Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract

Antioxidants and Redox Signaling

Volumn 12, Issue 9, 2010, Pages 1125-1133

  Wallace, John L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYBUTYRIC ACID; ALCOHOL; ANTIINFLAMMATORY AGENT; ATB 337; ATB 429; CYCLOOXYGENASE 2 INHIBITOR; CYSTEINE; DICLOFENAC; DICLOFENAC DERIVATIVE; GAMMA INTERFERON; GLYCERYL TRINITRATE; HYDROGEN SULFIDE; INDOMETACIN; INTERLEUKIN 1; MESALAZINE; MYELOPEROXIDASE; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN; SODIUM SULFIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; COLITIS; CROHN DISEASE; EDEMA; ENZYME ACTIVITY; GASTRITIS; GASTROINTESTINAL TRACT; HUMAN; LEUKOCYTE ADHERENCE; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STOMACH MUCOSA; STOMACH ULCER; ULCER HEALING; VASCULAR ENDOTHELIUM; VASODILATATION; VISCERAL PAIN;

ANIMALS; ANTI-INFLAMMATORY AGENTS; COLITIS; GASTROINTESTINAL TRACT; HUMANS; HYDROGEN SULFIDE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-1; LEUKOCYTES; MODELS, BIOLOGICAL; MUCOUS MEMBRANE; NITRIC OXIDE; RATS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77950792008     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2009.2900     Document Type: Review

References (61)

1. Andruski B, McCafferty DM, Ignacy T, Millen B, and McDougall JJ. Leukocyte trafficking and pain behavioural responses to a hydrogen sulfide donor in acute monoarthritis. Am J Physiol 295: R814-R820, 2008.
2. Appleyard CB, McCafferty DM, Tigley AW, Swain MG, and Wallace JL. Tumor necrosis factor mediation of NSAIDinduced gastric damage: role of leukocyte adherence. Am J Physiol 270: G42-G48, 1996. (Pubitemid 26056809)
3. Bai AP, Ouyang Q, and Hu W. Diallyl trisuldife inhibits tumour necrosis factor-a expression in inflamed mucosa of ulcerative colitis. Dig Dis Sci 50: 1426-1431, 2005. (Pubitemid 41039189)
4. Barnett K, Bell CJ, McKnight W, Dicay M, Sharkey KA, and Wallace JL. Role of cyclooxygenase-2 in modulating gastric acid secretion in the normal and inflamed rat stomach. Am J Physiol 279: G1292-G1297, 2000.
5. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, Darley-Usmar VM, Doeller JE, and Kraus DW. Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A 104: 17977-17982, 2007.
6. Bernstein CN, Niazi N, Robert M, Mertz H, Kodner A, Munakata J, Naliboff B, and Mayer EA. Rectal afferent function in patients with inflammatory and functional intestinal disorders. Pain 66: 151-161, 1996. (Pubitemid 26283983)
7. Bhatia M, Sidhapuriwala J, Moochhala SM, and Moore PK. Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat. Br J Pharmacol 145: 141-144, 2005. (Pubitemid 40756518)
8. Boughton-Smith NK, Wallace JL, and Whittle BJR. Relationship between arachidonic acid metabolism, myeloperoxidase activity and leukocyte infiltration in a rat model of inflammatory bowel disease. Agents Actions 25: 115-123, 1988.
9. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, and Zhu YC. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 76: 29-40, 2007. (Pubitemid 47362041)
10. Cunha TM, Dal-Secco D, Verri WA, Guerrero AT, Souza GR, Vieira SM, Lotufo CM, Neto AF, Ferreira SH, and Cunha FQ. Dual role of hydrogen sulfide in mechanical inflammatory hypernociception. Eur J Pharmacol 20: 127-135, 2008.
11. Distrutti E, Sediari L, Mencarelli A, Renga B, Orlandi S, Russo G, Caliendo G, Santagada V, Cirino G, Wallace JL, and Fiorucci S. 5-Amino-2-hydroxybenzoic acid 4-(5-thioxo- 5H-[1,2]dithiol-3yl)-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: 447-458, 2006. (Pubitemid 44455152)
12. Distrutti E. Sediari L, Mencarelli A, Renga B, Orlandi S, Antonelli E, Roviezzo F, Morelli A, Cirino G, Wallace JL, and Fiorucci S. Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels. J Pharmacol Exp Ther 316: 325-335, 2006. (Pubitemid 41832612)
13. Elliott SN, McKnight W, Cirino G, and Wallace JL. A nitric oxide-releasing nonsteroidal anti-inflammatory drug accelerates gastric ulcer healing in rats. Gastroenterology 109: 524-530, 1995.
14. Fiorucci S, Antonelli E, Distrutti E, Rizzo G, Mencarelli A, Orlandi S, Zanardo R, Renga B, Di Sante M, Morelli A, Cirino G, and Wallace JL. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by antiinflammatory nonsteroidal drugs. Gastroenterology 129: 1210-1224, 2005. (Pubitemid 41446861)
15. Fiorucci S, Distrutti E, Cirino G, and Wallace JL. The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology 131: 259-271, 2006. (Pubitemid 44043128)
16. Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, Santucci L, Cirino G, and Wallace JL. Enhanced activity of a hydrogen sulfide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br J Pharmacol 150: 996-1002, 2007. (Pubitemid 46625099)
17. Furne J, Springfield J, Koenig T, DeMaster E, and Levitt MD. Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62: 255-259, 2001. (Pubitemid 32522947)
18. Gallego D, Clavé P, Donovan J, Rahmati R, Grundy D, Jime ́nez M, and Beyak MJ. The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol Motil 20: 1306-1316, 2008.
19. Goubern M, Andriamihaja M, Nübel T, Blachier F, and Bouillaud F. Sulfide, the first inorganic substrate for human cells. FASEB J 21: 1699-1706, 2007. (Pubitemid 46855615)
20. Hu LF, Wong PT, Moore PK, and Bian JS. Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem 100: 1121-1128, 2007. (Pubitemid 46213934)
21. Kamath AF, Chauhan AK, Kisucka J, Dole VS, Loscalzo J, Handy DE, and Wagner DD. (2006) Elevated levels of homocysteine compromise blood-brain barrier integrity in mice. Blood 107: 591-593, 2006. (Pubitemid 43090794)
22. Kashiba M, Kajimura M, Goda N, and Suematsu M. From O2 to H2S: a landscape view of gas biology. Keio J Med 51: 1-10, 2002.
23. Kimura H. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 267: 129-133, 2000. (Pubitemid 30072519)
24. Konturek SJ, Brzozowski T, Majka J, Pytko-Polonczyk J, and Stachura J. Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. Eur J Pharmacol 239: 215-217, 1993. (Pubitemid 23240162)
25. Li L, Rossoni G, Sparatore A, Lee LC, Del Soldato P, and Moore PK. Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Radic Biol Med 42: 706-719, 2007. (Pubitemid 46205152)
26. Linden DR, Sha L, Mazzone A, Stoltz GJ, Bernard CE, Furne JK, Levitt MD, Farrugia G, and Szurszewski JH. Production of the gaseous signal molecule hydrogen sulfide in mouse tissues. J Neurochem 106: 1577-1585, 2008.
27. Ma L and Wallace JL. Endothelial nitric oxide synthase modulates gastric ulcer healing in rats. Am J Physiol Gastrointest Liver Physiol 279: G341-G346, 2000.
28. Ma L, del Soldato P, and Wallace JL. Divergent effects of new cyclooxygenase inhibitors on gastric ulcer healing: shifting the angiogenic balance. Proc Natl Acad Sci U S A 99: 13243-113237, 2002.
29. Mariggiò MA, Minunno V, Riccardi S, Santacroce R, De Rinaldis P, and Fumarulo R. Sulfide enhancement of PMN apoptosis. Immunopharmacol Immunotoxicol 20: 399-408, 1998. (Pubitemid 28432237)
30. Martin GR, McKnight GW, Dicay MS, Coffin CS, Ferraz JG, and Wallace JL. Hydrogen sulphide synthesis in the rat and mouse gastrointestinal tract. Dig Liver Dis 42: 103-109, 2009.
31. Matsunami M, Tarui T, Mitani K, Nagasawa K, Fukushima O, Okubo K, Yoshida S, Takemura M, and Kawabata A. Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 58: 751-761, 2009.
32. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96: 795-803, 1989.
33. Oh G-S, Pae HO, Lee BS Kim BN, Kim JM, Kim HR, Jeon SB, Jeon WK, Chae HJ, and Chung HT. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med 41: 106-119, 2006.
34. Patacchini R, Santicioli P, Giuliani S, and Maggi CA. Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder. Br J Pharmacol 142: 31-41, 2004. (Pubitemid 38698190)
35. Rinaldi L, Gobbi G, Pambianco M, Micheloni C, Mirandola P, and Vitale M. Hydrogen sulfide prevents apoptosis of human PMN via inhibition of p38 and caspase 3. Lab Invest 86: 391-397, 2006.
36. Santucci L, Fiorucci S, Di Matteo FM, and Morelli A. Role of tumor necrosis factor alpha release and leukocyte margination in indomethacin-induced gastric injury in rats. Gastroenterology 108: 393-401, 1995.
37. Schemann M and Grundy D. Role of hydrogen sulfide in visceral nociception. Gut 58: 744-747, 2009.
38. Schicho R, Krueger D, Zeller F,Von Weyhern CWH, Frieling T, Kimura H, Ishii I, Di Giorgio R, Campi B, and Schemann M. Hydrogen sulfide is a novel prosecretory neuromodulator in the guinea-pig and human colon. Gastroenterology 131: 1542-1552, 2006. (Pubitemid 44708939)
39. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O'Neill LA, Perretti M, Rossi AG, and Wallace JL. Resolution of inflammation: state of the art, definitions and terms. FASEB J 21: 325-332, 2007. (Pubitemid 46213480)
40. Sidhapuriwala J, Li L, Sparatore A, Bhatia M, and Moore PK. Effect of S-diclofenac, a novel hydrogen sulfide releasing derivative, on carrageenan-induced hindpaw oedema formation in the rat. Eur J Pharmacol 569: 149-154, 2007. (Pubitemid 47175881)
41. Szabo H, Sato F, Takami K, Szabo S. New ulcerative colitis model induced by sulfhydryl blockers in rats and the effects of antiinflammatory drugs on the colitis. Jpn J Pharmacol 73: 299-309, 1997. (Pubitemid 27226161)
42. Tang G, Wu L, Liang W, and Wang R. Direct stimulation of KATP channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells. Mol Pharmacol 68: 1757-1764, 2005. (Pubitemid 41654358)
43. 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.
44. Wallace JL and Del Soldato P. The therapeutic potential of NO-NSAIDs. Fund Clin Pharmacol 17: 11-20, 2003. (Pubitemid 36241449)
45. Wallace JL, Arfors K-E, and McKnight GW. A monoclonal antibody against the CD18 leukocyte adhesion molecule prevents indomethacin-induced gastric damage in the rabbit. Gastroenterology 100: 878-883, 1991.
46. Wallace JL, Caliendo G, Santagada V, Cirino G, and Fiorucci S. Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat. Gastroenterology 132: 261-271, 2007. (Pubitemid 46108763)
47. Wallace JL, Dicay M, McKnight W, and Martin GR. Hydrogen sulfide modulates gastric ulcer healing in rats. FASEB J 21: 4070-4076, 2007. (Pubitemid 350232363)
48. Wallace JL, Keenan CM, and Granger DN. Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process. Am J Physiol 259: G462-G467, 1990. (Pubitemid 20317856)
49. Wallace JL, McKnight GW, Miyasaka M, Tamatani T, Pauson J, Anderson DC, Granger DN, and Kubes P. Role of endothelial adhesion molecules in NSAID-induced gastric mucosal injury. Am J Physiol 265: G993-G998, 1993. (Pubitemid 2015793)
50. Wallace JL, Viappiani S, and Bolla M. Cyclooxygenaseinhibiting nitric oxide donators for osteoarthritis. Trends Pharmacol Sci 30: 112-117, 2009.
51. Wallace JL, Vong L, McKnight W, Dicay M, and Martin G. Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137: 569-578, 2009.
52. Wallace JL. Gastric ulceration: critical events at the neutrophil endothelium interface. Can J Physiol Pharmacol 71: 98-102, 1993.
53. Wallace JL. Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci 28: 501-505, 2007.
54. Wallace JL. Mechanisms of nonsteroidal anti-inflammatory drug (NSAID) induced gastrointestinal damage: potential for development of gastrointestinal tract safe NSAIDs. Can J Physiol Pharmacol 72: 1493-1498, 1994.
55. Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev 88: 1547-1565, 2008.
56. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798, 2002 (Pubitemid 35340360)
57. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, Halliwell B, and Moore PK. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90: 765-768, 2004. (Pubitemid 38989409)
58. 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. (Pubitemid 39655989)
59. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, and Wang R. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322: 587-590, 2008.
60. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, and Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120, 2006. (Pubitemid 44953872)
61. 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.