Nitrosopersulfide (SSNO-) accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide

Redox Biology

Volumn 2, Issue 1, 2014, Pages 234-244

  Cortese Krott, Miriam M ^a   Fernandez, Bernadette O ^b   Santos, José L T ^b   Mergia, Evanthia ^c   Grman, Marian ^d   Nagy, Péter ^e   Kelm, Malte ^a   Butler, Anthony ^f   Feelisch, Martin ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d INSTITUTE OF MOLECULAR PHYSIOLOGY AND GENETICS   (Slovakia)

^e NATIONAL INSTITUTE OF ONCOLOGY   (Hungary)

^f UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

CGMP; HSNO; Hydrogen sulfide; Nitric oxide; Nitroxyl; Polysulfides

Indexed keywords

CYCLIC GMP; GUANYLATE CYCLASE; HYDROGEN SULFIDE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NITROUS OXIDE; OXYGEN; PHOSPHODIESTERASE; S NITROSOTHIOL; SULFIDE; GYY 4137; HYDRODISULFIDE; NITRITE; NITROSO DERIVATIVE; NITROSOPERSULFIDE; S NITROSOPENICILLAMINE; SOLUBLE GUANYLATE CYCLASE; THIONITRITE; UNCLASSIFIED DRUG; CELL RECEPTOR; MORPHOLINE DERIVATIVE; NITRIC OXIDE DONOR; PERSULFIDES; PHOSPHOROTHIOIC ACID DERIVATIVE; S-NITROSOPENICILLAMINE; SOLUBLE GUANYLYL CYCLASE;

AQUEOUS SOLUTION; ARTICLE; BIOLOGICAL ACTIVITY; CHEMICAL INTERACTION; CHEMICAL REACTION; CHEMOLUMINESCENCE; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REGULATORY SEQUENCE; SOLID PHASE SYNTHESIS; ULTRAVIOLET SPECTROSCOPY; ANIMAL CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DECOMPOSITION; DOSE RESPONSE; ENZYME ACTIVATION; GAS PHASE CHEMILUMINESCENCE; KINETICS; NONHUMAN; PH; SOLID PHASE TRANSNITROSATION; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; RAT;

ANIMALS; CELL LINE; CYCLIC GMP; GUANYLATE CYCLASE; MORPHOLINES; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROSO COMPOUNDS; ORGANOTHIOPHOSPHORUS COMPOUNDS; OXYGEN CONSUMPTION; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; S-NITROSOTHIOLS; SULFIDES;

EID: 84893371806     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.12.031     Document Type: Article

References (59)

1. Li L., Rose P., Moore P.K. Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol. 2011, 51(2011):169-187.
2. Olson K.R.A. Practical look at the chemistry and biology of hydrogen Sulfide. Antioxid. Redox. Signal. 2012, 17:32-44.
3. 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. Circ. Res. 2009, 105:365-374.
4. Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol. Rev. 2012, 92:791-896.
5. Fukuto J.M., Carrington S.J., Tantillo D.J., Harrison J.G., Ignarro L.J., Freeman B.A., Chen A., Wink D.A. Small molecule signaling agents: the integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species. Chem. Res. Toxicol. 2012, 25:769-793.
6. 2S be the third endogenous gaseous transmitter?. Faseb J. 2002, 16:1792-1798.
7. Feelisch M., Olson K.R. Embracing sulfide and CO to understand nitric oxide biology. Nitric Oxide: Biol. Chem./Off. J. Nitric Oxide Soc. 2013, 35:2-4.
8. Morse J.W., Millero F.J., Cornwell J.C., Rickard D. The chemistry of the hydrogen sulfide and iron sulfide systems in natural waters. Earth-Sci. Rev. 2002, 24:1-42.
9. Nagy P., Palinkas Z., Nagy A., Budai B., Toth I., Vasas A. Chemical aspects of hydrogen sulfide measurements in physiological samples. Biochim. Biophys. Acta 1840, 876-891:2014.
10. 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?. Br. J. Pharmacol. 2006, 149:625-634.
11. 2S gas biology. Antioxid. Redox Signal. 2010, 13:157-192.
12. Shatalin K., Shatalina E., Mironov A., Nudler E. H2S: A universal defense against antibiotics in bacteria. Science (New York, N.Y.) 2011, 334:986-990.
13. Yoon P.J., Parajuli S.P., Zuo D.C., Shahi P.K., Oh H.J., Shin H.R., Lee M.J., Yeum C.H., Choi S., Jun J.Y. Interplay of hydrogen sulfide and nitric oxide on the pacemaker activity of interstitial cells of cajal from mouse small intestine. Chonnam Med. J. 2011, 47:72.
14. 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. Cardiovasc. Res. 2010, 88:482-491.
15. Kolluru G.K., Shen X., Bir S.C., Kevil C.G. Hydrogen sulfide chemical biology: Pathophysiological roles and detection. Nitric Oxide: Biol. Chem./Off. J. Nitric Oxide Soc. 2013, 35:5-20.
16. 2S, foes or friends for life?. Redox Biol. 2013, 1:313-318.
17. Bruce King S. Potential biological chemistry of hydrogen sulfide (H2S) with the nitrogen oxides. Free Radic. Biol. Med. 2013, 55:1-7.
18. Li Q., Lancaster J.R. Chemical foundations of hydrogen sulfide biology. Nitric Oxide: Biol. Chem./Off. J. Nitric Oxide Soc. 2013, 35C:21-34.
19. Yang G., Wu L., Jiang B., Yang W., Qi J., Cao K., Meng Q., Mustafa A.K., Mu W., Zhang S., Snyder S.H., Wang R. H(2)S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008, 322:587-590.
20. Wang R. Signaling pathways for the vascular effects of hydrogen sulfide. Curr. Opin. Nephrol. Hypertens. 2011, 20:107-112.
21. 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. Biochem. Biophys. Res. Commun. 2006, 343:303-310.
22. Yong Q.C., Cheong J.L., Hua F., Deng L.W., Khoo Y.M., Lee H.S., Perry A., Wood M., Whiteman M., Bian J.S. Regulation of heart function by endogenous gaseous mediators-crosstalk between nitric oxide and hydrogen sulfide. Antioxid. Redox Signal. 2011, 14:2081-2091.
23. Williams D.L.H. Nitrosation reactions and the chemistry of nitric oxide 2004, Elsevier, Amsterdam, The Netherlands.
24. 2S and S-nitrosothiols. J. Am. Chem. Soc. 2012, 134:12016-12027.
25. Nonella M., Huber R., Ha T.-K. Photolytic preparation and isomerization of HNSO, HOSN, HSNO, and HONS in an argon matrix. An experimental and theoretical study. J. Phys. Chem. 1987, 91:5203-5209.
26. Ondrias K., Stasko A., Cacanyiova S., Sulova Z., Krizanova O., Kristek F., Malekova L., Knezl V., Breier A. H(2)S and HS(-) donor NaHS releases nitric oxide from nitrosothiols, metal nitrosyl complex, brain homogenate and murine L1210 leukaemia cells. Pflügers Archiv. Eur. J. Physiol. 2008, 457:271-279.
27. Teng X., Scott Isbell T., Crawford J.H., Bosworth C.A., Giles G.I., Koenitzer J.R., Lancaster J.R., Doeller J.E., W Kraus D., Patel R. Novel method for measuring S-nitrosothiols using hydrogen sulfide. Methods Enzymol. 2008, 441:161-172.
28. 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. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1998-2004.
29. Kraft P.J., Haynes-Johnson D., Bhattacharjee S., Lundeen S.G., Qiu Y. Altered activities of cyclic nucleotide phosphodiesterases and soluble guanylyl cyclase in cultured RFL-6 cells. Int. J. Biochem. Cell. Biol. 2004, 36:2086-2095.
30. Stamler J., Feelisch M. Preparation and detection of S-nitrosothiols. Methods in Nitric Oxide Research 1996, 521-539. John Wiley & Sons, Chichester. M. Feelisch, J. Stamler (Eds.).
31. Ishii K., Sheng H., Warner T.D., Förstermann U., Murad F. A simple and sensitive bioassay method for detection of EDRF with RFL-6 rat lung fibroblasts. Am. J. Physiol.- Heart Circulatory Physiol. 1991, 261:H598-H603.
32. Noack E., Feelisch M. Molecular mechanisms of nitrovasodilator bioactivation. Basic. Res. Cardiol. 1991, 86(2):37-50.
33. Riego J.A., Broniowska K.A., Kettenhofen N.J., Hogg N. Activation and inhibition of soluble guanylyl cyclase by S-nitrosocysteine: involvement of amino acid transport system L. Free Rad. Biol. Med. 2009, 47:269-274.
34. Fernhoff N.B., Derbyshire E.R., Underbakke E.S., Marletta M.A. Heme-assisted S-nitrosation desensitizes ferric soluble guanylate cyclase to nitric oxide. J. Biol. Chem. 2012, 287:43053-43062.
35. McAninly J., Williams D.L.H., Askew S.C., Butler A.R., Russell C. Metal ion catalysis in nitrosothiol (RSNO) decomposition. J. Chem. Soc. Chem. Commun. 1993, 1758-1759.
36. Seel F., Wagner M. Reaction of sulfides with nitrogen monoxide in aqueous solution. Z. Anorg. Allg. Chem. 1988, 558:189-192.
37. Munro A.P., Williams D.L.H. Reactivity of sulfur nucleophiles towards S-nitrosothiols. J. Chem. Soc., Perkin Trans. 2000, 2:1794-1797.
38. Seel F., Wagner M. The reaction of polysulfides with nitrogen monoxide in non-acqueous solvents- nitrosodisulfides. Z. Naturforsch 1985, 40:762.
39. 2S-derived signaling molecules in rat brain. Faseb J. 2013, 27:2451-2457.
40. 2S to protein thiol oxidation. Antioxid. Redox Signal. 2013, 19:1749-1765.
41. Williams D.L.H. The chemistry of S-nitrosothiols. Acc. Chem. Res. 1999, 32:869-876.
42. Timerghazin Q.K., Peslherbe G.H., English A.M. Structure and stability of HSNO, the simplest S-nitrosothiol. Phys. Chem. Chem. Phys. 2008, 10:1532-1539.
43. Seel F., Kuhn R., Simon G., Wagner M., Krebs B., Dartmann M. PNP-Perthionitrit und PNP-Monothionitrit. Zeitschrift für Naturforschung. Teil b, Anorg. Chemie, Org. Chem. 1985, 40:1607-1617.
44. Goehring M., Messner J. Zur Kenntnis der schwefligen Säure. III Das Sulfinimid und seine Isomeren. Z. Anorg. Allg. Chem. 1952, 268:47-56.
45. Müller R.P., Nonella M., Huber J.R. Spectroscopic investigation of HSNO in a low temperature matrix. UV, vis, and IR-induced isomerisations. Chem. Phys. 1984, 87:351-361.
46. Pino R.Z., Feelisch M. Bioassay discrimination between nitric oxide (NO.) and nitroxyl (NO-) using l-cysteine. Biochem. Biophys. Res. Commun. 1994, 201:54-62.
47. 2S biology. Arch. Biochem. Biophys. 2011, 516:146-153.
48. Kamyshny A., Gun J., Rizkov D., Voitsekovski T., Lev O. Equilibrium distribution of polysulfide ions in aqueous solutions at different temperatures by rapid single phase derivatization. Environ. Sci. Technol. 2007, 41:2395-2400.
49. Littlejohn D., Hu K.Y., Chang S.G. Kinetics of the reaction of nitric oxide with sulfite and bisulfite ions in aqueous solution. Inorg. Chem. 1986, 25:3131-3135.
50. Olson K.R., Whitfield N.L. Hydrogen sulfide and oxygen sensing in the cardiovascular system. Antioxid. Redox Signal. 2010, 12:1219-1234.
51. Bucci M., Papapetropoulos A., Vellecco V., Zhou Z., Zaid A., Giannogonas P., Cantalupo A., Dhayade S., Karalis K.P., Wang R., Feil R., Cirino G. cGMP-Dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS ONE 2012, 7:e53319.
52. Coletta C., Papapetropoulos A., Erdelyi K., Olah G., Módis K., Panopoulos P., Asimakopoulou A., Gerö D., Sharina I., Martin E. 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.
53. Cai W., Wang M., Moore P., Jin H., Yao T., Zhu Y. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc. Res. 2007, 76:29-40.
54. Honda A., Adams S.R., Sawyer C.L., Lev-Ram V., Tsien R.Y., Dostmann W.R.G. Spatiotemporal dynamics of guanosine 3',5'-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc. Natl. Acad. Sci. 2001, 98:2437-2442.
55. Broniowska K.A., Hogg N. The chemical biology of S-nitrosothiols. Antioxid. Redox Signal. 2012, 17:969-980.
56. Rodriguez J., Maloney R.E., Rassaf T., Bryan N.S., Feelisch M. Chemical nature of nitric oxide storage forms in rat vascular tissue. Proc. Natl. Acad. Sci. U. S. A. 2002, 100:336-341.
57. Levitt M.D., Abdel-Rehim M.S., Furne J. Free and acid-labile hydrogen sulfide concentrations in mouse tissues: anomalously high free hydrogen sulfide in aortic tissue. Antioxid. Redox Signal. 2011, 15:373-378.
58. Kimura H. Production and physiological effects of hydrogen sulfide. Antioxid. Redox Signal. 2013.
59. Szabó C., Papapetropoulos A. Hydrogen sulphide and angiogenesis: mechanisms and applications. Br. J. Pharmacol. 2011, 164:853-865.