423.
15. Bir S.C., Kolluru G.K., McCarthy P., Shen X., Pardue S., Pattillo C.B., Kevil C.G. Hydrogen sulfide stimulates ischemic vascular remodeling through nitric oxide synthase and nitrite reduction activity regulating hypoxia-inducible factor-1α and vascular endothelial growth factor-dependent angiogenesis. Journal of the American Heart Association 2012.
16. Gu Q., Wang B., Zhang X.F., Ma Y.P., Liu J.D., Wang X.Z. Contribution of hydrogen sulfide and nitric oxide to exercise-induced attenuation of aortic remodeling and improvement of endothelial function in spontaneously hypertensive rats. Molecular and Cellular Biochemistry 2013, 375:199-206.
17. Coletta C., Papapetropoulos A., Erdelyi K., Olah G., Modis K., Panopoulos P., Asimakopoulou A., Gero D., Sharina I., Martin E., Szabo C. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proceedings of the National Academy of Sciences of USA 2012, 109:9161-9166.
18. Predmore B.L., Kondo K., Bhushan S., Zlatopolsky M.A., King A.L., Aragon J.P., Grinsfelder D.B., Condit M.E., Lefer D.J. The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability. American Journal of Physiology. Heart and Circulatory Physiology 2012, 302:H2410-H2418.
19. Kida M., Sugiyama T., Yoshimoto T., Ogawa Y. Hydrogen sulfide increases nitric oxide production with calcium-dependent activation of endothelial nitric oxide synthase in endothelial cells. European Journal of Pharmaceutical Sciences 2013, 48:211-215.
20. Yong Q.C., Hu L.F., Wang S., Huang D., Bian J.S. Hydrogen sulfide interacts with nitric oxide in the heart: possible involvement of nitroxyl. Cardiovascular Research 2010, 88:482-491.
21. Lei Y.P., Liu C.T., Sheen L.Y., Chen H.W., Lii C.K. Diallyl disulfide and diallyl trisulfide protect endothelial nitric oxide synthase against damage by oxidized low-density lipoprotein. Molecular Nutrition and Food Research 2010, 54(Suppl 1):S42-S52.
22. Yong Q.C., Lee S.W., Foo C.S., Neo K.L., Chen X., Bian J.S. Endogenous hydrogen sulphide mediates the cardioprotection induced by ischemic postconditioning. American Journal of Physiology. Heart and Circulatory Physiology 2008, 295:H1330-H1340.
23. Sojitra B., Bulani Y., Putcha U.K., Kanwal A., Gupta P., Kuncha M., Banerjee S.K. Nitric oxide synthase inhibition abrogates hydrogen sulfide-induced cardioprotection in mice. Molecular and Cellular Biochemistry 2012, 360:61-69.
24. Eto K., Kimura H. A novel enhancing mechanism for hydrogen sulfide-producing activity of cystathionine beta-synthase. Journal of Biological Chemistry 2002, 277:42680-42685.
25. Li H., Marshall Z.M., Whorton A.R. Stimulation of cystine uptake by nitric oxide: regulation of endothelial cell glutathione levels. American Journal of Physiology 1999, 276:C803-C811.
26. Liew H.C., Khoo H.E., Moore P.K., Bhatia M., Lu J., Moochhala S.M. Synergism between hydrogen sulfide (H(2)S) and nitric oxide (NO) in vasorelaxation induced by stonustoxin (SNTX), a lethal and hypotensive protein factor isolated from stonefish Synanceja horrida venom. Life Science 2007, 80:1664-1668.
27. Geng B., Cui Y., Zhao J., Yu F., Zhu Y., Xu G., Zhang Z., Tang C., Du J. Hydrogen sulfide downregulates the aortic l-arginine/nitric oxide pathway in rats. American Journal of Physiology-Regulatory, Integrative, and Comparative Physiology 2007, 293:R1608-R1618.
28. Oh G.S., Pae H.O., Lee B.S., Kim B.N., Kim J.M., Kim H.R., Jeon S.B., Jeon W.K., Chae H.J., Chung H.T. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radical Biology and Medicine 2006, 41:106-119.
29. Calvert J.W., Jha S., Gundewar S., Elrod J.W., Ramachandran A., Pattillo C.B., Kevil C.G., Lefer D.J. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circulation Research 2009, 105:365-374.
30. Peake B.F., Nicholson C.K., Lambert J.P., Hood R.L., Amin H., Amin S., Calvert J.W. Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner. American Journal of Physiology. Heart and Circulatory Physiology 2013, 304:H1215-H1224.
31. Muzaffar S., Shukla N., Bond M., Newby A.C., Angelini G.D., Sparatore A., Del Soldato P., Jeremy J.Y. Exogenous hydrogen sulfide inhibits superoxide formation, NOX-1 expression and Rac1 activity in human vascular smooth muscle cells. Journal of Vascular Research 2008, 45:521-528.
32. Yusof M., Kamada K., Kalogeris T., Gaskin F.S., Korthuis R.J. Hydrogen sulfide triggers late-phase preconditioning in postischemic small intestine by an NO- and p38 MAPK-dependent mechanism. American Journal of Physiology. Heart and Circulatory Physiology 2009, 296:H868-H876.
33. Friebe A., Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circulation Research 2003, 93:96-105.
34. Bucci M., Papapetropoulos A., Vellecco V., Zhou Z., Pyriochou A., Roussos C., Roviezzo F., Brancaleone V., Cirino G. Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arteriosclerosis, Thrombosis, and Vascular Biology 2010, 30:1998-2004.
35. Dombkowski R.A., Russell M.J., Schulman A.A., Doellman M.M., Olson K.R. Vertebrate phylogeny of hydrogen sulfide vasoactivity. American Journal of Physiology-Regulatory, Integrative, and Comparative Physiology 2005, 288:R243-R252.
36. Webb G.D., Lim L.H., Oh V.M., Yeo S.B., Cheong Y.P., Ali M.Y., El Oakley R., Lee C.N., Wong P.S., Caleb M.G., Salto-Tellez M., Bhatia M., Chan E.S., Taylor E.A., Moore P.K. Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. Journal of Pharmacology and Experimental Therapeutics 2008, 324:876-882.
37. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995, 377:239-242.
38. 2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008, 322:587-590.
39. Arnelle D.R., Stamler J.S. NO+, NO, and NO- donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Archives of Biochemistry and Biophysics 1995, 318:279-285.
40. Mustafa A.K., Gadalla M.M., Sen N., Kim S., Mu W., Gazi S.K., Barrow R.K., Yang G., Wang R., Snyder S.H. H2S signals through protein S-sulfhydration. Science Signaling 2009, 2. ra72.
41. Stamler J.S., Simon D.I., Osborne J.A., Mullins M.E., Jaraki O., Michel T., Singel D.J., Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proceedings of the National Academy of Sciences of USA 1992, 89:444-448.
42. Finkel T. From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Science Signaling 2012, 5. pe10.
43. Lancaster J.R. Protein cysteine thiol nitrosation: maker or marker of reactive nitrogen species-induced nonerythroid cellular signaling?. Nitric Oxide 2008, 19:68-72.
44. Chen Y.Y., Chu H.M., Pan K.T., Teng C.H., Wang D.L., Wang A.H., Khoo K.H., Meng T.C. Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation. Journal of Biological Chemistry 2008, 283:35265-35272.
45. Krishnan N., Fu C., Pappin D.J., Tonks N.K. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Science Signaling 2011, 4. ra86.
46. Paul B.D., Snyder S.H. H(2)S signalling through protein sulfhydration and beyond. Nature Reviews Molecular Cell Biology 2012, 13:499-507.
47. Sen N., Paul B.D., Gadalla M.M., Mustafa A.K., Sen T., Xu R., Kim S., Snyder S.H. Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Molecular Cell 2012, 45:13-24.
48. Hosoki R., Matsuki N., Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochemical and Biophysical Research Communications 1997, 237:527-531.
49. Whiteman M., Armstrong J.S., Chu S.H., Jia-Ling S., Wong B.S., Cheung N.S., Halliwell B., Moore P.K. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'?. Journal of Neurochemistry 2004, 90:765-768.
50. Ali M.Y., Ping C.Y., Mok Y.Y., Ling L., Whiteman M., Bhatia M., Moore P.K. Regulation of vascular nitric oxide in vitro and in vivo: a new role for endogenous hydrogen sulphide?. British Journal of Pharmacology 2006, 149:625-634.
51. Whiteman M., Li L., Kostetski I., Chu S.H., Siau J.L., Bhatia M., Moore P.K. Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochemical and Biophysical Research Communications 2006, 343:303-310.
52. Bruce King S. Potential biological chemistry of hydrogen sulfide (H2S) with the nitrogen oxides. Free Radical Biology and Medicine 2013, 55:1-7.
53. Filipovic M.R., Eberhardt M., Prokopovic V., Mijuskovic A., Orescanin-Dusic Z., Reeh P., Ivanovic-Burmazovic I. Beyond H(2)S and NO interplay: hydrogen sulfide and nitroprusside react directly to give nitroxyl (HNO). A new pharmacological source of HNO. Journal of Medicinal Chemistry 2013.
54. Filipovic M.R., Ivanovic-Burmazovic I. The kinetics and character of the intermediates formed in the reaction between sodium nitroprusside and hydrogen sulfide need further clarification. Chemistry 2012, 18:13538-13540.
55. Filipovic M.R., Miljkovic J., Allgauer A., Chaurio R., Shubina T., Herrmann M., Ivanovic-Burmazovic I. Biochemical insight into physiological effects of H(2)S: reaction with peroxynitrite and formation of a new nitric oxide donor, sulfinyl nitrite. Biochemical Journal 2012, 441:609-621.
56. 2S and S-nitrosothiols. Journal of the American Chemical Society 2012, 134:12016-12027.
57. Schmidt H.H., Hofmann H., Schindler U., Shutenko Z.S., Cunningham D.D., Feelisch M. No NO from NO synthase. Proceedings of the National Academy of Sciences of USA 1996, 93:14492-14497.
58. Sharpe M.A., Cooper C.E. Reactions of nitric oxide with mitochondrial cytochrome c: a novel mechanism for the formation of nitroxyl anion and peroxynitrite. Biochemical Journal 1998, 332(Pt 1):9-19.
59. Donzelli S., Espey M.G., Flores-Santana W., Switzer C.H., Yeh G.C., Huang J., Stuehr D.J., King S.B., Miranda K.M., Wink D.A. Generation of nitroxyl by heme protein-mediated peroxidation of hydroxylamine but not N-hydroxy-L-arginine. Free Radical Biology and Medicine 2008, 45:578-584.
60. Irvine J.C., Ritchie R.H., Favaloro J.L., Andrews K.L., Widdop R.E., Kemp-Harper B.K. Nitroxyl (HNO): the Cinderella of the nitric oxide story. Trends in Pharmacological Sciences 2008, 29:601-608.
61. Lin E.Q., Irvine J.C., Cao A.H., Alexander A.E., Love J.E., Patel R., McMullen J.R., Kaye D.M., Kemp-Harper B.K., Ritchie R.H. Nitroxyl (HNO) stimulates soluble guanylyl cyclase to suppress cardiomyocyte hypertrophy and superoxide generation. PLoS One 2012, 7:e34892.
62. Hewett S.J., Espey M.G., Uliasz T.F., Wink D.A. Neurotoxicity of nitroxyl: insights into HNO and NO biochemical imbalance. Free Radical Biology and Medicine 2005, 39:1478-1488.
63. Paolocci N., Jackson M.I., Lopez B.E., Miranda K., Tocchetti C.G., Wink D.A., Hobbs A.J., Fukuto J.M. The pharmacology of nitroxyl (HNO) and its therapeutic potential: not just the janus face of NO. Pharmacology and Therapeutics 2007, 113:442-458.