Skip to main content
Top
Published in: Digestive Diseases and Sciences 1/2017

01-01-2017 | Original Article

Nitric Oxide and Hydrogen Sulfide Interact When Modulating Gastric Physiological Functions in Rodents

Authors: Larisse Tavares Lucetti, Renan Oliveira Silva, Ana Paula Macedo Santana, Bruno de Melo Tavares, Mariana Lima Vale, Pedro Marcos Gomes Soares, Francisco José Batista de Lima Júnior, Pedro Jorge Caldas Magalhães, Fernando de Queiroz Cunha, Ronaldo de Albuquerque Ribeiro, Jand-Venes Rolim Medeiros, Marcellus Henrique Loiola Ponte Souza

Published in: Digestive Diseases and Sciences | Issue 1/2017

Login to get access

Abstract

Aim

The objective was to evaluate the effects of nitric oxide (NO) and hydrogen sulfide (H2S) donors and possible interactions between these two systems in modulating gastric function.

Methods

Mice received saline, sodium nitroprusside (SNP), or sodium hydrosulfite (NaHS), and after 1 h, the animals were killed for immunofluorescence analysis of CSE or eNOS expressions, respectively. Other groups received saline, SNP, NaHS, Lawesson’s reagent (H2S donor), PAG + SNP, l-NAME, l-NAME + NaHS, or l-NAME + Lawesson’s reagent. Then, the gastric secretions (mucous and acid), gastric blood flow, gastric defense against ethanol, and gastric motility (gastric emptying and gastric contractility) were evaluated.

Results

SNP and NaHS increased the expression of CSE or eNOS, respectively. SNP or Lawesson’s reagent did not alter gastric acid secretion but increased mucus production, and these effects reverted with PAG and l-NAME treatment, respectively. SNP or NaHS increased gastric blood flow and protected the gastric mucosa against ethanol injury, and these effects reverted with PAG and l-NAME treatments, respectively. SNP delayed gastric emptying when compared with saline, and PAG partially reversed this effect. NaHS accelerate gastric emptying, and l-NAME partially reversed this effect. SNP and NaHS alone induced gastric fundus and pylorus relaxation. However, pretreatment with PAG or l-NAME reversed these relaxant effects only in the pylorus but not in the gastric fundus.

Conclusion

NO and H2S interact in gastric physiological functions, and this “cross-talk” is important in the control of mucus secretion, gastric blood flow, gastric mucosal defense, and gastric motility, but not in the control of basal gastric acid secretion.
Literature
1.
go back to reference Martin F, Kenneth RO. Embracing sulfide and CO to understand nitric oxide biology. Nitric Oxide. 2013;35:2–4.CrossRef Martin F, Kenneth RO. Embracing sulfide and CO to understand nitric oxide biology. Nitric Oxide. 2013;35:2–4.CrossRef
2.
go back to reference Wang R. Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 2002;16:1792–1798.CrossRefPubMed Wang R. Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 2002;16:1792–1798.CrossRefPubMed
3.
go back to reference Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H. Protective role of endothelial nitric oxide synthase. J Pathol. 2003;199:8–17.CrossRefPubMed Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H. Protective role of endothelial nitric oxide synthase. J Pathol. 2003;199:8–17.CrossRefPubMed
4.
go back to reference Matsuda NM, Miller SM. Non-adrenergic non-cholinergic inhibition of GI smooth muscle and its intracelular mechanism(s). Fundam Clin Pharmacol. 2010;24:261–268.CrossRefPubMed Matsuda NM, Miller SM. Non-adrenergic non-cholinergic inhibition of GI smooth muscle and its intracelular mechanism(s). Fundam Clin Pharmacol. 2010;24:261–268.CrossRefPubMed
5.
go back to reference Takahashi T. Pathophysiological significance of neuronal nitric oxide synthase in the GI tract. J Gastroenterol. 2003;38:421–430.CrossRefPubMed Takahashi T. Pathophysiological significance of neuronal nitric oxide synthase in the GI tract. J Gastroenterol. 2003;38:421–430.CrossRefPubMed
6.
go back to reference Lowicka E, Bełtowski J. Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists. Pharmacol Rep. 2007;59:4–24.PubMed Lowicka E, Bełtowski J. Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists. Pharmacol Rep. 2007;59:4–24.PubMed
7.
8.
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
9.
go back to reference Dal-Secco D, Cunha TM, Freitas A, et al. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels. J Immunol. 2008;181:4287–4298.CrossRefPubMed Dal-Secco D, Cunha TM, Freitas A, et al. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels. J Immunol. 2008;181:4287–4298.CrossRefPubMed
10.
go back to reference Magierowski M, Jasnos K, Kwiecien S, et al. Endogenous prostaglandins and afferent sensory nerves in gastroprotective effect of hydrogen sulfide against stress-induced gastric lesions. PLoS One. 2015;10:e0118972.CrossRefPubMedPubMedCentral Magierowski M, Jasnos K, Kwiecien S, et al. Endogenous prostaglandins and afferent sensory nerves in gastroprotective effect of hydrogen sulfide against stress-induced gastric lesions. PLoS One. 2015;10:e0118972.CrossRefPubMedPubMedCentral
11.
go back to reference Fiorucci S, Distrutti E, Cirino G, Wallace JL. The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology. 2006;131:259–271.CrossRefPubMed Fiorucci S, Distrutti E, Cirino G, Wallace JL. The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology. 2006;131:259–271.CrossRefPubMed
12.
go back to reference Medeiros JV, Bezerra VH, Gomes AS, et al. Hydrogen sulphide prevents ethanol-induced gastric damage in mice: role of KATP channels and capsaicin-sensitive primary afferent neurons. J Pharmacol Exp Ther. 2009;330:764–770.CrossRefPubMed Medeiros JV, Bezerra VH, Gomes AS, et al. Hydrogen sulphide prevents ethanol-induced gastric damage in mice: role of KATP channels and capsaicin-sensitive primary afferent neurons. J Pharmacol Exp Ther. 2009;330:764–770.CrossRefPubMed
13.
go back to reference Santana AP, Tavares BM, Lucetti LT Jr, et al. The nitric oxide donor cis-[Ru(bpy)2(SO3)NO](PF6) increases gastric mucosa protection in mice—involvement of the soluble guanylate cyclase/KATP pathway. Nitric Oxide. 2015;45:35–42.CrossRefPubMed Santana AP, Tavares BM, Lucetti LT Jr, et al. The nitric oxide donor cis-[Ru(bpy)2(SO3)NO](PF6) increases gastric mucosa protection in mice—involvement of the soluble guanylate cyclase/KATP pathway. Nitric Oxide. 2015;45:35–42.CrossRefPubMed
14.
go back to reference Hosoki R, Matsuki N, Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun. 1997;237:527–531.CrossRefPubMed Hosoki R, Matsuki N, Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun. 1997;237:527–531.CrossRefPubMed
15.
go back to reference Takeuchi K, Ise F, Takahashi K, Aihara E, Hayashi S. H2S-induced HCO3 − secretion in the rat stomach-involvement of nitric oxide, prostaglandins, and capsaicin-sensitive sensory neurons. Nitric Oxide. 2015;30:157–164.CrossRef Takeuchi K, Ise F, Takahashi K, Aihara E, Hayashi S. H2S-induced HCO3 secretion in the rat stomach-involvement of nitric oxide, prostaglandins, and capsaicin-sensitive sensory neurons. Nitric Oxide. 2015;30:157–164.CrossRef
16.
17.
go back to reference Coletta C, Papapetropoulos A, Erdelyi K, et al. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA. 2012;109:9161–9166.CrossRefPubMedPubMedCentral Coletta C, Papapetropoulos A, Erdelyi K, et al. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA. 2012;109:9161–9166.CrossRefPubMedPubMedCentral
18.
go back to reference Magalhães PA, de Brito TS, Freire RS, et al. Metabolic acidosis aggravates experimental acute kidney injury. Life Sci. 2016;146:58–65.CrossRefPubMed Magalhães PA, de Brito TS, Freire RS, et al. Metabolic acidosis aggravates experimental acute kidney injury. Life Sci. 2016;146:58–65.CrossRefPubMed
19.
go back to reference Reitman S. Gastric secretion. In: Frankel S, Reitman S, Sonnenwirth AC, eds. Gradwohl’s Clinical Laboratory Methods and Diagnosis. London: Mosby; 1970:1949–1958. Reitman S. Gastric secretion. In: Frankel S, Reitman S, Sonnenwirth AC, eds. Gradwohl’s Clinical Laboratory Methods and Diagnosis. London: Mosby; 1970:1949–1958.
20.
go back to reference Carvalho ACS, Guedes MM, Sousa AL, et al. Gastroprotective effect of mangiferin, a xanthonoid from mangifera indica, against gastric injury induced by ethanol and indomethacin in rodents. Planta Medica (Stuttgart). 2007;73:1372–1376.CrossRef Carvalho ACS, Guedes MM, Sousa AL, et al. Gastroprotective effect of mangiferin, a xanthonoid from mangifera indica, against gastric injury induced by ethanol and indomethacin in rodents. Planta Medica (Stuttgart). 2007;73:1372–1376.CrossRef
21.
go back to reference Corne SJ, Morrissey SM, Woods RJ. A method for the quantitative estimation of gastric barrier mucous. J Physiol. 1974;242:116–117. Corne SJ, Morrissey SM, Woods RJ. A method for the quantitative estimation of gastric barrier mucous. J Physiol. 1974;242:116–117.
22.
go back to reference Ancha H, Ojeas H, Tedesco D, Ward A, Harty RF. Somatostatin-induced gastric protection against ethanol: involvement of nitric oxide and effects on gastric mucosal blood flow. Regul Pept. 2003;110:107–113.CrossRefPubMed Ancha H, Ojeas H, Tedesco D, Ward A, Harty RF. Somatostatin-induced gastric protection against ethanol: involvement of nitric oxide and effects on gastric mucosal blood flow. Regul Pept. 2003;110:107–113.CrossRefPubMed
23.
go back to reference Camara PRS, Ferraz GJN, Franco-Penteado CF. Ablation of primary afferent neurons by neonatal capsaicin treatment reduces the susceptibility of the portal hypertensive gastric mucosa to ethanol-induced injury in cirrhotic rats. Eur J Pharmacol. 2008;589:245–250.CrossRefPubMed Camara PRS, Ferraz GJN, Franco-Penteado CF. Ablation of primary afferent neurons by neonatal capsaicin treatment reduces the susceptibility of the portal hypertensive gastric mucosa to ethanol-induced injury in cirrhotic rats. Eur J Pharmacol. 2008;589:245–250.CrossRefPubMed
24.
go back to reference Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 1968;25:1192–1205.CrossRef Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 1968;25:1192–1205.CrossRef
25.
go back to reference Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978;86:271–278.CrossRefPubMed Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978;86:271–278.CrossRefPubMed
26.
go back to reference Reynell PC, Spray GH. The simultaneous measurement of absorption and transit in the gastrointestinal tract of the rat. J Physiol. 1978;15:361–371. Reynell PC, Spray GH. The simultaneous measurement of absorption and transit in the gastrointestinal tract of the rat. J Physiol. 1978;15:361–371.
27.
go back to reference Farrugia G, Szurszewski JH. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology. 2014;147:303–313.CrossRefPubMedPubMedCentral Farrugia G, Szurszewski JH. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology. 2014;147:303–313.CrossRefPubMedPubMedCentral
28.
go back to reference Pae HO, Lee YC, Jo EK, Chung HT. Subtle interplay of endogenous bioactive gases (NO, CO and H(2)S) in inflammation. Arch Pharm Res. 2009;32:1155–1162.CrossRefPubMed Pae HO, Lee YC, Jo EK, Chung HT. Subtle interplay of endogenous bioactive gases (NO, CO and H(2)S) in inflammation. Arch Pharm Res. 2009;32:1155–1162.CrossRefPubMed
29.
go back to reference King AL, Polhemus DJ, Bhushan S, et al. Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent. Proc Natl Acad Sci USA. 2014;1113:182–187. King AL, Polhemus DJ, Bhushan S, et al. Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent. Proc Natl Acad Sci USA. 2014;1113:182–187.
30.
go back to reference Kondo K, Bhushan S, King AL, et al. H2S protects against pressure overload-induced heart failure via up-regulation of endothelial nitric oxide synthase. Circulation. 2013;127:1116–1127.CrossRefPubMedPubMedCentral Kondo K, Bhushan S, King AL, et al. H2S protects against pressure overload-induced heart failure via up-regulation of endothelial nitric oxide synthase. Circulation. 2013;127:1116–1127.CrossRefPubMedPubMedCentral
31.
go back to reference Al-Magableh MR, Kemp-Harper BK, Ng HH, Miller AA, Hart JL. Hydrogen sulfide protects endothelial nitric oxide function under conditions of acute oxidative stress in vitro. Naunyn Schmiedebergs Arch Pharmacol. 2014;387:67–74.CrossRefPubMed Al-Magableh MR, Kemp-Harper BK, Ng HH, Miller AA, Hart JL. Hydrogen sulfide protects endothelial nitric oxide function under conditions of acute oxidative stress in vitro. Naunyn Schmiedebergs Arch Pharmacol. 2014;387:67–74.CrossRefPubMed
33.
go back to reference Altaany Z, Ju Y, Yang G, Wang R. The coordination of S-sulfhydration, S-nitrosylation, and phosphorylation of endothelial nitric oxide synthase by hydrogen sulfide. Sci Signal. 2014;7:ra87.CrossRefPubMed Altaany Z, Ju Y, Yang G, Wang R. The coordination of S-sulfhydration, S-nitrosylation, and phosphorylation of endothelial nitric oxide synthase by hydrogen sulfide. Sci Signal. 2014;7:ra87.CrossRefPubMed
34.
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;2014:1–7.CrossRef 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;2014:1–7.CrossRef
35.
go back to reference Shi L, Du JB, Pu DF, Qi JG, Tang CS. Regulation of endogenous cystathionine-gamma-lyase gene expression in high pulmonary flow by nitric oxide precursor. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2006;22:343–347.PubMed Shi L, Du JB, Pu DF, Qi JG, Tang CS. Regulation of endogenous cystathionine-gamma-lyase gene expression in high pulmonary flow by nitric oxide precursor. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2006;22:343–347.PubMed
36.
go back to reference Kato S, Kitamura M, Roman P, Takeuchi K, Takeuchi K. Role of nitric oxide in regulation of gastric acid secretion in rats: effects of NO donors and NO synthase inhibitor. Br J Pharmacol. 1998;123:839–846.CrossRefPubMedPubMedCentral Kato S, Kitamura M, Roman P, Takeuchi K, Takeuchi K. Role of nitric oxide in regulation of gastric acid secretion in rats: effects of NO donors and NO synthase inhibitor. Br J Pharmacol. 1998;123:839–846.CrossRefPubMedPubMedCentral
37.
go back to reference Esplugues JV, Barrachina MD, Beltran B, Cala-tayud S, Whittle BJR, Moncada S. Inhibition of gastric acid secretion by stress: a protective reflex mediated by cerebral nitric oxide. Proc Natl Acad Sci. 1996;93:14839–14844.CrossRefPubMedPubMedCentral Esplugues JV, Barrachina MD, Beltran B, Cala-tayud S, Whittle BJR, Moncada S. Inhibition of gastric acid secretion by stress: a protective reflex mediated by cerebral nitric oxide. Proc Natl Acad Sci. 1996;93:14839–14844.CrossRefPubMedPubMedCentral
38.
go back to reference Kitamura M, Sugamoto S, Kawauchi S, Kato S, Takeuchi K. Modulation by endogenous nitric oxide of acid secretion induced by gastric distention in rats: enhancement by nitric oxide synthase inhibitor. J Pharmacol Exp Ther. 1999;291:181–187.PubMed Kitamura M, Sugamoto S, Kawauchi S, Kato S, Takeuchi K. Modulation by endogenous nitric oxide of acid secretion induced by gastric distention in rats: enhancement by nitric oxide synthase inhibitor. J Pharmacol Exp Ther. 1999;291:181–187.PubMed
39.
go back to reference Laine L, Takeuchi K, Tarnawski A. Gastric mucosal defense and cytoprotection: benchto bedside. Gastroenterology. 2008;135:41–60.CrossRefPubMed Laine L, Takeuchi K, Tarnawski A. Gastric mucosal defense and cytoprotection: benchto bedside. Gastroenterology. 2008;135:41–60.CrossRefPubMed
40.
go back to reference Brown JF, Keates AC, Hanson PJ, Whittle BJ. Nitric oxide generators and cGMP stimulate mucus secretion by rat gastric mucosal cells. Am J Physiol. 1993;265:G418–G422.PubMed Brown JF, Keates AC, Hanson PJ, Whittle BJ. Nitric oxide generators and cGMP stimulate mucus secretion by rat gastric mucosal cells. Am J Physiol. 1993;265:G418–G422.PubMed
41.
42.
go back to reference Magierowski M, Jasnos K, Kwiecień S, Brzozowski T. Role of hydrogen sulfide in the physiology of gastrointestinal tract and in the mechanism of gastroprotection. Postepy Hig Med Dosw. 2013;67:150–156.CrossRef Magierowski M, Jasnos K, Kwiecień S, Brzozowski T. Role of hydrogen sulfide in the physiology of gastrointestinal tract and in the mechanism of gastroprotection. Postepy Hig Med Dosw. 2013;67:150–156.CrossRef
43.
go back to reference de Souza GF, Taladriz-Blanco P, Velloso LA, de Oliveira MG. Nitric oxide released from luminal S-nitroso-N-acetylcysteine increases gastric mucosal blood flow. Molecules. 2015;20:4109–4123.CrossRefPubMed de Souza GF, Taladriz-Blanco P, Velloso LA, de Oliveira MG. Nitric oxide released from luminal S-nitroso-N-acetylcysteine increases gastric mucosal blood flow. Molecules. 2015;20:4109–4123.CrossRefPubMed
44.
go back to reference Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322:587–590.CrossRefPubMedPubMedCentral Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322:587–590.CrossRefPubMedPubMedCentral
45.
go back to reference Capettini LSA, Cortes SF, Silva JF, Alvarez-Leite JI, Lemos VS. Decreased production of neuronal NOS-derived hydrogen peroxide contributes to endothelial dysfunction in atherosclerosis. Br J Pharmacol. 2011;164:1738–1748.CrossRefPubMedPubMedCentral Capettini LSA, Cortes SF, Silva JF, Alvarez-Leite JI, Lemos VS. Decreased production of neuronal NOS-derived hydrogen peroxide contributes to endothelial dysfunction in atherosclerosis. Br J Pharmacol. 2011;164:1738–1748.CrossRefPubMedPubMedCentral
46.
go back to reference Minamishima S, Bougaki M, Sips PY, et al. Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation. 2009;120:888–896.CrossRefPubMedPubMedCentral Minamishima S, Bougaki M, Sips PY, et al. Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation. 2009;120:888–896.CrossRefPubMedPubMedCentral
47.
go back to reference Silva RO, Lucetti LT, Wong DV, et al. Alendronate induces gastric damage by reducing nitric oxide synthase expression and NO/cGMP/KATP signaling pathway. Nitric Oxide. 2014;40:22–30.CrossRefPubMed Silva RO, Lucetti LT, Wong DV, et al. Alendronate induces gastric damage by reducing nitric oxide synthase expression and NO/cGMP/KATP signaling pathway. Nitric Oxide. 2014;40:22–30.CrossRefPubMed
48.
go back to reference Nicolau LA, Silva RO, Damasceno SR, et al. The hydrogen sulfide donor, Lawesson’s reagent, prevents alendronate-induced gastric damage in rats. Braz J Med Biol Res. 2013;46:708–714.CrossRefPubMedPubMedCentral Nicolau LA, Silva RO, Damasceno SR, et al. The hydrogen sulfide donor, Lawesson’s reagent, prevents alendronate-induced gastric damage in rats. Braz J Med Biol Res. 2013;46:708–714.CrossRefPubMedPubMedCentral
49.
go back to reference Fiorucci S, Antonelli E, Distrutti E, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology. 2005;129:1210–1224.CrossRefPubMed Fiorucci S, Antonelli E, Distrutti E, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology. 2005;129:1210–1224.CrossRefPubMed
50.
go back to reference Nakagiri A, Sunamoto M, Takeuchi K, Murakami M. Evidence for the involvement of NADPH oxidase in ischemia/reperfusion-induced gastric damage via angiotensin II. J Physiol Pharmacol. 2010;61:171–179.PubMed Nakagiri A, Sunamoto M, Takeuchi K, Murakami M. Evidence for the involvement of NADPH oxidase in ischemia/reperfusion-induced gastric damage via angiotensin II. J Physiol Pharmacol. 2010;61:171–179.PubMed
51.
go back to reference Russo A, Fraser R, Adachi K, Horowitz M, Boeckxstaens G. Evidence that nitric oxide mechanisms regulate small intestinal motility in humans. Gut. 1999;44:72–76.CrossRefPubMedPubMedCentral Russo A, Fraser R, Adachi K, Horowitz M, Boeckxstaens G. Evidence that nitric oxide mechanisms regulate small intestinal motility in humans. Gut. 1999;44:72–76.CrossRefPubMedPubMedCentral
52.
go back to reference Huang X, Meng XM, Liu DH, et al. Different regulatory effects of hydrogen sulfide and nitric oxide on gastric motility in mice. Eur J Pharmacol. 2013;720:276–285.CrossRefPubMed Huang X, Meng XM, Liu DH, et al. Different regulatory effects of hydrogen sulfide and nitric oxide on gastric motility in mice. Eur J Pharmacol. 2013;720:276–285.CrossRefPubMed
53.
go back to reference Sun WM, Doran S, Jones KL, et al. Effects of nitroglycerin on liquid gastric emptying and antropyloroduodenal motility. Am J Physiol. 1998;275:G1173–G1178.PubMed Sun WM, Doran S, Jones KL, et al. Effects of nitroglycerin on liquid gastric emptying and antropyloroduodenal motility. Am J Physiol. 1998;275:G1173–G1178.PubMed
54.
go back to reference Rosalmeida MC, Saraiva LD, da Graça JR, et al. Sildenafil, a phosphodiesterase-5 inhibitor, delays gastric emptying and gastrointestinal transit of liquid in awake rats. Dig Dis Sci. 2003;10:2064–2068.CrossRef Rosalmeida MC, Saraiva LD, da Graça JR, et al. Sildenafil, a phosphodiesterase-5 inhibitor, delays gastric emptying and gastrointestinal transit of liquid in awake rats. Dig Dis Sci. 2003;10:2064–2068.CrossRef
55.
go back to reference Vetri T, Bonvissuto F, Marino A, Postorino A. Nitrergic and purinergic interplay in inhibitory transmission in rat gastric fundus. Auton Autacoid Pharmacol. 2007;27:151–157.CrossRefPubMed Vetri T, Bonvissuto F, Marino A, Postorino A. Nitrergic and purinergic interplay in inhibitory transmission in rat gastric fundus. Auton Autacoid Pharmacol. 2007;27:151–157.CrossRefPubMed
56.
go back to reference Medeiros JV, Bezerra VH, Lucetti LT, et al. Role of KATP channels and TRPV1 receptors in hydrogen sulfide-enhanced gastric emptying of liquid in awake mice. Eur J Pharmacol. 2012;693:57–63.CrossRefPubMed Medeiros JV, Bezerra VH, Lucetti LT, et al. Role of KATP channels and TRPV1 receptors in hydrogen sulfide-enhanced gastric emptying of liquid in awake mice. Eur J Pharmacol. 2012;693:57–63.CrossRefPubMed
Metadata
Title
Nitric Oxide and Hydrogen Sulfide Interact When Modulating Gastric Physiological Functions in Rodents
Authors
Larisse Tavares Lucetti
Renan Oliveira Silva
Ana Paula Macedo Santana
Bruno de Melo Tavares
Mariana Lima Vale
Pedro Marcos Gomes Soares
Francisco José Batista de Lima Júnior
Pedro Jorge Caldas Magalhães
Fernando de Queiroz Cunha
Ronaldo de Albuquerque Ribeiro
Jand-Venes Rolim Medeiros
Marcellus Henrique Loiola Ponte Souza
Publication date
01-01-2017
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 1/2017
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-016-4377-x

Other articles of this Issue 1/2017

Digestive Diseases and Sciences 1/2017 Go to the issue

UNM Clinical Case Conferences

Splenic Rupture Following Colonoscopy

Stanford Multidisciplinary Seminars

Pulmonary Crohn’s Disease

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.