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Published in: Digestive Diseases and Sciences 9/2017

01-09-2017 | Invited Review

Gaseous Mediators in Gastrointestinal Mucosal Defense and Injury

Authors: John L. Wallace, Angela Ianaro, Gilberto de Nucci

Published in: Digestive Diseases and Sciences | Issue 9/2017

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Abstract

Of the numerous gaseous substances that can act as signaling molecules, the best characterized are nitric oxide, carbon monoxide and hydrogen sulfide. Contributions of each of these low molecular weight substances, alone or in combination, to maintenance of gastrointestinal mucosal integrity have been established. There is considerable overlap in the actions of these gases in modulating mucosal defense and responses to injury, and in some instances they act in a cooperative manner. Each also play important roles in regulating inflammatory and repair processes throughout the gastrointestinal tract. In recent years, significant progress has been made in the development of novel anti-inflammatory and cytoprotective drugs that exploit the beneficial activities of one or more of these gaseous mediators.
Literature
1.
go back to reference Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn’t the stomach digest itself? Physiol Rev. 2008;88:1547–1565.CrossRefPubMed Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn’t the stomach digest itself? Physiol Rev. 2008;88:1547–1565.CrossRefPubMed
2.
go back to reference Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109–142.PubMed Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109–142.PubMed
3.
go back to reference Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066–1071.PubMed Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066–1071.PubMed
4.
6.
go back to reference Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov. 2015;14:329–345.CrossRefPubMed Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov. 2015;14:329–345.CrossRefPubMed
7.
go back to reference Olson KR, Straub KD. The role of hydrogen sulfide in evolution and the evolution of hydrogen sulfide in metabolism and signaling. Physiology. 2016;31:60–72.CrossRefPubMed Olson KR, Straub KD. The role of hydrogen sulfide in evolution and the evolution of hydrogen sulfide in metabolism and signaling. Physiology. 2016;31:60–72.CrossRefPubMed
8.
go back to reference Goubern M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F. Sulfide, the first inorganic substrate for human cells. FASEB J. 2007;21:1699–1706.CrossRefPubMed Goubern M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F. Sulfide, the first inorganic substrate for human cells. FASEB J. 2007;21:1699–1706.CrossRefPubMed
9.
go back to reference Mimoun S, Andriamihaja M, Chaumontet C, et al. Detoxification of H2S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal. 2012;17:1–10.CrossRefPubMed Mimoun S, Andriamihaja M, Chaumontet C, et al. Detoxification of H2S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal. 2012;17:1–10.CrossRefPubMed
10.
go back to reference Motterlini R, Foresti R. Biological signaling by carbon monoxide and carbon monoxide-releasing molecules. Am J Physiol Cell Physiol. 2017;312:C302–C313.CrossRefPubMed Motterlini R, Foresti R. Biological signaling by carbon monoxide and carbon monoxide-releasing molecules. Am J Physiol Cell Physiol. 2017;312:C302–C313.CrossRefPubMed
11.
go back to reference Chang M, Xue J, Sharma V, Habtezion A. Protective role of hemeoxygenase-1 in gastrointestinal diseases. Cell Mol Life Sci. 2015;72:1161–1173.CrossRefPubMed Chang M, Xue J, Sharma V, Habtezion A. Protective role of hemeoxygenase-1 in gastrointestinal diseases. Cell Mol Life Sci. 2015;72:1161–1173.CrossRefPubMed
12.
go back to reference Gibbons SJ, Verhurst PJ, Bharucha A, Farrugia G. Review article: carbon monoxide in gastrointestinal physiology and its potential in therapeutics. Aliment Pharmacol Ther. 2013;38:689–702.CrossRefPubMedPubMedCentral Gibbons SJ, Verhurst PJ, Bharucha A, Farrugia G. Review article: carbon monoxide in gastrointestinal physiology and its potential in therapeutics. Aliment Pharmacol Ther. 2013;38:689–702.CrossRefPubMedPubMedCentral
13.
go back to reference Farugia G, Szurszewski JH. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology. 2014;147:303–313.CrossRef Farugia G, Szurszewski JH. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology. 2014;147:303–313.CrossRef
14.
go back to reference Yoda Y, Amagase K, Kato S, et al. Prevention by lansoprazole, a proton pump inhibitor, of indomethacin-induced small intestinal ulceration in rats through induction of heme oxygenase-1. J Physiol Pharmacol. 2010;61:287–294.PubMed Yoda Y, Amagase K, Kato S, et al. Prevention by lansoprazole, a proton pump inhibitor, of indomethacin-induced small intestinal ulceration in rats through induction of heme oxygenase-1. J Physiol Pharmacol. 2010;61:287–294.PubMed
15.
go back to reference Brown JF, Hanson PJ, Whittle BJ. Nitric oxide donors increase mucus gel thickness in rat stomach. Eur J Pharmacol. 1992;223:103–104.CrossRefPubMed Brown JF, Hanson PJ, Whittle BJ. Nitric oxide donors increase mucus gel thickness in rat stomach. Eur J Pharmacol. 1992;223:103–104.CrossRefPubMed
16.
go back to reference Price KJ, Hanson PJ, Whittle BJR. Stimulation by carbachol of mucus gel thickness in rat stomach involves nitric oxide. Eur J Pharmacol. 1994;263:199–202.CrossRefPubMed Price KJ, Hanson PJ, Whittle BJR. Stimulation by carbachol of mucus gel thickness in rat stomach involves nitric oxide. Eur J Pharmacol. 1994;263:199–202.CrossRefPubMed
17.
go back to reference Lucetti LT, Silva RO, Santana AP, et al. Nitric oxide and hydrogen sulfide interact when modulating gastric physiological functions in rodents. Dig Dis Sci. 2017;62:93–104.CrossRefPubMed Lucetti LT, Silva RO, Santana AP, et al. Nitric oxide and hydrogen sulfide interact when modulating gastric physiological functions in rodents. Dig Dis Sci. 2017;62:93–104.CrossRefPubMed
18.
go back to reference Costa NR, Silva RO, Nicolau LA, et al. Role of soluble guanylate cyclase activation in the gastroprotective effect of the HO-1/CO pathway against alendronate-induced gastric damage in rats. Eur J Pharmacol. 2013;700:51–59.CrossRefPubMed Costa NR, Silva RO, Nicolau LA, et al. Role of soluble guanylate cyclase activation in the gastroprotective effect of the HO-1/CO pathway against alendronate-induced gastric damage in rats. Eur J Pharmacol. 2013;700:51–59.CrossRefPubMed
19.
go back to reference Motta JP, Flannigan KL, Agbor TA, et al. Hydrogen sulfide protects from colitis and restores intestinal microbiota biofilm and mucus production. Inflamm Bowel Dis. 2015;21:1006–1017.CrossRefPubMed Motta JP, Flannigan KL, Agbor TA, et al. Hydrogen sulfide protects from colitis and restores intestinal microbiota biofilm and mucus production. Inflamm Bowel Dis. 2015;21:1006–1017.CrossRefPubMed
20.
go back to reference Perdue MH, McKay DM. Integrative immunophysiology in the intestinal mucosa. Am J Physiol. 1994;267:G151–G165.PubMed Perdue MH, McKay DM. Integrative immunophysiology in the intestinal mucosa. Am J Physiol. 1994;267:G151–G165.PubMed
21.
go back to reference MacNaughton WK. Nitric oxide-donating compounds stimulate electrolyte transport in the guinea pig intestine in vitro. Life Sci. 1993;53:585–593.CrossRefPubMed MacNaughton WK. Nitric oxide-donating compounds stimulate electrolyte transport in the guinea pig intestine in vitro. Life Sci. 1993;53:585–593.CrossRefPubMed
22.
go back to reference Tamai H, Gaginella TS. Direct evidence for nitric oxide stimulation of electrolyte secretion in the rat colon. Free Radic Res. 1993;19:229–239.CrossRef Tamai H, Gaginella TS. Direct evidence for nitric oxide stimulation of electrolyte secretion in the rat colon. Free Radic Res. 1993;19:229–239.CrossRef
23.
go back to reference Asfaha S, MacNaughton WK, Appleyard CB, Chadee K, Wallace JL. Persistent epithelial dysfunction and bacterial translocation after resolution of intestinal inflammation. Am J Physiol Gastrointest Liver Physiol. 2001;281:G635–G644.PubMed Asfaha S, MacNaughton WK, Appleyard CB, Chadee K, Wallace JL. Persistent epithelial dysfunction and bacterial translocation after resolution of intestinal inflammation. Am J Physiol Gastrointest Liver Physiol. 2001;281:G635–G644.PubMed
24.
go back to reference Asfaha S, Bell CJ, Wallace JL, MacNaughton WK. Prolonged colonic epithelial hyperresponsiveness after colitis: role of inducible nitric oxide synthase. Am J Physiol. 1999;276:G703–G710.PubMed Asfaha S, Bell CJ, Wallace JL, MacNaughton WK. Prolonged colonic epithelial hyperresponsiveness after colitis: role of inducible nitric oxide synthase. Am J Physiol. 1999;276:G703–G710.PubMed
25.
go back to reference Takeuchi K, Aihara E, Kimura M, Dogishi K, Hara T, Hayashi S. Gas mediators involved in modulating duodenal HCO3 secretion. Curr Med Chem. 2012;19:43–54.CrossRefPubMed Takeuchi K, Aihara E, Kimura M, Dogishi K, Hara T, Hayashi S. Gas mediators involved in modulating duodenal HCO3 secretion. Curr Med Chem. 2012;19:43–54.CrossRefPubMed
26.
go back to reference Takasuka H, Hayashi S, Koyama M, et al. Carbon monoxide involved in modulating HCO 3 - secretion in rat duodenum. J Pharmacol Exp Ther. 2011;337:293–300.CrossRefPubMed Takasuka H, Hayashi S, Koyama M, et al. Carbon monoxide involved in modulating HCO 3 - secretion in rat duodenum. J Pharmacol Exp Ther. 2011;337:293–300.CrossRefPubMed
27.
go back to reference Takeuchi K, Kita K, Hayashi S, Aihara E. Regulatory mechanism of duodenal bicarbonate secretion: roles of endogenous prostaglandins and nitric oxide. Pharmacol Ther. 2011;130:59–70.CrossRefPubMed Takeuchi K, Kita K, Hayashi S, Aihara E. Regulatory mechanism of duodenal bicarbonate secretion: roles of endogenous prostaglandins and nitric oxide. Pharmacol Ther. 2011;130:59–70.CrossRefPubMed
28.
go back to reference Blackler R, Syer S, Bolla M, Ongini E, Wallace JL. Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS ONE. 2012;7:e35196.CrossRefPubMedPubMedCentral Blackler R, Syer S, Bolla M, Ongini E, Wallace JL. Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS ONE. 2012;7:e35196.CrossRefPubMedPubMedCentral
29.
go back to reference Mard SA, Askari H, Neisi N, Veisi A. Antisecretory effect of hydrogen sulfide on gastric acid secretion and the involvement of nitric oxide. Biomed Res Int. 2014;2014:480921.CrossRefPubMedPubMedCentral Mard SA, Askari H, Neisi N, Veisi A. Antisecretory effect of hydrogen sulfide on gastric acid secretion and the involvement of nitric oxide. Biomed Res Int. 2014;2014:480921.CrossRefPubMedPubMedCentral
30.
go back to reference Verdu E, Viani F, Armstrong D, et al. Effect of omeprazole on intragastric bacterial counts, nitrates, nitrites, and N-nitroso compounds. Gut. 1994;35:455–460.CrossRefPubMedPubMedCentral Verdu E, Viani F, Armstrong D, et al. Effect of omeprazole on intragastric bacterial counts, nitrates, nitrites, and N-nitroso compounds. Gut. 1994;35:455–460.CrossRefPubMedPubMedCentral
31.
go back to reference Imhann F, Vich Vila A, Bonder MJ, et al. The influence of proton pump inhibitors and other commonly used medication on the gut microbiota. Gut Microbes. 2017;24:1–8.CrossRef Imhann F, Vich Vila A, Bonder MJ, et al. The influence of proton pump inhibitors and other commonly used medication on the gut microbiota. Gut Microbes. 2017;24:1–8.CrossRef
32.
go back to reference Keszthelyi D, Jansen SV, Schouten GA, et al. Proton pump inhibitor use is associated with an increased risk for microscopic colitis: a case-control study. Aliment Pharmacol Ther. 2010;32:1124–1128.CrossRefPubMed Keszthelyi D, Jansen SV, Schouten GA, et al. Proton pump inhibitor use is associated with an increased risk for microscopic colitis: a case-control study. Aliment Pharmacol Ther. 2010;32:1124–1128.CrossRefPubMed
33.
go back to reference Shah R, Richardson P, Yu H, Kramer J, Hou JK. Gastric acid suppression is associated with an increased risk of adverse outcomes in inflammatory bowel disease. Digestion. 2017;95:188–193.CrossRefPubMed Shah R, Richardson P, Yu H, Kramer J, Hou JK. Gastric acid suppression is associated with an increased risk of adverse outcomes in inflammatory bowel disease. Digestion. 2017;95:188–193.CrossRefPubMed
34.
go back to reference Fujimori S. What are the effects of proton pump inhibitors on the small intestine? World J Gastroenterol. 2015;21:6817–6819.PubMedPubMedCentral Fujimori S. What are the effects of proton pump inhibitors on the small intestine? World J Gastroenterol. 2015;21:6817–6819.PubMedPubMedCentral
35.
go back to reference Wallace JL, Syer S, Denou E, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011;141:1314–1322.CrossRefPubMed Wallace JL, Syer S, Denou E, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011;141:1314–1322.CrossRefPubMed
36.
go back to reference Watanabe T, Tanigawa T, Nadatani Y, et al. Risk factors for severe nonsteroidal anti-inflammatory drug-induced small intestinal damage. Dig Liver Dis. 2013;45:390–395.CrossRefPubMed Watanabe T, Tanigawa T, Nadatani Y, et al. Risk factors for severe nonsteroidal anti-inflammatory drug-induced small intestinal damage. Dig Liver Dis. 2013;45:390–395.CrossRefPubMed
37.
go back to reference Washio E, Esaki M, Maehata Y, et al. Proton pump inhibitors increase incidence of nonsteroidal anti-inflammatory drug-induced small bowel injury: a randomized placebo-controlled trial. Clin Gastroenterol Hepatol. 2016;14:809–815.CrossRefPubMed Washio E, Esaki M, Maehata Y, et al. Proton pump inhibitors increase incidence of nonsteroidal anti-inflammatory drug-induced small bowel injury: a randomized placebo-controlled trial. Clin Gastroenterol Hepatol. 2016;14:809–815.CrossRefPubMed
38.
go back to reference Nuki Y, Umeno J, Washio E, et al. The influence of CYP2C19 polymorphisms on exacerbating effect of rabeprazole in celecoxib-induced small bowel injury. Aliment Pharmacol Ther. 2017. doi:10.1111/apt.14134.PubMed Nuki Y, Umeno J, Washio E, et al. The influence of CYP2C19 polymorphisms on exacerbating effect of rabeprazole in celecoxib-induced small bowel injury. Aliment Pharmacol Ther. 2017. doi:10.​1111/​apt.​14134.PubMed
39.
go back to reference Blackler RW, De Palma G, Manko A, et al. Deciphering the pathogenesis of NSAID enteropathy using proton pump inhibitors and a hydrogen sulfide-releasing NSAID. Am J Physiol Gastrointest Liver Physiol. 2015;308:G994–G1003.CrossRefPubMed Blackler RW, De Palma G, Manko A, et al. Deciphering the pathogenesis of NSAID enteropathy using proton pump inhibitors and a hydrogen sulfide-releasing NSAID. Am J Physiol Gastrointest Liver Physiol. 2015;308:G994–G1003.CrossRefPubMed
40.
go back to reference Blackler RW, Motta JP, Manko A, et al. Hydrogen sulphide protects against NSAID-enteropathy through modulation of bile and the microbiota. Br J Pharmacol. 2015;172:992–1004.CrossRefPubMed Blackler RW, Motta JP, Manko A, et al. Hydrogen sulphide protects against NSAID-enteropathy through modulation of bile and the microbiota. Br J Pharmacol. 2015;172:992–1004.CrossRefPubMed
41.
go back to reference Kidder GW. Carbon monoxide insensitivity of gastric acid secretion. Am J Physiol. 1980;238:G197–G202.PubMed Kidder GW. Carbon monoxide insensitivity of gastric acid secretion. Am J Physiol. 1980;238:G197–G202.PubMed
42.
go back to reference Pique JM, Esplugues JV, Whittle BJ. Endogenous nitric oxide as a mediator of gastric mucosal vasodilatation during acid secretion. Gastroenterology. 1992;102:168–174.CrossRefPubMed Pique JM, Esplugues JV, Whittle BJ. Endogenous nitric oxide as a mediator of gastric mucosal vasodilatation during acid secretion. Gastroenterology. 1992;102:168–174.CrossRefPubMed
43.
go back to reference Holzer P, Sametz W. Gastric mucosal protection against ulcerogenicfactors in the rat mediated by capsaicin-sensitive afferent neurons. Gastroenterology. 1986;91:975–981.CrossRefPubMed Holzer P, Sametz W. Gastric mucosal protection against ulcerogenicfactors in the rat mediated by capsaicin-sensitive afferent neurons. Gastroenterology. 1986;91:975–981.CrossRefPubMed
44.
45.
go back to reference Lippe IT, Holzer P. Participation of endothelium-derived nitric oxide but not prostacyclin in the gastric mucosal hyperaemia due to acid back-diffusion. Br J Pharmacol. 1992;105:708–714.CrossRefPubMedPubMedCentral Lippe IT, Holzer P. Participation of endothelium-derived nitric oxide but not prostacyclin in the gastric mucosal hyperaemia due to acid back-diffusion. Br J Pharmacol. 1992;105:708–714.CrossRefPubMedPubMedCentral
46.
go back to reference Fiorucci S, Antonelli T, Distrutti E, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory non-steroidal drugs. Gastroenterology. 2005;129:1210–1224.CrossRefPubMed Fiorucci S, Antonelli T, Distrutti E, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory non-steroidal drugs. Gastroenterology. 2005;129:1210–1224.CrossRefPubMed
47.
go back to reference Magierowska K, Magierowski M, Hubalewska-Mazgaj M, et al. Carbon monoxide (CO) released from tricarbonyldichlororuthenium (II) dimer (CORM-2) in gastroprotection against experimental ethanol-induced gastric damage. PLoS One. 2015;10:e0140493.CrossRefPubMedPubMedCentral Magierowska K, Magierowski M, Hubalewska-Mazgaj M, et al. Carbon monoxide (CO) released from tricarbonyldichlororuthenium (II) dimer (CORM-2) in gastroprotection against experimental ethanol-induced gastric damage. PLoS One. 2015;10:e0140493.CrossRefPubMedPubMedCentral
48.
go back to reference Magierowski M, Magierowska K, Hubalewska-Mazgaj M, et al. Interaction between endogenous carbon monoxide and hydrogen sulfide in the mechanism of gastroprotection against acute aspirin-induced gastric damage. Pharmacol Res. 2016;114:235–250.CrossRefPubMed Magierowski M, Magierowska K, Hubalewska-Mazgaj M, et al. Interaction between endogenous carbon monoxide and hydrogen sulfide in the mechanism of gastroprotection against acute aspirin-induced gastric damage. Pharmacol Res. 2016;114:235–250.CrossRefPubMed
49.
go back to reference Banick PD, Chen QP, Xu YA, Thom SR. Nitric oxide inhibits neutrophil b2 integrin function by inhibiting membrane-associated cyclic GMP synthesis. J Cell Physiol. 1997;172:12–24.CrossRefPubMed Banick PD, Chen QP, Xu YA, Thom SR. Nitric oxide inhibits neutrophil b2 integrin function by inhibiting membrane-associated cyclic GMP synthesis. J Cell Physiol. 1997;172:12–24.CrossRefPubMed
50.
go back to reference Davenpeck KL, Gauthier TW, Lefer AM. Inhibition of endothelial derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology. 1994;107:1050–1058.CrossRefPubMed Davenpeck KL, Gauthier TW, Lefer AM. Inhibition of endothelial derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology. 1994;107:1050–1058.CrossRefPubMed
52.
go back to reference Wallace JL, Vergnolle N, Muscara MN, et al. Enhanced anti-inflammatory effects of a nitric oxide-releasing derivative of mesalamine in rats. Gastroenterology. 1999;117:557–566.CrossRefPubMed Wallace JL, Vergnolle N, Muscara MN, et al. Enhanced anti-inflammatory effects of a nitric oxide-releasing derivative of mesalamine in rats. Gastroenterology. 1999;117:557–566.CrossRefPubMed
53.
go back to reference Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006;20:2118–2120.CrossRefPubMed Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006;20:2118–2120.CrossRefPubMed
54.
go back to reference Wallace JL, Caliendo G, Santagada V, Cirino G. Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). Br J Pharmacol. 2010;159:1236–1246.CrossRefPubMedPubMedCentral Wallace JL, Caliendo G, Santagada V, Cirino G. Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). Br J Pharmacol. 2010;159:1236–1246.CrossRefPubMedPubMedCentral
55.
go back to reference Urquhart P, Rosignoli G, Cooper D, Motterlini R, Perretti M. Carbon monoxide-releasing molecules modulate leukocyte-endothelial interactions under flow. J Pharmacol Exp Ther. 2007;321:656–662.CrossRefPubMed Urquhart P, Rosignoli G, Cooper D, Motterlini R, Perretti M. Carbon monoxide-releasing molecules modulate leukocyte-endothelial interactions under flow. J Pharmacol Exp Ther. 2007;321:656–662.CrossRefPubMed
56.
go back to reference Paul G, Bataille F, Obermeier F, et al. Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin Exp Immunol. 2005;140:547–555.CrossRefPubMedPubMedCentral Paul G, Bataille F, Obermeier F, et al. Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin Exp Immunol. 2005;140:547–555.CrossRefPubMedPubMedCentral
57.
go back to reference Tepperman BL, Soper BD. Nitric oxide synthase induction and cytoprotection of rat gastric mucosa from injury by ethanol. Can J Physiol Pharmacol. 1994;72:1308–1312.CrossRefPubMed Tepperman BL, Soper BD. Nitric oxide synthase induction and cytoprotection of rat gastric mucosa from injury by ethanol. Can J Physiol Pharmacol. 1994;72:1308–1312.CrossRefPubMed
58.
go back to reference Motterlini R, Foresti R, Intaglietta M, Winslow RM. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol. 1996;270:H107–H114.PubMed Motterlini R, Foresti R, Intaglietta M, Winslow RM. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol. 1996;270:H107–H114.PubMed
59.
go back to reference Lohmander LS, McKeith D, Svensson O, et al. Ramos-Remus C; STAR Multinational Study Group. A randomised, placebo controlled, comparative trial of the gastrointestinal safety and efficacy of AZD3582 versus naproxen in osteoarthritis. Ann Rheum Dis. 2005;64:449–456.CrossRefPubMed Lohmander LS, McKeith D, Svensson O, et al. Ramos-Remus C; STAR Multinational Study Group. A randomised, placebo controlled, comparative trial of the gastrointestinal safety and efficacy of AZD3582 versus naproxen in osteoarthritis. Ann Rheum Dis. 2005;64:449–456.CrossRefPubMed
60.
go back to reference Wallace JL. Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid Redox Signal. 2010;12:1125–1133.CrossRefPubMed Wallace JL. Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid Redox Signal. 2010;12:1125–1133.CrossRefPubMed
61.
go back to reference Wallace JL, Vaughan D, Dicay M, MacNaughton WK, de Nucci G. Hydrogen sulfide-releasing therapeutics: Translation to the clinic. Antiox Redox Signal 2017; in press (doi: 10.1089/ars.2017.7068). Wallace JL, Vaughan D, Dicay M, MacNaughton WK, de Nucci G. Hydrogen sulfide-releasing therapeutics: Translation to the clinic. Antiox Redox Signal 2017; in press (doi: 10.​1089/​ars.​2017.​7068).
62.
go back to reference Uc A, Zhu X, Wagner BA, Guettner GR, Berg DJ. Heme oxygenase-1 is protective against nonsteroidal anti-inflammatory drug-induced gastric ulcers. J Ped Gastroenterol Nutr. 2012;54:471–476.CrossRef Uc A, Zhu X, Wagner BA, Guettner GR, Berg DJ. Heme oxygenase-1 is protective against nonsteroidal anti-inflammatory drug-induced gastric ulcers. J Ped Gastroenterol Nutr. 2012;54:471–476.CrossRef
63.
go back to reference Cheng Y-T, Wu C-H, Ho C-Y, Yen G-C. Catechin protects against ketoprofen-induced oxidative damage of the gastric mucosa by up-regulating Nrf2 in vitro and in vivo. J Nutr Biochem. 2013;24:475–483.CrossRefPubMed Cheng Y-T, Wu C-H, Ho C-Y, Yen G-C. Catechin protects against ketoprofen-induced oxidative damage of the gastric mucosa by up-regulating Nrf2 in vitro and in vivo. J Nutr Biochem. 2013;24:475–483.CrossRefPubMed
64.
go back to reference De Backer O, Elinck E, Blanckaert B, Leybaert L, Motterlini R, Lefebvre RA. Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut. 2009;58:347–356.CrossRefPubMed De Backer O, Elinck E, Blanckaert B, Leybaert L, Motterlini R, Lefebvre RA. Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut. 2009;58:347–356.CrossRefPubMed
65.
go back to reference Konturek SJ, Brzozowski T, Majka J, Pytko-Polonczyk J, Stachura J. Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. Eur J Pharmacol. 1993;239:215–217.CrossRefPubMed Konturek SJ, Brzozowski T, Majka J, Pytko-Polonczyk J, Stachura J. Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. Eur J Pharmacol. 1993;239:215–217.CrossRefPubMed
66.
go back to reference Elliott SN, McKnight W, Cirino G, Wallace JL. A nitric oxide-releasing nonsteroidal anti-inflammatory drug accelerates gastric ulcer healing in rats. Gastroenterology. 1995;109:524–530.CrossRefPubMed Elliott SN, McKnight W, Cirino G, Wallace JL. A nitric oxide-releasing nonsteroidal anti-inflammatory drug accelerates gastric ulcer healing in rats. Gastroenterology. 1995;109:524–530.CrossRefPubMed
67.
go back to reference Wallace JL, Dicay M, McKnight W, Martin GR. Hydrogen sulfide enhances ulcer healing in rats. FASEB J. 2007;21:4070–4076.CrossRefPubMed Wallace JL, Dicay M, McKnight W, Martin GR. Hydrogen sulfide enhances ulcer healing in rats. FASEB J. 2007;21:4070–4076.CrossRefPubMed
68.
go back to reference Wallace JL, Vong L, McKnight W, Dicay M, Martin GR. Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology. 2009;137:569–578.CrossRefPubMed Wallace JL, Vong L, McKnight W, Dicay M, Martin GR. Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology. 2009;137:569–578.CrossRefPubMed
69.
go back to reference Flannigan KL, Ferraz JGP, Wang R, Wallace JL. Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: A site-specific, pro-resolution mechanism. PLoS One. 2013;8:e71962.CrossRefPubMedPubMedCentral Flannigan KL, Ferraz JGP, Wang R, Wallace JL. Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: A site-specific, pro-resolution mechanism. PLoS One. 2013;8:e71962.CrossRefPubMedPubMedCentral
70.
go back to reference Takagi T, Naito Y, Uchiyama K, et al. Carbon monoxide promotes gastric wound healing in mice via the protein kinase C pathway. Free Radic Res. 2016;50:1098–1105.CrossRefPubMed Takagi T, Naito Y, Uchiyama K, et al. Carbon monoxide promotes gastric wound healing in mice via the protein kinase C pathway. Free Radic Res. 2016;50:1098–1105.CrossRefPubMed
71.
go back to reference Schaffer MR, Tantry U, Gross SS, Wasserkrug HL, Barbul A. Nitric oxide regulates wound healing. J Surg Res. 1996;63:237–240.CrossRefPubMed Schaffer MR, Tantry U, Gross SS, Wasserkrug HL, Barbul A. Nitric oxide regulates wound healing. J Surg Res. 1996;63:237–240.CrossRefPubMed
72.
go back to reference Hirose H, Takeuchi K, Okabe S. Effect of indomethacin on gastric mucosal blood flow around acetic acid–induced gastric ulcers in rats. Gastroenterology. 1991;100:1259–1265.CrossRefPubMed Hirose H, Takeuchi K, Okabe S. Effect of indomethacin on gastric mucosal blood flow around acetic acid–induced gastric ulcers in rats. Gastroenterology. 1991;100:1259–1265.CrossRefPubMed
73.
go back to reference Papapetropoulos A, Foresti R, Ferdiandy P. Pharmacology of the ‘gasotransmitters’ NO, CO and H2S: translational opportunities. Br J Pharmacol. 2015;172:1395–1396.CrossRefPubMedPubMedCentral Papapetropoulos A, Foresti R, Ferdiandy P. Pharmacology of the ‘gasotransmitters’ NO, CO and H2S: translational opportunities. Br J Pharmacol. 2015;172:1395–1396.CrossRefPubMedPubMedCentral
74.
go back to reference Flannigan KL, Agbor TA, Blackler RW, et al. Impaired hydrogen sulfide synthesis and IL-10 signaling underlie hyperhomocysteinemia-associated exacerbation of colitis. Proc Natl Acad Sci USA. 2014;111:13559–13564.CrossRefPubMedPubMedCentral Flannigan KL, Agbor TA, Blackler RW, et al. Impaired hydrogen sulfide synthesis and IL-10 signaling underlie hyperhomocysteinemia-associated exacerbation of colitis. Proc Natl Acad Sci USA. 2014;111:13559–13564.CrossRefPubMedPubMedCentral
75.
go back to reference Lagoutte E, Mimoun S, Andriamihaja M, et al. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta. 2010;1797:1500–1511.CrossRefPubMed Lagoutte E, Mimoun S, Andriamihaja M, et al. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta. 2010;1797:1500–1511.CrossRefPubMed
76.
go back to reference Shen X, Carlström M, Borniquel S, Jädert C, Kevil CG, Lundberg JO. Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic Biol Med. 2013;60:195–200.CrossRefPubMedPubMedCentral Shen X, Carlström M, Borniquel S, Jädert C, Kevil CG, Lundberg JO. Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic Biol Med. 2013;60:195–200.CrossRefPubMedPubMedCentral
77.
go back to reference Flannigan KL, McCoy KD, Wallace JL. Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am J Physiol Gastrointest Liver Physiol. 2011;301:G188–G193.CrossRefPubMed Flannigan KL, McCoy KD, Wallace JL. Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am J Physiol Gastrointest Liver Physiol. 2011;301:G188–G193.CrossRefPubMed
78.
go back to reference Lund JN, Scholefield JH. Glyceryl trinitrate is an effective treatment for anal fissure. Dis Colon Rectum. 1997;40:468–470.CrossRefPubMed Lund JN, Scholefield JH. Glyceryl trinitrate is an effective treatment for anal fissure. Dis Colon Rectum. 1997;40:468–470.CrossRefPubMed
79.
go back to reference Hogaboam CM, Jacobson K, Collins SM, Blennerhassett MG. The selective beneficial effects of nitric oxide inhibition in experimental colitis. Am J Physiol. 1995;268:G673–G684.PubMed Hogaboam CM, Jacobson K, Collins SM, Blennerhassett MG. The selective beneficial effects of nitric oxide inhibition in experimental colitis. Am J Physiol. 1995;268:G673–G684.PubMed
80.
go back to reference Aiko S, Fuseler J, Grisham MB. Effects of nitric oxide synthase inhibition or sulfasalazine on the spontaneous colitis observed in HLA-B27 transgenic rats. J Pharmacol Exp Ther. 1998;284:722–727.PubMed Aiko S, Fuseler J, Grisham MB. Effects of nitric oxide synthase inhibition or sulfasalazine on the spontaneous colitis observed in HLA-B27 transgenic rats. J Pharmacol Exp Ther. 1998;284:722–727.PubMed
81.
go back to reference Soufli I, Toumi R, Rafa H, Touil-Boukoffa C. Overview of cytokines and nitric oxide involvement in immuno-pathogenesis of inflammatory bowel diseases. World J Gastrointest Pharmacol Ther. 2016;7:353–360.CrossRefPubMedPubMedCentral Soufli I, Toumi R, Rafa H, Touil-Boukoffa C. Overview of cytokines and nitric oxide involvement in immuno-pathogenesis of inflammatory bowel diseases. World J Gastrointest Pharmacol Ther. 2016;7:353–360.CrossRefPubMedPubMedCentral
82.
go back to reference McCafferty DM, Mudgett JS, Swain MG, Kubes P. Inducible nitric oxide synthase plays a critical role in resolving intestinal inflammation. Gastroenterology. 1997;112:1022–1027.CrossRefPubMed McCafferty DM, Mudgett JS, Swain MG, Kubes P. Inducible nitric oxide synthase plays a critical role in resolving intestinal inflammation. Gastroenterology. 1997;112:1022–1027.CrossRefPubMed
83.
go back to reference Takagi T, Naito Y, Uchiyama K, et al. Carbon monoxide liberated from carbon monoxide-releasing molecule exerts an anti-inflammatory effect on dextran sulfate sodium-induced colitis in mice. Dig Dis Sci. 2011;56:1663–1671.CrossRefPubMed Takagi T, Naito Y, Uchiyama K, et al. Carbon monoxide liberated from carbon monoxide-releasing molecule exerts an anti-inflammatory effect on dextran sulfate sodium-induced colitis in mice. Dig Dis Sci. 2011;56:1663–1671.CrossRefPubMed
84.
go back to reference Uddin MJ, Jeong SO, Zheng M, et al. Carbon monoxide attenuates dextran sulfate sodium-induced colitis via inhibition of GSK-3ß signaling. Oxid Med Cell Longev. 2013;2013:210563.CrossRefPubMedPubMedCentral Uddin MJ, Jeong SO, Zheng M, et al. Carbon monoxide attenuates dextran sulfate sodium-induced colitis via inhibition of GSK-3ß signaling. Oxid Med Cell Longev. 2013;2013:210563.CrossRefPubMedPubMedCentral
85.
go back to reference Megias J, Busserolles J, Alcaraz MJ. The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol. 2007;150:977–986.CrossRefPubMedPubMedCentral Megias J, Busserolles J, Alcaraz MJ. The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol. 2007;150:977–986.CrossRefPubMedPubMedCentral
86.
go back to reference Onyiah JC, Sheikh SZ, Maharshak N, Otterbein LE, Plevy SE. Heme oxygenase-1 and carbon monoxide regulate intestinal homeostasis and mucosal immune responses to the enteric microbiota. Gut Microbes. 2014;5:220–224.CrossRefPubMed Onyiah JC, Sheikh SZ, Maharshak N, Otterbein LE, Plevy SE. Heme oxygenase-1 and carbon monoxide regulate intestinal homeostasis and mucosal immune responses to the enteric microbiota. Gut Microbes. 2014;5:220–224.CrossRefPubMed
87.
go back to reference Szczesny B, Módis K, Yanagi K, et al. AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide. 2014;41:120–130.CrossRefPubMedPubMedCentral Szczesny B, Módis K, Yanagi K, et al. AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide. 2014;41:120–130.CrossRefPubMedPubMedCentral
88.
go back to reference Shibuya N, Koike S, Tanaka M, et al. A novel pathway for the production of hydrogen sulfide from d-cysteine in mammalian cells. Nat Commun. 2013;4:1366.CrossRefPubMed Shibuya N, Koike S, Tanaka M, et al. A novel pathway for the production of hydrogen sulfide from d-cysteine in mammalian cells. Nat Commun. 2013;4:1366.CrossRefPubMed
89.
go back to reference Wallace JL, Blackler RW, Chan MV, et al. Anti-inflammatory and cytoprotective actions of hydrogen sulfide: translation to therapeutics. Antiox Redox Signal. 2015;22:398–410.CrossRef Wallace JL, Blackler RW, Chan MV, et al. Anti-inflammatory and cytoprotective actions of hydrogen sulfide: translation to therapeutics. Antiox Redox Signal. 2015;22:398–410.CrossRef
Metadata
Title
Gaseous Mediators in Gastrointestinal Mucosal Defense and Injury
Authors
John L. Wallace
Angela Ianaro
Gilberto de Nucci
Publication date
01-09-2017
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 9/2017
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-017-4681-0

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