Anti-inflammatory and cytoprotective actions of hydrogen sulfide: Translation to therapeutics

Antioxidants and Redox Signaling

Volumn 22, Issue 5, 2015, Pages 398-410

  Wallace, John L ^a   Blackler, Rory W ^b   Chan, Melissa V ^b   Da Silva, Gabriela J ^c   Elsheikh, Wagdi ^b   Flannigan, Kyle L ^b   Gamaniek, Iulia ^b   Manko, Anna ^b   Wang, Lu ^b   Motta, Jean Paul ^a   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

DICLOFENAC; HYDROGEN SULFIDE; MESALAZINE; MYELOPEROXIDASE; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; SODIUM DITHIONITE; SODIUM SULFATE; ANTIINFLAMMATORY AGENT; PROTECTIVE AGENT;

ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; CELL PROTECTION; DRUG EFFICACY; DRUG SAFETY; EXPERIMENTAL COLITIS; GASTROINTESTINAL MUCOSA; HOST RESISTANCE; HUMAN; INFECTION RESISTANCE; INFLAMMATION; INJURY; MUCOSAL IMMUNITY; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; STOMACH PROTECTION; TISSUE INJURY; ULCER HEALING; ANIMAL; CHEMISTRY; METABOLISM; MUCOSA; WOUNDS AND INJURIES;

ANIMALIA;

ANIMALS; ANTI-INFLAMMATORY AGENTS; HUMANS; HYDROGEN SULFIDE; INFLAMMATION; MUCOUS MEMBRANE; PROTECTIVE AGENTS; WOUNDS AND INJURIES;

EID: 84921932417     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5901     Document Type: Review

References (116)

1. Aboubakr E, Taye A, El-Moselhy MA, and Hassan MK. Protective effect of hydrogen sulfide against cold restraint stress-induced gastric mucosal injury in rats. Arch Pharmacol Res 36: 1507-1515, 2013.
2. Arber N, Eagle CJ, Spicak J, Rácz I, Dite P, Hajer J, Zavoral M, Lechuga MJ, Gerletti P, Tang J, Rosenstein RB, Macdonald K, Bhadra P, Fowler R, Wittes J, Zauber AG, Solomon SD, and Levin B. Celecoxib for the prevention of colorectal adenomatous polyps. N Engl J Med 355: 885-895, 2006.
3. Asimakopoulou A, Panopoulos P, Chasapis CT, Coletta C, Zhou Z, Cirino G, Giannis A, Szabo C, Spyroulias GA, and Papapetropoulos A. Selectivity of commonly used pharmacological inhibitors for cystathionine b synthase (CBS) and cystathionine c lyase (CSE). Br J Pharmacol 169: 922-932, 2013.
4. Aslami H, Pulskens WP, Kuipers MT, Bos AP, van Kuilenburg AB, Wanders RJ, Roelofsen J, Roelofs JJ, Kerindongo RP, Beurskens CJ, Schultz MJ, Kulik W, Weber NC, and Juffermans NP. Hydrogen sulfide donor NaHS reduces organ injury in a rat model of pneumococcal pneumosepsis, associated with improved bio-energetic status. PLoS One 8:-63497, 2013.
5. Bai AP, Ouyang Q, and Hu RW. Diallyl trisulfide inhibits tumor necrosis factor-alpha expression in inflamed mucosa of ulcerative colitis. Dig Dis Sci 50: 1426-1431, 2005.
6. 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 Gastrointest Liver Physiol 279: G1292-G1297, 2000.
7. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, Kim K, Tang J, Rosenstein RB, Wittes J, Corle D, Hess TM, Woloj GM, Boisserie F, Anderson WF, Viner JL, Bagheri D, Burn J, Chung DC, Dewar T, Foley TR, Hoffman N, Macrae F, Pruitt RE, Saltzman JR, Salzberg B, Sylwestrowicz T, Gordon GB, and Hawk ET. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 355: 873-884, 2006.
8. Bertrand V, Guimbaud R, Tulliez M, Mauprivez C, Sogni P, Couturier D, Giroud JP, Chaussade S, and Chauvelot-Moachon L. Increase in tumor necrosis factor-alpha production linked to the toxicity of indomethacin for the rat small intestine. Br J Pharmacol 124: 1385-1394, 1998.
9. Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, and Ahmad MS. Hydrogen sulfide ameliorates leadinduced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res Int 21: 717-731, 2014.
10. 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.
11. Blackler R, Manko A, and Wallace JL. Exacerbation of NSAID-induced enteropathy by antisecretory drugs: role of enhanced cytotoxicity of bile. Can J Gastroenterol Hepatol 28 (Suppl A): 80, 2014.
12. Blackler R, Syer SD, Bolla M, Ongini E, and Wallace JL. Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS One 7:-35196, 2012.
13. 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.
14. Brancaleone V, Sampaio AL, Cirino C, Flower RJ, and Perretti M. A novel cross-talk in resolution: H2S activates the annexin A1 pathway. Inflammation Res 60: S291-S293, 2011.
15. Bucci M, Papapetropoulos A, Vellecco V, Zhou Z, Pyriochou A, Roussos C, Roviezzo F, Brancaleone V, and Cirino G. Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 30: 1998-2004, 2010.
16. 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.
17. 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.
18. Campolo M, Esposito E, Ahmad A, Di Paola R, Wallace JL, and Cuzzocrea S. A hydrogen sulfide-releasing cyclooxygenase inhibitor markedly accelerates recovery from experimental spinal cord injury. FASEB J 27: 4489-4499, 2013.
19. Chan MV and Wallace JL. Hydrogen sulfide-based therapeutics and gastrointestinal diseases: translating physiology to treatments. Am J Physiol Gastrointest Liver Physiol 305: G467-G473, 2013.
20. Chattopadhyay M, Kodela R, Nath N, Street CR, Vela źquez-Martńez CA, Boring D, and Kashfi K. Hydrogen sulfide-releasing aspirin modulates xenobiotic metabolizing enzymes in vitro and in vivo. Biochem Pharmacol 83: 733-740, 2012.
21. Chattopadhyay M, Kodela R, Olson KR, and Kashfi K. NOSH-aspirin (NBS-1120), a novel nitric oxide-and hydrogen sulfide-releasing hybrid is a potent inhibitor of colon cancer cell growth in vitro and in a xenograft mouse model. Biochem Biophys Res Commun 419: 523-528, 2012.
22. Cornell NW. Selective inhibition of alanine amino transferase and aspartate aminotransferase in rat hepatocytes. Biochem J 220: 707-716, 1984.
23. Cukier-Meisner E. GIcare: colonoscopy comfort. Bio-Century A13, 2013.
24. Cunha TM, Dal-Secco D, Verri WA Jr, 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 590: 127-135, 2008.
25. D'Araio E, Shaw N, Millward A, Demaine A, Whiteman M, and Hodgkinson A. Hydrogen sulfide induces heme oxygenase-1 in human kidney cells. Acta Diabetol 51: 155-157, 2013.
26. Davenport HW. Why the stomach does not digest itself. Sci Am 226: 87-93, 1972.
27. Din FV, Theodoratou E, Farrington SM, Tenesa A, Barnetson RA, Cetnarskyj R, Stark L, Porteous ME, Campbell H, and Dunlop MG. Effect of aspirin and NSAIDs on risk and survival from colorectal cancer. Gut 59: 1670-1679, 2010.
28. Distrutti E, Sediari L, Mencarelli A, et al. Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels. J Pharmacol Exp Ther 316: 325-335, 2006.
29. 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.
30. Dooley FD, Nair SP, and Ward PD. Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8:-62048, 2013.
31. Dufton N and Wallace JL. Phenotypic differences in hydrogen sulfide synthesis and signaling in primary macrophages. Inflamm Res 60: 121, 2011.
32. Ekundi-Valentim E, Mesquita FP, Santos KT, de Paula MA, Florenzano J, Zanoni CI, Rodrigues L, de Nucci G, Teixeira SA, Ferreira HH, Wallace JL, Costa SK, and Muscará MN. A comparative study on the anti-inflammatory effects of single oral doses of naproxen and its hydrogen sulfide H2S-releasing derivative ATB-346 in rats with carrageenan-induced synovitis. Med Gas Res 3: 24, 2013.
33. Ekundi-Valentim E, Santos KT, Camargo EA, Denadai-Souza A, Teixeira SA, Zanoni CI, Grant AD, Wallace J, Muscará MN, and Costa SK. Differing effects of exogenous and endogenous hydrogen sulphide in carrageenaninduced knee joint synovitis in the rat. Br J Pharmacol 159: 1463-1474, 2010.
34. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow C-W, and Lefer DJ. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Nat Acad Sci U S A 104: 15560-15565, 2007.
35. Elsheikh W, Blackler RW, Flannigan KL and Wallace JL. Enhanced chemopreventative effects of a hydrogen sulfidereleasing NSAID (ATB-346) in experimental colorectal cancer. Nitric Oxide [in press].
36. Fan H, Guo Y, Liang X, Yuan Y, Qi X, Wang M, Ma J, and Zhou H. Hydrogen sulfide protects against amyloid beta-peptide induced neuronal injury via attenuating inflammatory responses in a rat model. J Biomed Res 27: 296-304, 2013.
37. Fiorucci S, Antonelli E, Distrutti E, Mencarelli A, Orlandi S, Zanardo R, Renga B, Rizzo G, Morelli A, Cirino G, and Wallace JL. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129: 1210-1224, 2005.
38. 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.
39. Fiorucci S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, Santucci L, Cirino G, and Wallace JL. Enhanced activity of a hydrogen-sulfide releasing mesalamine derivative (ATB-429) in a mouse model of colitis. Br J Pharmacol 150: 996-1002, 2007.
40. Flannigan KL, Ferraz JG, Wang R, and Wallace JL. Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: a site-specific pro-resolution mechanism. PLoS One 8:-71962, 2013.
41. Flannigan KL, McCoy KD, and Wallace JL. Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am J Physiol Gastrointest Liver Physiol 301: G188-G193, 2011.
42. Fu M, Zhang W, Wu L, Yang G, Li H, and Wang R. Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production. Proc Natl Acad Sci U S A 109: 2943-2948, 2012.
43. 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-R1485, 2008.
44. Goulbern M, Andriamihaja M, Nübel T, Blachier F, and Bouillaud F. Sulfide, the first inorganic substrate for human cells. FASEB J 21: 1699-1706, 2007.
45. Guan Q, Wang X, Gao L, Chen J, Liu Y, Yu C, Zhang N, Zhang X, and Zhao J. Hydrogen sulfide suppresses high glucose-induced expression of intercellular adhesion molecule-1 in endothelial cells. J Cardiovasc Pharmacol 62: 278-284, 2013.
46. Guo C, Liang F, Shah Masood W, and Yan X. Hydrogen sulfide protected gastric epithelial cell from ischemia/reperfusion injury by Keap1 s-sulfhydration, MAPK dependent anti-apoptosis and NF-jB dependent antiinflammation pathway. Eur J Pharmacol 725: 70-78, 2014.
47. Hirata I, Naito Y, Takagi T, Mizushima K, Suzuki T, Omatsu T, Handa O, Ichikawa H, Ueda H, and Yoshikawa T. Endogenous hydrogen sulfide is an anti-inflammatory molecule in dextran sodium sulfate induced colitis in mice. Dig Dis Sci 56: 1379-1386, 2011.
48. Huang J, Khan S, and O'Brien PJ. The glutathione dependence of inorganic sulfate formation from l-or dcysteine in isolated rat hepatocytes. Chem Biol Interact 110: 189-202, 1998.
49. Ise F, Takasura S, Hayashi K, Takahashi K, Koyama M, Aihara E, and Takeuchi K. Stimulation of duodental HCO3-secretion by hydrogen sulphide in rats: relation to prostaglandins, nitric oxide and sensory neurones. Acta Physiol 201: 117-126, 2011.
50. Kai S, Tanaka T, Daijo H, Harada H, Kishimoto S, Suzuki K, Takabuchi S, Takenaga K, Fukuda K, and 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.
51. Kamath AF, Chauhan AK, Kisucka J, Dole VS, Loscalzo J, Handy DE, and Wagner DD. Elevated levels of homocysteine compromise blood-brain barrier integrity in mice. Blood 107: 591-593, 2006.
52. Kamiya T, Wang L, Forsythe P, Goettsche G, Mao Y, Wang Y, Tougas G, and Bienenstock J. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55: 191-196, 2006.
53. Kashfi K. Anti-cancer activity of new designer hydrogen sulfide-donating hybrids. Antioxid Redox Signal 20: 831-846, 2014.
54. Kimura H, Shibuya N, and Kimura Y. Hydrogen sulfide is a signaling molecule and a cytoprotectant. Antioxid Redox Signal 17: 45-57, 2012.
55. Kimura H, Nagai Y, Umemura K, and Kimura Y. Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antiox Redox Signal 7: 795-803, 2005.
56. Kimura Y, Goto Y, and Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochrondria. Antioxid Redox Signal 12: 1-13, 2010.
57. Kondo K, Bhushan S, King AL, Prabhu SD, Hamid T, Koenig S, Murohara T, Predmore BL, Gojon G Sr, Gojon G Jr, Wang R, Karusula N, Nicholson CK, Calvert JW, and Lefer DJ. H2S protects against pressure overloadinduced heart failure via upregulation of endothelial nitric oxide synthase. Circulation 127: 1116-1127, 2013.
58. Konno R and Yasumura Y. Physiological role of d-aminoacid oxidase. Arch Toxicol 36: 54-62, 1991.
59. Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, and Bouillaud F. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta 1797: 1500-1511, 2010.
60. Lee HJ, Lee HG, Choi KS, Surh YJ, and Na HK. Diallyl trisulfide suppresses dextran sodium sulfate-induced mouse colitis: NF-kB and STAT3 as potential targets. Biochem Biophys Res Commun 437: 267-273, 2013.
61. Lee Z, Zhou J, Chen CS, Zhao Y, Tan CH, Li L, Moore PK, and Deng LW. The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS One 6:-21077, 2011.
62. Li L, Rose P, and Moore PK. Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51: 169-187, 2011.
63. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan C-H, and Moore PK. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117: 2351-2360, 2008.
64. Linden DR, Furne J, Stoltz GJ, Abdel-Rehim MS, Levitt MD, and Szurszewski JH. Sulphide quinone reductase contributes to hydrogen sulphide metabolism in murine peripheral tissues but not in the CNS. Br J Pharmacol 165: 2178-2190, 2012.
65. Liu H, Bai XB, Shi S, and Cao YX. Hydrogen sulfide protects from intestinal ischaemia-reperfusion injury in rats. J Pharm Pharmacol 61: 207-212, 2009.
66. 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: 13243-13247, 2002.
67. Mahmud T, Rafi SS, Scott DL, Wrigglesworth JM, and Bjarnason I. Nonsteroidal anti-inflammatory drugs and uncoupling of mitochondrial phosphorylation. Arthritis Rheum 39: 1998-2003, 1996.
68. Mard SA, Neisi N, Solgi G, Hassanpour M, Darbor M, and Maleki M. Gastroprotective effect of NaHS against mucosal lesions induced by ischemia-reperfusion injury in rat. Dig Dis Sci 57: 1496-1503, 2012.
69. Mariggio MA, Minunno V, Riccardi S, Santacroce R, De Rinaldis P, and Fumarulo R. Sulfide enhancement of PMN apoptosis. Immunopharmacol Immunotoxicol 20: 399-408, 1998.
70. Martin GR, McKnight GW, Dicay M, Coffin CS, Ferraz JG, and Wallace JL. Hydrogen sulfide synthesis in the rat and mouse gastrointestinal tract. Dig Liver Dis 42: 103-109, 2010.
71. Matsunami M, Kirishi S, Okui T, and Kawabata A. Hydrogen sulfide-induced colonic mucosal cytoprotection involves T-type calcium channel-dependent neuronal excitation in rats. J Physiol Pharmacol 63: 61-68, 2012.
72. 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: 751-671, 2009.
73. McCafferty DM, Granger DN, and Wallace JL. Indomethacin-induced gastric injury and leukocyte adherence in arthritis versus healthy rats. Gastroenterology 109: 1173-1180, 1995.
74. Mimoun S, Andriamihaja M, Chaumontet C, Atanasiu C, Benamouzig R, Blouin JM, Tomé D, Bouillaud F, and Blachier F. Detoxification of H2S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal 17: 1-10, 2012.
75. Mizuno H, Sakamoto C, Matsuda K, Wada K, Uchida T, Noguchi H, Akamatsu T, and Kasuga M. Induction of cyclooxygenase 2 in gastric mucosal lesions and its inhibition by the specific antagonist delays healing in mice. Gastroenterology 112: 387-397, 1997.
76. Motta JP, Blackler R, Workentine M, da Silva G, Buret A, and Wallace JL. Hydrogen sulfide alters gut bacterial growth and diversity, and stimulates host mucosal immunity. Can J Gastroenterol Hepatol 28 (suppl SA): 88A, 2014.
77. Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, and Gallo RL. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457, 2001.
78. Palinkas Z, Furtmuller PG, Nagy A, Jakopitsch C, Pirker KF, Magierowski M, Jasnos K, Wallace JL, Obinger C, and Nagy P. Interactions of hydrogen sulfide with human myeloperoxidase. Br J Pharmacol [in press].
79. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, Jeschke MG, Branski LK, Herndon DN, Wang R, and Szabó C. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci U S A 106: 21972-21977, 2009.
80. Peake BF, Nicholson CK, Lambert JP, Hood RL, Amin H, Amin S, and Calvert JW. Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner. Am J Physiol Heart Circ Physiol 304: H1215-H1224, 2013.
81. Perretti M and D'Acquisto F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 9: 62-70, 2009.
82. Reuter BK and Wallace JL. Phosphodiesterase inhibitors prevent NSAID enteropathy independently of TNF-alpha release. Am J Physiol Gastrointest Liver Physiol 277: G847-G854, 1999.
83. Santucci L, Fiorucci S, Di Matteo FM, and Morelli A. Role of tumour necrosis factor alpha release and leukocyte margination in indomethacin-induced gastric injury in rats. Gastroenterology 108: 393-401, 1995.
84. Satoh H, Sato F, Takami K, and 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.
85. Serhan CN, Brain SD, Buckley C, 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.
86. Shen X, Carlström M, Borniquel S, Jädert C, Kevil CG, and Lundberg JO. Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic Biol Med 60: 195-200, 2013.
87. Shi H, Ye T, and Chan Z. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in Bermuda grass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71: 226-234, 2013.
88. Tan G, Pan S, Li J, Dong X, Kang K, Zhao M, Jiang X, Kanwar JR, Qiao H, Jiang H, and Sun X. Hydrogen sulfide attenuates carbon tetrachloride-induced hepatotoxicity, liver cirrhosis and portal hypertension in rats. PLoS One 6:-25943, 2011.
89. Tripatara P, Sa Patel N, Collino M, Gallicchio M, Kieswich J, Castiglia S, Benetti E, Stewart KN, Brown PA, Yaqoob MM, Fantozzi R, and Thiemermann C. Generation of endogenous hydrogen sulfide by cystathionine gamma-lyase limits renal ischemia/reperfusion injury and dysfunction. Lab Invest 88: 1038-1048, 2008.
90. Ulrich CM, Bigler J, and Potter JD. Non-steroidal antiinflammatory drugs for cancer prevention: promise, perils and pharmacogenetics. Nat Rev Cancer 6: 130-140, 2006.
91. Vong L, D'Acquisto F, Pederzoli-Ribeil M, Lavagno L, Flower RJ, Witko-Sarsat V, and Perretti M. Annexin-2 cleavage in activated neutrophils: a pivotal role for proteinase 3. J Biol Chem 282: 29998-30004, 2007.
92. 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.
93. Wallace JL, Caliendo G, Santagada V, and Cirino G. Markedly reduced toxicity of a hydrogen sulfide-releasing derivative of naproxen (ATB-346). Br J Pharmacol 159: 1236-1246, 2010.
94. Wallace JL and Devchand PR. Emerging roles for cyclooxygenase-2 in gastrointestinal mucosal defense. Br J Pharmacol 145: 275-282, 2005.
95. Wallace JL, Dicay M, McKnight W, and Martin GR. Hydrogen sulfide enhances ulcer healing. FASEB J 21: 4070-4076, 2007.
96. Wallace JL, Ferraz JG, and Muscara MN. Hydrogen sulfide: an endogenous mediator of resolution of inflammation and injury. Antioxid Redox Signal 17: 58-67, 2012.
97. Wallace JL, Flannigan KL, McKnight W, Wang L, Ferraz JG, and Tuitt D. Pro-resolution, protective and anti-nociceptive effects of a cannabis extract in the rat gastrointestinal tract. J Physiol Pharmacol 64: 167-175, 2013.
98. Wallace JL, Keenan CM, and Granger DN. Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process. Am J Physiol 1259: G462-G467, 1990.
99. Wallace JL and McKnight GW. The mucoid cap over superficial gastric damage in the rat. A high-pH microenvironment dissipated by nonsteroidal anti-inflammatory drugs and endothelin. Gastroenterology 99: 295-304, 1990.
100. Wallace JL, Syer S, Denou E, De Palma G, Vong L, McKnight W, Jury J, Bolla M, Bercik P, Collins SM, Verdu E, and Ongini E. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 141: 1314-1322, 2011.
101. Wallace JL, Vong L, McKnight W, Dicay M, and Martin GR. Endogenous and exogenous hydrogen sulphide promotes resolution of colitis in rats. Gastroenterology 137: 569-578, 2009.
102. Wallace JL. Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci 28: 501-505, 2007.
103. Wallace JL. Mechanisms, prevention and clinical implications of nonsteroidal anti-inflammatory drug-enteropathy. World J Gastroenterol 19: 1861-1876, 2013.
104. Wallace JL. NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br J Pharmacol 165: 67-74, 2012.
105. Wallace JL. Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid Redox Signal 12: 1125-1133, 2010.
106. Wallace JL. Polypharmacy of osteoarthritis: the perfect intestinal storm. Dig Dis Sci 58: 3088-3093, 2013.
107. Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev 88: 1547-1565, 2008.
108. Wang L and Wallace JL. Hydrogen sulfide reduces cardioautonomic responses to gastric distention (GD) in an ATPsensitive potassium channel KATP-dependent manner. Neurogastroenterol Motil 23 (suppl 1): 59, 2011.
109. Wang R, Guo L, Wang P, Yang W, Lu Y, Huang Z, and Tang C. Chemoprevention of cancers in gastrointestinal tract with cyclooxygenase 2 inhibitors. Curr Pharm Des 19: 115-125, 2013.
110. Watanabe T, Higuchi K, Kobata A, Nishio H, Tanigawa T, Shiba M, Tominaga K, Fujiwara Y, Oshitani N, Asahara T, Nomoto K, Takeuchi K, and Arakawa T. Nonsteroidal anti-inflammatory drug-induced small intestinal damage is toll-like receptor 4 dependent. Gut 57: 181-187, 2008.
111. Whiteman M, Armstrong JS, Chu SH, Siau JL, Wong BS, Cheung NS, Halliwell B, and Moore PK. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite scavenger? J Neurochem 90: 765-768, 2004.
112. 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.
113. Whiteman M, Haigh R, Tarr JM, Gooding KM, Shore AC, and Winyard PG. Detection of hydrogen sulfide in plasma and knee-joint synovial fluid from rheumatoid arthritis patients: relation to clinical and laboratory measures of inflammation. Ann N Y Acad Sci 1203: 146-150, 2010.
114. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, and Wang R. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18: 1906-1919, 2013.
115. Zanardo RCO, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, and Wallace JL. Hydrogen sulphide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120, 2006.
116. Zhao W, Zhang J, Lu Y, and Wang R. The vasorelaxant effects of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20: 6008-6016, 2001.