Hydrogen sulfide is a signaling molecule and a cytoprotectant

Antioxidants and Redox Signaling

Volumn 17, Issue 1, 2012, Pages 45-57

  Kimura, Hideo ^a   Shibuya, Norihiro ^a   Kimura, Yuka ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 MERCAPTOPYRUVATE SULFURTRANSFERASE; 3 MERCAPTOPYRUVIC ACID; AQUAPORIN; CALCIUM; CYSTEINE AMINOTRANSFERASE; CYSTEINE DERIVATIVE; DIHYDROLIPOATE; FLUORESCENT DYE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; HYDROGEN SULFIDE; LEUKEMIA INHIBITORY FACTOR; NITRIC OXIDE; SULFUR; THIOREDOXIN; UNCLASSIFIED DRUG;

CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL STIMULATION; CHROMOSOME PAIRING; ENZYME ACTIVITY; ENZYME MODIFICATION; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CYSTATHIONINE GAMMA-LYASE; CYTOPROTECTION; HUMANS; HYDROGEN SULFIDE; SIGNAL TRANSDUCTION; TRANSAMINASES;

EID: 84860761445     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4345     Document Type: Review

References (82)

1. Abe K and Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071, 1996.
2. Aizenman E, Lipton DA, and Loring RH. Selective modulation of NMDA responses by reduction and oxidation. Neuron 2: 1257-1263, 1989.
3. Basker R and Bian J. Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656: 5-9, 2011.
4. Braunstein AE, Goryachenkowa EV, Tolosa EA, Willhardt IH, and Yefremova LL. Specificity and some other properties of liver serine sulphhydrase: Evidence for its identity with cystathionine b-synthase. BiochimBiophys Acta 242: 247-260, 1971.
5. Caliendo G, Cirino G, Santagada V, and Wallace JL. Synthesis and biological effects of hydrogen sulfide (H2S): Development of H2S-releasing drugs as pharmaceuticals. J Med Chem 53: 6275-6286, 2010.
6. Calvert JW Jha S, Gundewar S, Elrod JW Ramachandran A, Pattillo CB, Kevil CG, and Lefer DJ. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105: 365-374, 2009.
7. Cavallini D, Mondovi B, De Marco C, and Scioscia-Santoro A. The mechanism of desulphhydration of cysteine. Enzymologia 24: 253-266, 1962.
8. Chen X, Jhee KH, and Kruger WD. Production of the neuromodulator H2S by cystathionine beta-synthase via the condensation of cysteine and homocysteine. J Biol Chem 279: 52082-52086, 2004.
9. Cheung NS, Peng ZF, Chen MJ, and Moore PK. Hydrogen sulfide induced neuronal death occurs via glutamate receptor and is associated with calpain activation and lysosomal rupture in mouse primary cortical neurons. Neuropharmacology 53: 505-514, 2007.
10. Chiku T, Padovani D, Zhu W, Singh S, Vitvitsky V, and Banerjee R. H2S biogenesis by human cystathionine clyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J Biol Chem 284: 11601-11612, 2009.
11. Cooper AJL. Biochemistry of sulfur-containing amino acids. Annu Rev Biochem 52: 187-222, 1983.
12. Dani JW, Chernjavsky A, and Smith SJ. Neuronal activity triggers calcium waves in hipp9ocampal astrocyte networks. Neuron 8: 429-440, 1992.
13. Dello Russo C, Tringali G, Ragazzoni E, Maggiano N, Menini E, Vairano M, Preziosi P, and Navarra P. Evidence that hydrogen sulphide can modulate hypothalamo-pituitaryadrenal axis function: In vitro and in vivo studies in the rat. J Neuroendocrinol 12: 225-233, 2000.
14. Dombkowski RA, Russell MJ, and Olson KR. Hydrogen sulfide as an endogenous regulator of vascular smooth muscle tone in trout. Am J Physiol Regul Integr Comp Physiol 286: R678-685, 2004.
15. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104: 15560-15565, 2007.
16. Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, and Kimura H. Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. FASEB J 19: 1854-1856, 2005.
17. Finkelstein JD. Methionine metabolism in mammals. J Nutr Biochem 1: 228-237, 1990.
18. Furne J, Saeed A, and Levitt MD. Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am J Physiol Regul Integr Comp Physiol 295: R1479-R1498, 2008.
19. Gadalla MM and Snyder SH. Hydrogen sulfide as a gasotransmitter. J Neurochem 113: 14-26, 2010.
20. Goodwin LR, Francom D, Dieken FP, Taylor JD, Warenycia MW, Reiffenstein RJ, and Dowling G. Determination of sulfidein brain tissue by gas dialysis/ion chromatography: Postmortem studies and two case reports. J Anal Toxicol 13: 105-109, 1989.
21. Griffith OW. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 27: 922-935, 1999.
22. Hosoki R, Matsuki N, and Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237: 527-531, 1997.
23. Ichinohe A, Kanaumi T, Takashima S, Enokido Y, Naai Y, and Kimura H. Cystathionine beta-synthase is enriched in the brains of Down's patients. Biochem Biophys Res Commun 338: 1547-1550, 2005.
24. Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K, and Kimura H. A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid Redox Signal 11: 205-214, 2009.
25. Ishii I, Akahoshi N, Yamada H, Nakano S, Izumi T, and Suematsu M. Cystathionine c-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J Biol Chem 285: 26358-26368, 2010.
26. Ishii I, Akahoshi N, Yu X-N, Kobayashi Y, Namekata K, Komaki G, and Kimura H. Murine cystathionine c-lyase: Complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem J 381: 113-123, 2004.
27. Jocelyn PC. The standard redox potential of cysteine-cystine form the thiol-disulphide exchange reaction with glutathione and lipoic acid. Eur J Biochem 2: 327-331, 1967.
28. Junier MP, Coulpier M, Le Forestier N, Cadusseau J, Suzuki F, Peschanski M, and Dreyfus PA. Transforming growth factor alpha expression in degenerating motoneurons of the murine mutant wobbler: A neuronal signal for astrogliosis? J Neurosci 14: 4206-4216, 1994.
29. Kato A, Ogura M, and Suda M. Control mechanism in the rat liver enzyme system converting L-methionine to Lcystine. Noncompetitive inhibition of cystathionine synthetase-serine dehydratase by elemental sulfur and competitive inhibition of cystathionine-homoserine dehydratase by L-cysteine and L-cystine. J Biochem 59: 40-48, 1966.
30. Kimura Y, Dargusch R, Schubert D, and Kimura H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal 8: 661-670, 2006.
31. Kimura Y, Goto Y-I, and Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal 12: 1-13, 2010.
32. Kimura Y and Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18: 1165-1167, 2004.
33. Kombian SB, Warenycia MW, Mele FG, and Reiffenstein RJ. Effects of acute intoxication with hydrogen sulfide on central amino acid transmitter systems. NeuroToxicology 9: 587-596, 1988.
34. Lee JK, Kozono D, Remis J, Kitagawa Y, Agre P, and Stroud RM. Structural basis for conductance by the archaeal aquaporin AsqpM at 1.68 A. Proc Natl Acad Sci USA 102: 18932-18937, 2005.
35. Lee M, Tazzari V, Glustarini D, Rossi R, Sparatore A, Soldato PD, McGeer E, and McGeer PL. Effects of hydrogen sulfide-releasing L-DOPA derivatives on glial activation. J Biol Chem 285: 17318-17328, 2010.
36. Levitt MD, Abdel-Rehim MS, and Furne J. Free and acidlabile hydrogen sulfide concentrations in mouse tissues: Anomalously high free hydrogen sulfide in aortic tissue. Antioxid Redox Signal 15: 373-378, 2011.
37. Lin MT and Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795, 2006.
38. Lippert AR, New EJ, and Chang CJ. Re-based fluorescent probes for selective imaging of hydrogen sulfide in living cells. J Am Chem Soc 133: 10078-10080, 2010.
39. Liu C, Pan J, Li S, Zhao Y, Wu LY, Berkman CE, Whorton AR, and Xian M. Capture and visualization of hydrogen sulfide by a fluorescent probe. Angew Chem Int Ed 50: 10327-10329, 2011.
40. Mathai JC, Missner A, Kugler P, Saparov SM, Zeidel ML, Lee JK, and Pohl P. No facilitator required for membrane transport of hydrogen sulfide. Proc Natl Acad Sci USA 106: 16633-16638, 2009.
41. Meister A, Fraser PE, and Tice SV. Enzymatic desulfuration of b-mercaptopyruvate to pyruvate. J Biol Chem 206: 561-575, 1954.
42. Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, and Kimura H. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439: 479-485, 2011.
43. Mikami Y, Shibuya N, Kimura Y, Nagahara N, Yamada M, and Kimura H. Hydrogen sulfide protects the retina from light-induced degeneration by the modulation of Ca2 + influx. J Biol Chem 286: 39379-39386, 2011.
44. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, and Snyder SH. H2S signals through protein S-sulfhydration. Sci Signal 2: ra72, 2009.
45. Nagahara N, Ito T, Kitamura H, and Nishino T. Tissue and subcellular distribution of mercaptopyruvate sulfurtransferase in the rat: Confocal laser fluorescence and immunoelectron microscopic studies combined with biochemical analysis. Histochem Cello Biol 110: 243-250, 1998.
46. Nagahara N, Okazaki T, and Nishino T. Cytosolic mercaptypyruvate sulfurtransferase is evolutionarily related to mitochondrial rhodanese. Striking similarity in active site amino acid sequence and the increase in the mercaptopyruvate sulfurtransferase activity of rhodanese by site-directed mutagenesis. J Biol Chem 270: 16230-16235, 1995.
47. Nagai Y, Tsugane M, Oka J, and Kimura H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18: 557-559, 2004.
48. O'Dell TJ, Hawkins RD, Kandel ER, and Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: Evidence for nitric oxide as a possible early retrograde messenger. Proc Natl Acad Sci USA 88: 11285-1289, 1991.
49. Olson KR, Whitfield NL, Bearden SE, Leger JS, Nilson E, Gao Y, and Maddeen JA. Hypoxic pulmonary vasodilation: A paradigm shift with a hydrogen sulfide mechanism. Am J Physiol Regal Integr Comp Physiol 298: R51-R60, 2010.
50. Peng H, Cheng Y, Dai C, King AL, Predmore BL, Lefer DJ, and Wang B. A fluorescent probe for fast and quantitaqtive detection of hydrogen sulfide in blood. Angew Chem Int Ed 50: 9672-9675, 2011.
51. Predmore BL and Lefer DJ. Development of hydrogen sulfide-based therapeutics for cardiovascular disease. J Cardiovasc Transl Res 3: 487-498, 2010.
52. Qian Y, Karpus J, KIabil O, Zhang S-Y, Zhu H-L, Banerjee R, Zhao J and He C. Selective fluorescent probes for live-cell monitoring of sulphide. Nat Commun 2-495, 2011.
53. Reiffenstein RJ, Hulbert WC, and Roth SH. Toxicology of hydrogensulfide. Annu Rev Pharmacol Toxicol 32: 109-134, 1992.
54. Rossoni G, Manfredi B, Tazzari V, Sparatore A, Trivulzio S, Del Soldato P, and Berti F. Activity of a new hydrogen sulfide-releasing aspirin (ACS14) on pathological cardiovascular alterations induced by glutathione depletion in rats. Eur J Pharmacol 648: 139-145, 2010.
55. Sasakura K, Hanaoka K, Shibuya N, Mikami Y, Kimura Y, Komatsu T, Ueno T, Terai T, Kimura H, and Nagano T. Development of a highly selective fluorescence probe for hydrogen sulfide. J Am Chem Soc 133: 18003-18005, 2011.
56. Savage JC and Gould DH. Determination of sulfide in brain tissue and rumen fluid by ion-interaction reversed-phase high-performance liquid chromatography. J Chromatogr 526: 540-545, 1990.
57. Shibuya N, Mikami Y, Kimura Y, Nagahara N, and Kimura H. Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem 146: 623-626, 2009.
58. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, and Kimura H. 3-Mercaptopyruvate sulfurtransferease produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11: 703-714, 2009.
59. Suh JH, Shenvi SV, Dixon BM Liu H, Jaiswal AKI, Liu RM, and Hagen TM. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci USA 101: 3381-3386, 2004.
60. Stipanuk MH and Beck PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 206: 267-277, 1982.
61. Tan S, Schubert D, and Maher P. Oxytosis: A novel form of programmed cell death. Cur Top Med Chem 1: 497-506, 2001.
62. Taniguchi T and Kimura T. Role of 3-mercaptopyruvate sulfurtransferase in the formation of the iron-sulfur chromophore of adrenal ferredoxin. Biochim Biophys Acta 364: 284-295, 1974.
63. Tateishi N, Higashi T, Naruse A Nakashima K, and Shiozaki H. Rat liver glutathione: Possible role as a reservoir of cysteine. J Nutr 107: 51-60, 1977.
64. Taub JW, Huang X, Matherly LH, Stout ML, Buck SA, Massey GV, Becton DL, Chang MN, Weinstein HJ, and Ravindranath Y. Expression of chromosome 21-localized genes in acute myeloid leukemia: Differences between Down syndrome and non-Down syndrome blast cells and relationship to in vitro sensitivity to cytosine arabinoside and daunorubicin. Blood 94: 1393-1400, 1999.
65. Teague B, Asiedu S, and Moore PK. The smooth muscle relaxant effect of hydrogen sulphide in vitro: Evidence for a physiological role to control intestinal contractility. Br J Pharmacol 137: 139-145, 2002.
66. Tiranti V, Viscomi C, Hildebrandt T, Di Meo I, Mineri R, Tiveron C, Levitt MD, Prelle A, Fagiolari G, Rimoldi M, and Zeviani M. Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat Med 15: 200-205, 2009.
67. Toohey JI. Sulphane sulphur in biological systems: A possible regulatory role. Biochem J 264: 625-632, 1989.
68. Toohey JI. Sulfur signaling: Is the agent sulfide or sulfane? Anal Biochem 413: 1-7, 2011.
69. Tsugane M, Nagai Y, Kimura Y, Oka J-I, and Kimura H. Differentiated astrocytes acquire sensitivity to hydrogen sulfide that is diminished by the transformation into reactive astrocytes. Antioxid Redox Signal 9: 257-269, 2007.
70. Ubuka T, Umemura S, Yuasa S, Kinuta M, and Watanabe K. Purification and characterization of mitochondrial cysteine aminotransferase from rat liver. Physiol Chem Physics 10: 483-500, 1978.
71. Umemura K and Kimura H. Hydrogen sulfide enhances reducing activity in neurons: Neurotropic role of H2S in the brain? Antioxid Redox Signal 9: 2035-2041, 2007
72. Vitvitsky V, Tomas M, Ghorpade A, Gendelman HE, and Banerjee R. A functional transsulfuration pathway in the brain links to glutathione homeostasis. J Biol Chem 281: 35785-35793, 2006.
73. Warenycia MW, Goodwin LR, Benishin CG, Reiffenstein RJ, Grancom DM, Taylor JD, and Dieken FP. Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem Pharmacol 38: 973-981, 1989.
74. Warenycia MW, Smith KA, Blashko CS, Kombian SB, and Reiffenstein Rj. Monoamine oxidase inhibition as a sequel of hydrogen sulfide intoxication: Increases in brain catecholamine and 5-hydroxytryptamine. Arch Toxicol 63: 131-136, 1989.
75. Westrop GD, Georg I, and Coombs GH. The mercaptopyruvate sulfurtransferase of Trichomonas vaginalis links cysteine catabolism to the production of thioredoxin persulfide. J Biol Chem 284: 33485-33494, 2009.
76. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong, BS, Hheung NS, Halliwell B, and Moore PK. The novel neuromodulator hydrogen sulfide: An endogenous peroxynitrite 'scavenger'? J Neurochem 90: 765-768, 2004.
77. Whiteman M, Cheung NS, Zhu YZ, Chu SH, Siau JL, Wong BS, Armstrong JS, and Moore PK. Hydrogen sulphide: A novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 326: 794-798, 2005.
78. Whiteman M and Winyard PG. Hydrogen sulfide and inflammation: The good, the bad, the ugly and the promising. Expert Rev Clin Pharmacol 4: 13-32, 2011.
79. Wintner EA, Deckwerth TL, Langston W, Bengtsson A, Leviten D, Hill P, Insko MA, Dumpit R, VandenEkart E, Toombs CF, and Szabo C. A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br J Pharmacol 160: 941-957, 2010.
80. Wisniewski KE, Wisniewski HM, and Wen GY. Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome. Ann Neurol 17: 278-282, 1985.
81. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, et al. H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine c-lyase. Science 322: 587-590, 2008.
82. Zhao W, Zhang J, Lu Y, and Wang R. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20: 6008-6016, 2001.