Thiosulfate: A readily accessible source of hydrogen sulfide in oxygen sensing

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 6, 2013, Pages

  Olson, Kenneth R ^a   DeLeon, Eric R ^a,b   Gao, Yan ^a   Hurley, Kevin ^a   Sadauskas, Victor ^a,b   Batz, Catherine ^a   Stoy, Gilbrian F ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROLIPOATE; DITHIOTHREITOL; GLUTATHIONE; HYDROGEN SULFIDE; OXYGEN; THIOSULFATE;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA; ARTICLE; COW; HYPOXIC LUNG VASOCONSTRICTION; LIVER; LUNG; MOUSE; NONHUMAN; OXIDATION; OXYGEN SENSING; PRIORITY JOURNAL; PULMONARY ARTERY; RAT; VASODILATATION; VOLATILIZATION;

GASOTRANSMITTER; MITOCHONDRIA; OXYGEN SENSING;

ANIMALS; CATTLE; CELL HYPOXIA; FEMALE; HYDROGEN SULFIDE; LAMPREYS; OXYGEN; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; THIOSULFATES;

EID: 84884384095     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00421.2012     Document Type: Article

References (47)

1. 2S biogenesis by human cystathionine gamma-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J Biol Chem 284: 11601-11612, 2009.
2. DeLeon ER, Stoy GF, Olson KR. Passive loss of hydrogen sulfide in biological experiments. Anal Biochem 421: 203-207, 2012.
3. Di Meo I, Fagiolari G, Prelle A, Viscomi C, Zeviani M, Tiranti V. Chronic exposure to sulfide causes accelerated degradation of cytochrome c oxidase in ethylmalonic encephalopathy. Antioxid Redox Signal 15: 353-362, 2011.
4. Doeller JE, Isbell TS, Benavides G, Koenitzer J, Patel H, Patel RP, Lancaster JR, Darley-Usmar VM, Kraus DW. Polarographic measurement of hydrogen sulfide production and consumption by mammalian tissues. Anal Biochem 341: 40-51, 2005.
5. Dombkowski RA, Doellman MM, Head SK, Olson KR. Hydrogen sulfide mediates hypoxia-induced relaxation of trout urinary bladder smooth muscle. J Exp Biol 209: 3234-3240, 2006.
6. Dombkowski RA, Naylor MG, Shoemaker E, Smith M, DeLeon ER, Stoy GF, Gao Y, Olson KR. Hydrogen sulfide (HS) and hypoxia inhibit salmonid gastrointestinal motility: evidence for HS as an oxygen sensor. J Exp Biol 214: 4030-4040, 2011.
7. Drousiotou A, DiMeo I, Mineri R, Georgiou T, Stylianidou G, Tiranti V. Ethylmalonic encephalopathy: application of improved biochemical and molecular diagnostic approaches. Clin Genet 79: 385-390, 2011.
8. Farese S, Stauffer E, Kalicki R, Hildebrandt T, Frey BM, Frey FJ, Uehlinger DE, Pasch A. Sodium thiosulfate pharmacokinetics in hemodialysis patients and healthy volunteers. Clin J Am Soc Nephrol 6: 1447-1455, 2011.
9. 2S) metabolism in mitochondria and its regulatory role in energy production. Proc Natl Acad Sci USA 109: 2943-2948, 2012.
10. Giordano C, Viscomi C, Orlandi M, Papoff P, Spalice A, Burlina A, Di MI, Tiranti V, Leuzzi V, d'Amati G, Zeviani M. Morphologic evidence of diffuse vascular damage in human and in the experimental model of ethylmalonic encephalopathy. J Inherit Metab Dis 35: 451-458, 2012.
11. Hildebrandt TM, Grieshaber MK. Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275: 3352-3361, 2008.
12. Jackson MR, Melideo SL, Jorns MS. Human sulfide: quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51: 6804-6815, 2012.
13. Jones W, Li X, Qu ZC, Perriott L, Whitesell RR, May JM. Uptake, recycling, and antioxidant actions of alpha-lipoic acid in endothelial cells. Free Radic Biol Med 33: 83-93, 2002.
14. Julian D, Statile JL, Wohlgemuth SE, Arp AJ. Enzymatic hydrogen sulfide production in marine invertebrate tissues. Comp Biochem Physiol [A] Mol Integr Physiol 133: 105-115, 2002.
15. Kai S, Tanaka T, Daijo H, Harada H, Kishimoto S, Suzuki K, Takabuchi S, Takenaga K, Fukuda K, Hirota K. Hydrogen sulfide inhibits hypoxia-but not anoxia-induced hypoxia-inducible factor 1 activation in a von hippel-lindau-and mitochondria-dependent manner. Antioxid Redox Signal 16: 203-216, 2012.
16. Kimura H. Production and physiological effects of hydrogen sulfide. Antioxid Redox Signal In press.
17. Koj A, Frendo J, Wojtczak L. Subcellular distribution and intramitochondrial localization of three sulfurtransferases in rat liver. FEBS Lett 57: 42-46, 1975.
18. Li Q, Sun B, Wang X, Jin Z, Zhou Y, Dong L, Jiang LH, Rong W. A crucial role for hydrogen sulfide in oxygen sensing via modulating large-conductance calcium-activated potassium channels. Antioxid Redox Signal 12: 1179-1189, 2010.
19. Linden DR, Furne J, Stoltz GJ, bdel-Rehim MS, Levitt MD, Szurszewski JH. Sulfide quinone reductase contributes to hydrogen sulfide metabolism in murine peripheral tissues but not in the central nervous system. Br J Pharmacol 165: 2178-2190, 2011.
20. Madden JA, Ahlf SB, Dantuma MW, Olson KR, Roerig DL. Precursors and inhibitors of hydrogen sulfide synthesis affect acute hypoxic pulmonary vasoconstriction in the intact lung. J Appl Physiol 112: 411-418, 2012.
21. Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439: 479-485, 2011.
22. Mudd SH, Irreverre F, Laster L. Sulfite oxidase deficiency in man: demonstration of the enzymatic defect. Science 156: 1599-1602, 1967.
23. Olson KR. Hydrogen sulfide as an oxygen sensor. Clin Chem Lab Med 1-10, 2012.
24. Olson KR, Dombkowski RA, Russell MJ, Doellman MM, Head SK, Whitfield NL, Madden JA. Hydrogen sulfide as an oxygen sensor/ transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J Exp Biol 209: 4011-4023, 2006.
25. Olson KR, Forgan LG, Dombkowski RA, Forster ME. Oxygen dependency of hydrogen sulfide-mediated vasoconstriction in cyclostome aortas. J Exp Biol 211: 2205-2213, 2008.
26. Olson KR, Healy M, Qin J, Skovgaard N, Vulesevic B, Duff DW, Whitfield NL, Yang G, Wang R, Perry SF. Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors. Am J Physiol Regul Integr Comp Physiol 295: R669-R680, 2008.
27. Olson KR, Whitfield NL. Hydrogen sulfide and oxygen sensing in the cardiovascular system. Antioxid Redox Signal 12: 1219-1234, 2010.
28. Olson KR, Whitfield NL, Bearden SE, St. Leger J, Nilson E, Gao Y, Madden JA. Hypoxic pulmonary vasodilation: A paradigm shift with a hydrogen sulfide mechanism. Am J Physiol Regul Integr Comp Physiol 298: R51-R60, 2010.
29. 2 sensing in the carotid body. Proc Natl Acad Sci USA 107: 10719-10724, 2010.
30. Perry SF, McNeill B, Elia E, Nagpal A, Vulesevic B. Hydrogen sulfide stimulates catecholamine secretion in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 296: R133-R140, 2009.
31. Rajapakshe A, Tollin G, Enemark JH. Kinetic and thermodynamic effects of mutations of human sulfite oxidase. Chem Biodivers 9: 1621-1634, 2012.
32. 2S/HS production and evidence of pancreatic and lung toxicity. Antioxid Redox Signal In press.
33. Searcy DG. Metabolic integration during the evolutionary origin of mitochondria. Cell Res 13: 229-238, 2003.
34. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11: 703-714, 2009.
35. Skovgaard N, Olson KR. Hydrogen sulfide mediates hypoxic vasoconstriction through a production of mitochondrial ROS in trout gills. Am J Physiol Regul Integr Comp Physiol 303: R487-R494, 2012.
36. Stipanuk MH, Ueki I, Dominy JE, Jr, Simmons CR, Hirschberger LL. Cysteine dioxygenase: a robust system for regulation of cellular cysteine levels. Amino Acids 37: 55-63, 2009.
37. Sylvester JT, Shimoda LA, Aaronson PI, Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 92: 367-520, 2012.
38. Telezhkin V, Brazier SP, Cayzac S, Muller CT, Riccardi D, Kemp PJ. Hydrogen sulfide inhibits human BK (Ca) channels. Adv Exp Med Biol 648: 65-72, 2009.
39. Telezhkin V, Brazier SP, Cayzac SH, Wilkinson WJ, Riccardi D, Kemp PJ. Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels. Respir Physiol Neurobiol 172: 169-178, 2010.
40. Theissen U, Hoffmeister M, Grieshaber M, Martin W. Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20: 1564-1574, 2003.
41. Tiranti V, Viscomi C, Hildebrandt T, Di MI, Mineri R, Tiveron C, Levitt MD, Prelle A, Fagiolari G, Rimoldi M, Zeviani M. Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat Med 15: 200-205, 2009.
42. Ueki I, Roman HB, Valli A, Fieselmann K, Lam J, Peters R, Hirschberger LL, Stipanuk MH. Knockout of the murine cysteine dioxygenase gene results in severe impairment in ability to synthesize taurine and an increased catabolism of cysteine to hydrogen sulfide. Am J Physiol Endocrinol Metab 301: E668-E684, 2011.
43. Vairavamurthy A, Mantowitz B, Luther GW, III, Jeon Y. Oxidation state of sulfur in thiosulfate and implications for anaerobic energy metabolism. Geochim Cosmochim Acta 57: 1619-1623, 1993.
44. Villarejo M, Westley J. Mechanism of rhodanese catalysis of thiosulfatelipoate oxidation-reduction. J Biol Chem 238: 4016-4020, 1963.
45. Volini M, Westley J. The mechanism of the rhodanese-catalyzed thiosulfate-lipoate reaction. Kinetic analysis. J Biol Chem 241: 5168-5176, 1966.
46. Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J, Dokic D, Schumacker PT. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res 106: 526-535, 2010.
47. 2S/sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am J Physiol Regul Integr Comp Physiol 294: R1930-R1937, 2008.