Amino Acids

, Volume 39, Issue 2, pp 335–347 | Cite as

Luminal sulfide and large intestine mucosa: friend or foe?

  • François BlachierEmail author
  • Anne-Marie Davila
  • Sabria Mimoun
  • Pierre-Henri Benetti
  • Calina Atanasiu
  • Mireille Andriamihaja
  • Robert Benamouzig
  • Frédéric Bouillaud
  • Daniel Tomé
Review Article


Hydrogen sulfide (H2S) is present in the lumen of the human large intestine at millimolar concentrations. However, the concentration of free (unbound) sulfide is in the micromolar range due to a large capacity of fecal components to bind the sulfide. H2S can be produced by the intestinal microbiota from alimentary and endogenous sulfur-containing compounds including amino acids. At excessive concentration, H2S is known to severely inhibit cytochrome c oxidase, the terminal oxidase of the mitochondrial electron transport chain, and thus mitochondrial oxygen (O2) consumption. However, the concept that sulfide is simply a metabolic troublemaker toward colonic epithelial cells has been challenged by the discovery that micromolar concentration of H2S is able to increase the cell respiration and to energize mitochondria allowing these cells to detoxify and to recover energy from luminal sulfide. The main product of H2S metabolism by the colonic mucosa is thiosulfate. The enzymatic activities involved in sulfide oxidation by the colonic epithelial cells appear to be sulfide quinone oxidoreductase considered as the first and rate-limiting step followed presumably by the action of sulfur dioxygenase and rhodanese. From clinical studies with human volunteers and experimental works with rodents, it appears that H2S can exert mostly pro- but also anti-inflammatory effects on the colonic mucosa. From the available data, it is tempting to propose that imbalance between the luminal concentration of free sulfide and the capacity of colonic epithelial cells to metabolize this compound will result in an impairment of the colonic epithelial cell O2 consumption with consequences on the process of mucosal inflammation. In addition, endogenously produced sulfide is emerging as a prosecretory neuromodulator and as a relaxant agent toward the intestinal contractibility. Lastly, sulfide has been recently described as an agent involved in nociception in the large intestine although, depending on the experimental design, both pro- and anti-nociceptive effects have been reported.


Sulfide Large intestine Colon Detoxification Energy metabolism 


  1. Ahmad T, Satsangi J, McGovern D, Bunce M, Jewell DP (2001) Review article: the genetics of inflammatory bowel disease. Aliment Pharmacol Ther 15:731–748PubMedGoogle Scholar
  2. Allen A, Flemström G (2005) Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am J Physiol 288:C1–C19Google Scholar
  3. Attene-Ramos MS, Wagner ED, Plewa MJ, Gaskins HR (2006) Evidence that hydrogen sulfide is a genotoxic agent. Mol Cancer Res 4:9–14PubMedGoogle Scholar
  4. Attene-Ramos MS, Wagner ED, Gaskins HR, Plewa MJ (2007) Hydrogen sulfide induces direct radical-associated DNA damage. Mol Cancer Res 5:455–459PubMedGoogle Scholar
  5. Awano N, Wada M, Mori H, Nakamori S, Takagi H (2005) Identification and functional analysis of Escherichia coli cysteine desulfhydrases. Appl Environ Microbiol 71:4149–4152PubMedGoogle Scholar
  6. Babidge W, Millard S, Roediger W (1998) Sulfides impair short chain fatty acid beta-oxidation at acyl-CoA dehydrogenase level in colonocytes: implications for ulcerative colitis. Mol Cell Biochem 181:117–124PubMedGoogle Scholar
  7. Baglieri A, Mahe S, Zidi S, Huneau JF, Thuiller F, Marteau P, Tome D (1994) Gastro-jejunal digestion of soya-bean-milk protein in humans. Br J Nutr 72:519–532PubMedGoogle Scholar
  8. Blachier F, Mariotti F, Huneau JF, Tome D (2007) Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33:547–562PubMedGoogle Scholar
  9. Bos C, Juillet B, Fouillet H, Turlan L, Dare S, Luengo C, Ntounda R, Benamouzig R, Gausseres N, Tome D, Gaudichon C (2005) Postprandial metabolic utilization of wheat protein in humans. Am J Clin Nutr 81:87–94PubMedGoogle Scholar
  10. Buttgereit F, Brand MD (1995) A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 312:163–167PubMedGoogle Scholar
  11. Chacko A, Cummings JH (1988) Nitrogen losses from the human small bowel: obligatory losses and the effects of physical form of food. Gut 29:809–815PubMedGoogle Scholar
  12. Christl SU, Gibson GR, Cummings JH (1992) Role of dietary sulphate in the regulation of methanogenesis in the human large intestine. Gut 33:1234–1238PubMedGoogle Scholar
  13. Christl SU, Eisner HD, Dusel G, Kasper H, Scheppach W (1996) Antagonistic effects of sulfide and butyrate on proliferation of colonic mucosa: a potential role for these agents in the pathogenesis of ulcerative colitis. Dig Dis Sci 41:2477–2481PubMedGoogle Scholar
  14. Clauss MT, Zocher GE, Maier THP, Schulz GE (2005) Structure of the O-acetyl-serine sulfurhydralase, 2 isoenzyme CYSM from Escherichia coli. Biochem 44:8620–8626Google Scholar
  15. Deplancke B, Gaskins HR (2003) Hydrogen sulfide induces serum-independent cell cycle entry in nontransformed rat intestinal epithelial cells. FASEB J 17:1310–1312PubMedGoogle Scholar
  16. Deplancke B, Finster K, Graham WV, Collier CT, Thurmond JE, Gaskins HR (2003) Gastrointestinal and microbial responses to sulfate-supplemented drinking water in mice. Exp Biol Med 228:424–433Google Scholar
  17. Distrutti E, Sediari L, Mencarelli A, Renga B, Orlandi S, Antonelli E, Roviezzo F, Morelli A, Cirino G, Wallace JL, Fiorucci S (2006a) Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels. J Pharmacol Exp Ther 316:325–335PubMedGoogle Scholar
  18. Distrutti E, Sediari L, Mencarelli A, Renga B, Orlandi S, Russo G, Caliendo G, Santagada V, Cirino G, Wallace JL, Fiorucci S (2006b) 5-Amino-2-hydroxybenzoic acid 4-(5-thioxo-5H-(1, 2)dithiol-3-yl)-phenyl ester (ATB-429), a hydrogen sulfide-releasing derivative of mesalamine, exerts antinociceptive effects in a model of postinflammatory hypersensitivity. J Pharmacol Exp Ther 319:447–458PubMedGoogle Scholar
  19. Drassar BS, Hill MJ (1974) Human Intestinal Flora. Academic Press, LondonGoogle Scholar
  20. Edmond LM, Hopkins MJ, Magee EA, Cummings JH (2003) The effect of 5-aminosalicylic acid-containing drugs on sulfide production by sulfate-reducing and amino acid-fermenting bacteria. Inflamm Bowel Dis 9:10–17PubMedGoogle Scholar
  21. Evenepoel P, Claus D, Geypens B, Hiele M, Geboes K, Rutgeerts P, Ghoos Y (1999) Amount and fate of egg protein escaping assimilation in the small intestine of humans. Am J Physiol 277:G935–G943PubMedGoogle Scholar
  22. Florin T (1991) Hydrogen sulphide and total acid-volatile sulphide in faeces, determined with a direct spectrophotometric method. Clin Chim Acta 196:127–134PubMedGoogle Scholar
  23. Florin T, Neale G, Gibson GR, Christl SU, Cummings JH (1991) Metabolism of dietary sulphate: absorption and excretion in humans. Gut 32:766–773PubMedGoogle Scholar
  24. Furne JK, Suarez FL, Ewing SL, Springfield J, Levitt MD (2000) Binding of hydrogen sulfide by bismuth does not prevent dextran sulfate-induced colitis in rats. Dig Dis Sci 45:1439–1443PubMedGoogle Scholar
  25. Furne J, Springfield J, Koenig T, DeMaster E, Levitt MD (2001) Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62:255–259PubMedGoogle Scholar
  26. Gallego D, Clavé P, Donovan J, Rahmati R, Grundy D, Jimenez M, Beyak MJ (2008) The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol Motil 20:1306–1316PubMedGoogle Scholar
  27. Gaudichon C, Mahe S, Benamouzig R, Luengo C, Fouillet H, Dare S, Van Oycke M, Ferriere F, Rautureau J, Tome D (1999) Net postprandial utilization of (15N)-labeled milk protein nitrogen is influenced by diet composition in humans. J Nutr 129:890–895PubMedGoogle Scholar
  28. Gaudichon C, Bos C, Morens C, Petzke KJ, Mariotti F, Everwand J, Benamouzig R, Dare S, Tome D, Metges CC (2002) Ileal losses of nitrogen and amino acids in humans and their importance to the assessment of amino acid requirements. Gastroenterology 123:50–59PubMedGoogle Scholar
  29. Gaudio E, Taddei G, Vetuschi A, Sferra R, Frieri G, Ricciardi G, Caprilli R (1999) Dextran sulfate sodium colitis in rats: clinical structural, and ultrastructural aspects. Dig Dis Sci 44:1458–1475PubMedGoogle Scholar
  30. Gausseres N, Mahe S, Benamouzig R, Luengo C, Drouet H, Rautureau J, Tome D (1996) The gastro-ileal digestion of 15-N labelled pea nitrogen in adult humans. Br J Nutr 76:75–85PubMedGoogle Scholar
  31. Gibson JA, Sladem GE, Dawson AM (1976) Protein absorption and ammonia production: the effects of dietary protein and removal of the colon. Br J Nutr 35:61–65PubMedGoogle Scholar
  32. Gibson GR, Cummings JH, Macfarlane GT (1988a) Competition for hydrogen between sulphate-reducing bacteria and methanogenic bacteria from the human large intestine. J Appl Bacteriol 65:241–247PubMedGoogle Scholar
  33. Gibson GR, Cummings JH, Macfarlane GT (1988b) Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Appl Environ Microbiol 54:2750–2755PubMedGoogle Scholar
  34. Goubern M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F (2007) Sulfide, the first inorganic substrate for human cells. FASEB J 21:1699–1706PubMedGoogle Scholar
  35. Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565PubMedGoogle Scholar
  36. Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53PubMedGoogle Scholar
  37. Hedderich R, Klimmek O, Kroëger A, Dirmeier R, Keller M, Stetter KO (1999) Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 22:353–381Google Scholar
  38. Hildebrand TM, Grieshaber MK (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and inverterbrate mitochondria. FEBS J 275:3352–3361Google Scholar
  39. Hill BC, Woon TC, Nicholls P, Peterson J, Greenwood C, Thomson AJ (1984) Interactions of sulphide and other ligands with cytochrome c oxidase. Biochem J 224:591–600PubMedGoogle Scholar
  40. Jorgensen J, Mortensen PB (2001) Hydrogen sulfide and colonic epithelial metabolism: implications for ulcerative colitis. Dig Dis Sci 46:1722–1732PubMedGoogle Scholar
  41. Jowett SL, Seal CJ, Pearce MS, Phillips E, Gregory W, Barton JR, Welfare MR (2004) Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut 53:1479–1484PubMedGoogle Scholar
  42. Kadota H, Ishida Y (1972) Production of volatile sulfur compounds by microorganisms. Ann Rev Microbiol 26:127–138Google Scholar
  43. Kallio RE (1951) Function of pyridoxal phosphate in desulfhydrase systems of Proteus morganii. J Biol Chem 192:371–377PubMedGoogle Scholar
  44. Kanazawa K, Konishi F, Mitsuoka T, Terada A, Itoh K, Narushima S, Kumemura M, Kimura H (1996) Factors influencing the development of sigmoid colon cancer. Bacteriologic and biochemical studies. Cancer 77:1701–1706PubMedGoogle Scholar
  45. Kramer P (1966) The effect of varying sodium loads on the ileal excreta of human ileostomised subjects. J Clin Invest 45:1710–1718PubMedGoogle Scholar
  46. Kumagai H, Sejima S, Choi Y, Tanaka H, Yamada H (1975) Crystallization and properties of cysteine desulfhydrase from Aerobacter aerogenes. FEBS Lett 52:304–307PubMedGoogle Scholar
  47. Leschelle X, Goubern M, Andriamihaja M, Blottière HM, Couplan E, Gonzales-Barroso M, Petit C, Pagniez A, Chaumontet C, Mignotte B, Bouillaud F, Blachier F (2005) Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim Biophys Acta 1725:201–212PubMedGoogle Scholar
  48. Leung FW, Heng MC, Allen S, Seno K, Leung JWC, Heng MK (2000) Involvement of luminal bacteria, heat shock protein 60, macrophages and gammadelta T cells in dextran sulfate sodium-induced colitis in rats. Dig Dis Sci 45:1472–1479PubMedGoogle Scholar
  49. Levine J, Ellis CJ, Furne JK, Spingfield J, Levitt MD (1998) Fecal hydrogen sulfide production in ulcerative colitis. Am J Gastroenterol 93:83–87PubMedGoogle Scholar
  50. Levitt MD, Furne J, Springfield J, Suarez F, DeMaster E (1999) Detoxication of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest 104:1107–1114PubMedGoogle Scholar
  51. Levitt MD, Springfield J, Furne J, Koenig T, Suarez FL (2002) Physiology of sulfide in the rat colon: use of bismuth to assess colonic sulfide production. J Appl Physiol 92:1655–1660PubMedGoogle Scholar
  52. Lewis S, Cochrane S (2007) Alteration of sulfate and hydrogen metabolism in the human colon by changing intestinal transit rate. Am J Gastroenterol 102:624–633PubMedGoogle Scholar
  53. Liau YH, Horowitz MI (1976) The importance of PAPS in determining sulphation in gastrointestinal mucosa. Digestion 14:372–375PubMedGoogle Scholar
  54. Linden DR, Sha L, Mazzone A, Stolz GJ, Bernard CE, Furne JK, Levitt MD, Farrugia G, Szurszewski JH (2008) Production of the gaseous signal molecule hydrogen sulfide in mouse tissues. J Neurochem 106:1577–1585PubMedGoogle Scholar
  55. Loubinoux J, Bronowicki JP, Pereira IA, Mougenel JL, Faou AE (2002) Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. FEMS Microbiol Ecol 40:107–112PubMedGoogle Scholar
  56. Macfarlane S, Macfarlane GT (2003a) Food and the large intestine. In: Fuller R, Perdigon G (eds) Gut flora, nutrition, immunity and health. Blackwell, Oxford, pp 24–51Google Scholar
  57. Macfarlane S, Macfarlane GT (2003b) Regulation of short-chain fatty acid production. Proc Nutr Soc 62:67–72PubMedGoogle Scholar
  58. Macfarlane GT, Gibson GR, Cummings JH (1992) Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72:57–64PubMedGoogle Scholar
  59. Magee EA, Richardson CJ, Hughes R, Cummings JH (2000) Contribution of dietary protein to sulfide production in the large intestine: an in vitro and a controlled feeding study in humans. Am J Clin Nutr 72:1488–1494PubMedGoogle Scholar
  60. Matsunami M, Tarui T, Mitani K, Nagasawa K, Fukushima O, Okubo K, Yoshida S, Takemura M, Kawabata A (2009) Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 58:751–761PubMedGoogle Scholar
  61. Mitsui T, Edmond LM, Magee EA, Cummings JH (2003) The effects of bismuth, iron, zinc and nitrate on free sulfide in batch cultures seeded with fecal flora. Clin Chim Acta 335:131–135PubMedGoogle Scholar
  62. Moore JW, Babidge W, Millard S, Roediger WEW (1997) Effect of sulphide on short chain acyl-CoA metabolism in rat colonocytes. Gut 41:77–81PubMedCrossRefGoogle Scholar
  63. Moore J, Babidge W, Millard S, Roediger W (1998) Colonic luminal hydrogen sulfide is not elevated in ulcerative colitis. Dig Dis Sci 43:162–165PubMedGoogle Scholar
  64. Nicholson RA, Roth SH, Zhang A, Zheng J, Brookes J, Skrajny B, Bennington R (1998) Inhibition of respiratory and bioenergetic mechanisms by hydrogen sulfide in mammalian brain. J Toxicol Environ Health 54:491–507Google Scholar
  65. Petersen LC (1977) The effects of inhibitors on the oxygen kinetics of cytochrome c oxidase. Biochim Biophys Acta 460:299–307PubMedGoogle Scholar
  66. Picton R, Eggo MC, Merrill GA, Langman MJS, Singh S (2002) Mucosal protection against sulphide: importance of the enzyme rhodanese. Gut 50:201–205PubMedGoogle Scholar
  67. Picton R, Eggo MC, Langman MJ, Singh S (2007) Impaired detoxication of hydrogen sulfide in ulcerative colitis? Dig Dis Sci 52:373–378PubMedGoogle Scholar
  68. Pitcher MC, Pitcher JM (1996) Hydrogen sulfide: a bacterial toxin in ulcerative colitis? Gut 39:1–4PubMedGoogle Scholar
  69. Pitcher MC, Beatty ER, Cummings JH (2000) The contribution of sulphate reducing bacteria and 5-aminosalicylic acid to faecal sulphide in patients with ulcerative colitis. Gut 46:64–72PubMedGoogle Scholar
  70. Pochart P, Doré J, Lémann F, Goderel I, Rambaud JC (1992) Interrelations between populations of methanogenic archae and sulfate-reducing bacteria in the human colon. FEMS Microbiol Lett 77:225–228PubMedGoogle Scholar
  71. Rabus R, Hansen TH, Widdel F (2006) Dissimilatory sulfate- and sulfur-reducing prokaryotes. In: Dworkin M (ed) The prokaryotes. A handbook of the biology of bacteria: symbiotic associations, Biotechnology, Applied Microbiology, 3rd edn. Springer, New York, 2:659–768Google Scholar
  72. Ramasamy S, Singh S, Taniere P, Langman MJS, Eggo MC (2006) Sulfide-detoxifying enzymes in the human colon are decreased in cancer and upregulated in differentiation. Am J Physiol 291:G288–G296Google Scholar
  73. Reiffenstein RJ, Hulbert WC, Roth SH (1992) Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 32:109–134PubMedGoogle Scholar
  74. Roediger WEW, Duncan A, Kapanaris O, Millard S (1993a) Reducing sulfur compounds of the colon impair colonocyte nutrition: implications for ulcerative colitis. Gastroenterology 104:802–809PubMedGoogle Scholar
  75. Roediger WEW, Duncan A, Kapanaris O, Millard S (1993b) Sulphide impairment of substrate oxidation in rat colonocytes: a biochemical basis for ulcerative colitis? Clin Sci 85:623–627PubMedGoogle Scholar
  76. Roediger WE, Babidge W, Millard S (1996) Methionine derivatives diminish sulphide damage to colonocytes: implications for ulcerative colitis. Gut 39:77–81PubMedGoogle Scholar
  77. Scanlan PD, Shanahan F, Marchesi JR (2009) Culture-independent analysis of desulfovibrios in the human distal colon of healthy, colorectal cancer and polypectomized individuals. FEMS Microbiol Ecol 69:213–221PubMedGoogle Scholar
  78. Schauder R, Kröger A (1993) Bacterial sulphur respiration. Arch Microbiol 159:491–497Google Scholar
  79. Schicho R, Krueger D, Zeller F, Von Weyhern CW, Frieling T, Kimura H, Ishii I, De Giorgio R, Campi B, Schemann M (2006) Hydrogen sulfide is a novel prosecretory neuromodulator in the guinea-pig and human colon. Gastroenterology 131:1542–1552PubMedGoogle Scholar
  80. Shaw L, Engel PC (1987) CoA-persulphide: a possible in vivo inhibitor of mammalian short-chain acyl-CoA dehydrogenase. Biochim Biophys Acta 919:171–174PubMedGoogle Scholar
  81. Siegel LM, Murphy MJ, Kamin H (1973) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of Enterobacteria. I. The Escherichia coli hemoflavoprotein: molecular parameters and prosthetic groups. J Biol Chem 248:251–264PubMedGoogle Scholar
  82. Silvester KR, Cummings JH (1995) Does digestibility of meat protein help explain large bowel cancer risk? Nutr Cancer 24:279–288PubMedGoogle Scholar
  83. Smiddy FG, Gregory SD, Smith IB, Goligher JC (1960) Fecal loss of fluid, electrolytes and nitrogen in colitis before and after ileostomy. Lancet 1:14–19PubMedGoogle Scholar
  84. Smith EA, Marcfarlane GT (1997) Dissimilatory amino acid metabolism in human colonic bacteria. Anaerobe 3:327–337PubMedGoogle Scholar
  85. Stewart JA, Chadwick VS, Murray A (2006) Carriage, quantification, and predominance of methanogens and sulfate-reducing bacteria in faecal samples. Lett Appl Microbiol 43:58–63PubMedGoogle Scholar
  86. Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577PubMedGoogle Scholar
  87. Strocchi A, Furne J, Ellis C, Levitt MD (1994) Methanogens outcompete sulphate-reducing bacteria for H2 in the human colon. Gut 35:1098–1101PubMedGoogle Scholar
  88. Suarez F, Furne J, Springfield J, Levitt M (1998) Production and elimination of sulfur-containing gases in the rat colon. Am J Physiol 274:G727–G733PubMedGoogle Scholar
  89. Szabo C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6:917–935PubMedGoogle Scholar
  90. Tai CH, Burkhard P, Gani D, Jenn T, Johnson C, Cook PF (2001) Characterization of the allosteric anion-binding site of O-acetylserine sulfhydrylase. Biochem 40:7446–7452Google Scholar
  91. Tamaru T, Kobayashi H, Kishimoto S, Kajiyama G, Shimamoto F, Brown WR (1993) Histochemical study of colonic cancer in experimental colitis in rats. Dig Dis Sci 38:529–537PubMedGoogle Scholar
  92. Taniguchi E, Matsunami M, Kimura T, Yonezawa D, Ishiki T, Sekiguchi F, Nishikawa H, Maeda Y, Ishikura H, Kawabata A (2009) Rhodanese but not cystathionine-gamma-lyase is associated with dextran sulfate sodium-evoked colitis in mice: a sign of impaired colonic sulfide detoxification? Toxicology 264:96–103PubMedGoogle Scholar
  93. Teague B, Asiedu S, Moore PK (2002) The smooth muscle relaxant effect of hydrogen sulphide in vitro: evidence for a physiological role to control intestinal contractibility. Br J Pharmacol 137:139–145PubMedGoogle Scholar
  94. Tiranti V, Viscomi C, Hildebrand T, Di Meo I, Mineri R, Tiveron C, Levitt MD, Prelle A, Fagiolari G, Rimoldi M, Zeviani M (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat Med 15:200–205PubMedGoogle Scholar
  95. Wallace JL, Vong L, McKnight W, Dicay M, Martin GR (2009) Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137:569–578PubMedGoogle Scholar
  96. Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798PubMedGoogle Scholar
  97. Watt J, Marcus R (1973) Experimental ulcerative diseases of the colon in animals. Gut 14:506–510PubMedGoogle Scholar
  98. Wedzicha BL (1984) Chemistry of sulphur dioxide in foods. Elsevier Applied Science Publishers, LondonGoogle Scholar
  99. Weisiger RA, Pinkus LM, Jakoby WB (1980) Thiol S-methyltransferase: suggested role in detoxication of intestinal hydrogen sulfide. Biochem Pharmacol 29:2885–2887PubMedGoogle Scholar
  100. Willis CL, Cummings JH, Neale G, Gibson GR (1996) In vitro effects of mucin fermentation on the growth of human colonic sulphate-reducing bacteria. Anaerobe 2:117–122Google Scholar
  101. Willis CL, Cummings JH, Neale G, Gibson GR (1997) Nutritional aspects of dissimilatory sulfate reduction in the human large intestine. Curr microbiol 35:294–298PubMedGoogle Scholar
  102. Wilson TH (1962) Intestinal absorption. WB Saunders, Philadelphia, pp 134–137Google Scholar
  103. Wilson K, Mudra M, Furne J, Levitt M (2008) Differentiation of the roles of sulfide oxidase and rhodanese in the detoxication of sulfide by the colonic mucosa. Dig Dis Sci 53:277–283PubMedGoogle Scholar
  104. Xu GY, Winston JH, Shenoy M, Zhou S, Chen JD, Pasricha PJ (2009) The endogenous hydrogen sulfide producing enzyme cystathionine-beta synthase contributes to visceral hypersensitivity in a rat model of irritable bowel syndrome. Mol Pain 5:44PubMedGoogle Scholar
  105. Yoshikawa S (1999) X-ray structure and reaction mechanism of bovine heart cytochrome c oxidase. Biochem Soc Trans 27:351–362PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • François Blachier
    • 1
    Email author
  • Anne-Marie Davila
    • 1
  • Sabria Mimoun
    • 1
  • Pierre-Henri Benetti
    • 1
  • Calina Atanasiu
    • 2
  • Mireille Andriamihaja
    • 1
  • Robert Benamouzig
    • 2
  • Frédéric Bouillaud
    • 3
  • Daniel Tomé
    • 1
  1. 1.INRAAgroParisTech, CRNH IdF, UMR 914 Nutrition Physiology and Ingestive BehaviorParisFrance
  2. 2.Department of Gastroenterology, Hôpital AvicenneAssistance Publique-Hôpitaux de ParisBobignyFrance
  3. 3.CNRS-FRE3210Université René DescartesParisFrance

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