Gaseous mediators (H2S, NO and CO) a new approach in gastrointestinal protection
Abstract
Gastrointestinal damage is generated by a wide range of harmful agents, and is the result of the activation of inflammatory, oxidant and cytotoxic mechanisms, that together overwhelm the “mucosa defense” of the gastrointestinal (GI) tract. It is currently known that the mechanisms by which gastric damage is generated are slightly different from those that generate intestinal damage. The treatments available on the market such as citoprotectors, the use of selective Ciclooxigenase 2 (COX-2) inhibitors, the co-prescription of acid suppressive agents and the use of prostaglandin analogues are mainly focused on the mechanisms of gastric damage, and their use has begun to be limited due to its adverse effects at intestinal and cardiovascular level. Due to its multifactorial origin, the prevention and treatment of GI damage requires effective therapies that can protect both gastric and intestinal level modulating more than one mechanism. Recently, has been reported the contribution of gaseous mediators nitric oxide (NO), hydrogen sulfide (H2S) and carbon monoxide (CO) in many physiological processes in the gastrointestinal tract, including the maintenance of GI mucosal barrier integrity. Experimental evidence has shown promising results regarding the gastric safety of these gasotransmitters, especially those coupled to NSAIDs. This review will try to give a general overview of the mechanisms of gastric and intestinal damage, their main differences, the existing therapies for their treatment and the information available on gas transmitters with a brief description of roles of each of these gaseous molecules.
Downloads
References
Sulaieva O, Wallace JL. Gaseous mediator-based anti-inflammatory drugs. Curr. Opin. Pharmacol. 2015; 25:1–6.
Verbeure W, van Goor H, Mori H, van Beek AP, Tack J, van Dijk PR. The Role of Gasotransmitters in Gut Peptide Actions. Front. Pharmacol. 2021; 12:720703.
Dunlap JJ, Patterson S. Peptic Ulcer Disease. Gastroenterology Nurs. 2019; 42(5):451–454.
Konturek SJ, Konturek PC, Plonka A, Duda A, Sito E, Zuchowicz M, et al. Implication of gastrin in cyclooxygenase-2 expression in Helicobacter pylori infected gastric ulceration. Prostaglandins Other Lipid Mediat. 2001; 66(1):39-51.
Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE. Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol. Rev. 2014; 94(2):329–54.
Wallace JL. Pathogenesis of NSAID-induced gastroduodenal mucosal injury. Best. Pract. Res. Clin. Gastroenterol. 2001; 15(5):691-703.
Wallace JL. Eicosanoids in the gastrointestinal tract. Br. J. Pharmacol. 2019; 176(8):1000-1008.
Becker JC, Domschke W, Pohle T. Current approaches to prevent NSAID-induced gastropathy--COX selectivity and beyond. Br. J. Clin. Pharmacol. 2004; 58(6):587-600.
Cavallini ME, Andreollo NA, Metze K, Araújo MR. Omeprazole and misoprostol for preventing gastric mucosa effects caused by indomethacin and celecoxib in rats. Acta Cir. Bras. 2006; 21(3):168-76.
Wallace, J.L. Prevention of NSAID-Enteropathy: A Soluble Problem? Dig. Dis. Sci. 2016; 61: 1–3.
Wallace JL, Motta JP, Buret AG. Hydrogen sulfide: an agent of stability at the microbiome-mucosa interface. Am. J. Physiol. Gastrointest. Liver Physiol. 2018; 314(2): G143-G149.
Bi WP, Man HB, Man MQ. Efficacy and safety of herbal medicines in treating gastric ulcer: a review. World J. Gastroenterol. 2014; 20(45):17020-8.
Bindu S, Mazumder S, Bandyopadhyay U. Non-steroidal anti-inflammatory drugs (NSAIDs) and organ damage: A current perspective. Biochem. Pharmacology. 2020; 180:114147.
Bindu S, Mazumder S, Dey S, Pal C, Goyal M, Alam A, et al. Nonsteroidal anti-inflammatory drug induces proinflammatory damage in gastric mucosa through NF-κB activation and neutrophil infiltration: anti-inflammatory role of heme oxygenase-1 against nonsteroidal anti-inflammatory drug. Free Radic. Biol. Med. 2013; 65:456-467.
Bi WP, Man HB, Man MQ. Efficacy and safety of herbal medicines in treating gastric ulcer: a review. World J. Gastroenterol. 2014; 20(45):17020-8.
Mishra AP, Bajpai A, Chandra S. A Comprehensive Review on the Screening Models for the Pharmacological Assessment of Antiulcer Drugs. Curr. Clin. Pharmacol. 2019; 14(3):175-196.
Boelsterli UA, Ramirez-Alcantara V. NSAID Acyl Glucuronides and Enteropathy. Curr. Drug. Metab. 2011; 12(3):245-52.
LoGuidice A, Ramirez-Alcantara V, Proli A, Gavillet B, Boelsterli UA. Pharmacologic targeting or genetic deletion of mitochondrial cyclophilin D protects from NSAID-induced small intestinal ulceration in mice. Toxicol Sci. 2010; 118(1):276-85.
Boelsterli UA, Redinbo MR, Saitta KS. Multiple NSAID-induced hits injure the small intestine: underlying mechanisms and novel strategies. Toxicol Sci. 2013; 131(2):654-67.
Laine L, Takeuchi K, Tarnawski A. Gastric mucosal defense and cytoprotection: bench to bedside. Gastroenterology. 2008; 135(1):41-60.
Naito Y, Uchiyama K, Takagi T. Redox-related gaseous mediators in the gastrointestinal tract. J. Clin. Biochem. Nutr. 2018; 63(1):1-4.
Somasundaram S, Sigthorsson G, Simpson RJ, Watts J, Jacob M, Tavares IA, et al. Uncoupling of intestinal mitochondrial oxidative phosphorylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat. Aliment. Pharmacol. Ther. 2000; 14(5):639-50.
Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr. Biol. 2014; 24(10): R453-62.
Velázquez-Moyado JA, Martínez-González A, Linares E, Bye R, Mata R, Navarrete A. Gastroprotective effect of diligustilide isolated from roots of Ligusticum porteri coulter & rose (Apiaceae) on ethanol-induced lesions in rats. J. Ethnopharmacol. 2015; 174:403-9.
Matsui H, Shimokawa O, Kaneko T, Nagano Y, Rai K, Hyodo I. The pathophysiology of non-steroidal anti-inflammatory drug (NSAID)-induced mucosal injuries in stomach and small intestine. J. Clin. Biochem. Nutr. 2011; 48(2):107-11.
Wallace JL, Ma L. Inflammatory mediators in gastrointestinal defense and injury. Exp. Biol. Med. 2001; 226(11):1003-15.
Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn’t the stomach digest itself? Physiol. Rev. 2008; 88(4):1547-65.
Monteiro AP, Pinheiro CS, Luna-Gomes T, Alves LR, Maya-Monteiro CM, Porto BN, et al. Leukotriene B4 mediates neutrophil migration induced by heme. J. Immunol. 2011; 186(11):6562-7.
Stanley D, Kim Y. Prostaglandins and Other Eicosanoids in Insects: Biosynthesis and Biological Actions. Front. Physiol. 2019; 9:1927.
Xiao A, Wang H, Lu X, Zhu J, Huang D, Xu T, et al. H2S, a novel gasotransmitter, involves in gastric accommodation. Sci. Rep. 2015; 5:16086.
Takeuchi K, Tanaka A, Kato S, Amagase K, Satoh H. Roles of COX inhibition in pathogenesis of NSAID-induced small intestinal damage. Clin. Chim. Acta. 2010; 411(7-8):459-66.
Danielak A, Wallace JL, Brzozowski T, Magierowski M. Gaseous Mediators as a Key Molecular Targets for the Development of Gastrointestinal-Safe Anti-Inflammatory Pharmacology. Front. Pharmacol. 2021; 12:657457.
Tai FWD, McAlindon ME. NSAIDs and the small bowel. Curr. Opin. Gastroenterol. 2018; 34(3):175-182.
Takeuchi K, Kato S, Amagase K. Prostaglandin EP receptors involved in modulating gastrointestinal mucosal integrity. J. Pharmacol. Sci. 2010; 114(3):248-61.
Wallace JL. NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br. J. Pharmacol. 2012; 165(1):67-74.
LoGuidice A, Wallace BD, Bendel L, Redinbo MR, Boelsterli UA. Pharmacologic targeting of bacterial β-glucuronidase alleviates nonsteroidal anti-inflammatory drug-induced enteropathy in mice. J. Pharmacol. Exp. Ther. 2012; 341(2):447-54.
Wallace JL, Syer S, Denou E, de Palma G, Vong L, McKnight W, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011; 141(4):1314-22, 1322.e1-5.
Lanas A, Chan FKL. Peptic ulcer disease. Lancet. 2017; 390(10094):613-624.
Lazzaroni M, Sainaghi M, Bianchi Porro G. Non-steroidal anti-inflammatory drug gastropathy: clinical results with antacids and sucralfate. Ital. J. Gastroenterol. Hepatol. 1999; 31 Suppl 1: S48-53.
Kirch W, Hoensch H, Janisch HD. Interactions and non-interactions with ranitidine. Clin. Pharmacokinet. 1984; 9(6):493-510.
Wagner JA, Colombo JM. Medicine and Media: The Ranitidine Debate. Clin. Transl. Sci. 2020;13(4):649-651.
Strauss DG, Florian J, Keire D. Risk of N-Nitrosodimethylamine (NMDA) formation with Ranitidine. JAMA. 2021; 326(20):2077.
Syer SD, Wallace JL. Environmental and NSAID-enteropathy: dysbiosis as a common factor. Curr. Gastroenterol. Rep. 2014; 16(3):377.
Abed MN, Alassaf FA, Jasim MHM, Alfahad M, Qazzaz ME. Comparison of Antioxidant Effects of the Proton Pump-Inhibiting Drugs Omeprazole, Esomeprazole, Lansoprazole, Pantoprazole, and Rabeprazole. Pharmacology. 2020; 105(11-12):645-651.
Fujimori S, Gudis K, Takahashi Y, Seo T, Yamada Y, Ehara A, et al. Distribution of small intestinal mucosal injuries as a result of NSAID administration. Eur. J. Clin. Invest. 2010; 40(6):504-10.
Hagiwara M, Kataoka K, Arimochi H, Kuwahara T, Ohnishi Y. Role of unbalanced growth of gram-negative bacteria in ileal ulcer formation in rats treated with a nonsteroidal anti-inflammatory drug. J. Med. Invest. 2004; 51(1-2):43-51.
Thomson AB, Sauve MD, Kassam N, Kamitakahara H. Safety of the long-term use of proton pump inhibitors. World J. Gastroenterol. 2010; 16(19):2323-30.
Fontecha-Barriuso M, Martín-Sanchez D, Martinez-Moreno JM, Cardenas-Villacres D, Carrasco S, Sanchez-Niño MD, et al. Molecular pathways driving omeprazole nephrotoxicity. Redox. Biol. 2020; 32:101464.
Watson DJ, Harper SE, Zhao PL, Quan H, Bolognese JA, Simon TJ. Gastrointestinal tolerability of the selective cyclooxygenase-2 (COX-2) inhibitor rofecoxib compared with nonselective COX-1 and COX-2 inhibitors in osteoarthritis. Arch. Intern. Med. 2000; 160(19):2998-3003.
Süleyman H, Demircan B, Karagöz Y. Anti-inflammatory and side effects of cyclooxygenase inhibitors. Pharmacol. Rep. 2007; 59(3):247-58.
García Rodríguez LA, Barreales Tolosa L. Risk of upper gastrointestinal complications among users of traditional NSAIDs and COXIBs in the general population. Gastroenterology. 2007; 132(2):498-506.
Magierowski M, Magierowska K, Kwiecien S, Brzozowski T. Gaseous mediators nitric oxide and hydrogen sulfide in the mechanism of gastrointestinal integrity, protection and ulcer healing. Molecules. 2015; 20(5):9099-123.
Whittle BJ. Nitric oxide-modulating agents for gastrointestinal disorders. Expert Opin. Investig. Drugs. 2005;14(11):1347-58.
Shah V, Lyford G, Gores G, Farrugia G. Nitric oxide in gastrointestinal health and disease. Gastroenterology. 2004; 126(3):903-13.
Stanek A, Gadowska-Cicha A, Gawron K, Wielkoszynski T, Adamek B, Cieslar G, et al. Role of nitric oxide in physiology and pathology of the gastrointestinal tract. Mini. Rev. Med. Chem. 2008; 8(14):1549-60.
Sanders KM, Ward SM. Nitric oxide and its role as a non-adrenergic, non-cholinergic inhibitory neurotransmitter in the gastrointestinal tract. Br. J. Pharmacol. 2019; 176(2):212-227.
Fiorucci S, Antonelli E, Burgaud JL, Morelli A. Nitric oxide-releasing NSAIDs: a review of their current status. Drug Saf. 2001; 24(11):801-11.
Fiorucci S, Santucci L, Cirino G, Mencarelli A, Familiari L, Soldato P del, et al. IL-1 beta converting enzyme is a target for nitric oxide-releasing aspirin: new insights in the antiinflammatory mechanism of nitric oxide-releasing nonsteroidal antiinflammatory drugs. J. Immunol. 2000; 165(9):5245-54.
Takeuchi K, Mizoguchi H, Araki H, Komoike Y, Suzuki K. Lack of gastric toxicity of nitric oxide-releasing indomethacin, NCX-530, in experimental animals. Dig. Dis. Sci. 2001; 46(8):1805-18.
Tashima K, Fujita A, Umeda M, Takeuchi K. Lack of gastric toxicity of nitric oxide-releasing aspirin, NCX-4016, in the stomach of diabetic rats. Life Sci. 2000; 67(13):1639-52.
Fiorucci S, Santucci L, Antonelli E, Distrutti E, Del Sero G, Morelli O, Romani L, Federici B, Del Soldato P, Morelli A. NO-aspirin protects from T cell-mediated liver injury by inhibiting caspase-dependent processing of Th1-like cytokines. Gastroenterology. 2000; 118(2):404-21.
Magierowski M, Magierowska K, Kwiecien S, Brzozowski T. Gaseous mediators nitric oxide and hydrogen sulfide in the mechanism of gastrointestinal integrity, protection and ulcer healing. Molecules. 2015; 20(5):9099-123.
Mu K, Yu S, Kitts DD. The Role of Nitric Oxide in Regulating Intestinal Redox Status and Intestinal Epithelial Cell Functionality. Int. J. Mol. Sci. 2019; 20(7):1755.
Takeuchi K, Ukawa H, Konaka A, Kitamura M, Sugawa Y. Effect of nitric oxide-releasing aspirin derivative on gastric functional and ulcerogenic responses in rats: comparison with plain aspirin. J. Pharmacol. Exp. Ther. 1998; 286(1):115-21.
Wallace JL, Reuter B, Cicala C, McKnight W, Grisham MB, Cirino G. Novel nonsteroidal anti-inflammatory drug derivatives with markedly reduced ulcerogenic properties in the rat. Gastroenterology. 1994; 107(1):173-9.
Wallace JL, Del Soldato P. The therapeutic potential of NO-NSAIDs. Fundam. Clin. Pharmacol. 2003; 17(1):11-20.
Wallace JL. Nitric oxide in the gastrointestinal tract: opportunities for drug development. Br. J. Pharmacol. 2019; 176(2):147-154.
Gresele P, Migliacci R, Arosio E, Bonizzoni E, Minuz P, Violi F; NCX 4016-X-208 Study Group. Effect on walking distance and atherosclerosis progression of a nitric oxide-donating agent in intermittent claudication. J. Vasc. Surg. 2012; 56(6):1622-8, 1628.e1-5.
Gresele P, Migliacci R, Procacci A, De Monte P, Bonizzoni E. Prevention by NCX 4016, a nitric oxide-donating aspirin, but not by aspirin, of the acute endothelial dysfunction induced by exercise in patients with intermittent claudication. Thromb. Haemost. 2007; 97(3):444-50.
Pereira-Leite C, Nunes C, Jamal SK, Cuccovia IM, Reis S. Nonsteroidal Anti-Inflammatory Therapy: A Journey Toward Safety. Med. Res. Rev. 2017; 37(4):802-859.
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; 67:150-6.
Kimura H. Hydrogen sulfide: its production, release and functions. Amino Acids. 2011; 41(1):113-21.
Huang CW, Moore PK. H2S Synthesizing Enzymes: Biochemistry and Molecular Aspects. Handb. Exp. Pharmacol. 2015; 230:3-25.
Chan MV, Wallace JL. Hydrogen sulfide-based therapeutics and gastrointestinal diseases: translating physiology to treatments. Am. J. Physiol. Gastrointest. Liver Physiol. 2013; 305(7):G467-73.
Caliendo G, Cirino G, Santagada V, Wallace JL. Synthesis and biological effects of hydrogen sulfide (H2S): development of H2S-releasing drugs as pharmaceuticals. J. Med. Chem. 2010; 53(17):6275-86.
Blachier F, Beaumont M, Kim E. Cysteine-derived hydrogen sulfide and gut health: a matter of endogenous or bacterial origin. Curr. Opin. Clin. Nutr. Metab. Care. 2019; 22(1):68-75.
Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, Bouillaud F. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim. Biophys. Acta. 2010; 1797(8):1500-11.
Mimoun S, Andriamihaja M, Chaumontet C, Atanasiu C, Benamouzig R, Blouin JM, et al. Detoxification of H 2 S by Differentiated Colonic Epithelial Cells: Implication of the Sulfide Oxidizing Unit and of the Cell Respiratory Capacity. Antioxid. Redox Signal. 2012; 17(1):1-10.
Blachier F, Beaumont M, Kim E. Cysteine-derived hydrogen sulfide and gut health: a matter of endogenous or bacterial origin. Curr. Opin. Clin. Nutr. Metab. Care. 2019; 22(1):68-75.
Gemici B, Elsheikh W, Feitosa KB, Costa SK, Muscara MN, Wallace JL. H2S-releasing drugs: anti-inflammatory, cytoprotective and chemopreventative potential. Nitric Oxide. 2015; 46:25-31.
Gallego D, Clavé P, Donovan J, Rahmati R, Grundy D, Jiménez M, Beyak MJ. The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol. Motil. 2008; 20(12):1306-16.
Medeiros JVR, Bezerra VH, Lucetti LT, Lima-Júnior RCP, Barbosa ALR, Tavares BM, 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(1-3):57-63.
Pichette J, Gagnon J. Implications of Hydrogen Sulfide in Glucose Regulation: How H2S Can Alter Glucose Homeostasis through Metabolic Hormones. Oxid. Med. Cell. Longev. 2016; 2016:3285074.
Bełtowski J, Wójcicka G, Jamroz-Wiśniewska A. Hydrogen sulfide in the regulation of insulin secretion and insulin sensitivity: Implications for the pathogenesis and treatment of diabetes mellitus. Biochem. Pharmacol. 2018; 149:60-76.
Fiorucci S, Antonelli E, Distrutti E, Rizzo G, Mencarelli A, Orlandi S, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology. 2005; 129(4):1210-24.
Wallace JL. Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid. Redox Signal. 2010; 12(9):1125-33.
Lou LX, Geng B, Du JB, Tang CS. Hydrogen sulphide-induced hypothermia attenuates stress-related ulceration in rats. Clin. Exp. Pharmacol. Physiol. 2008; 35(2):223-8.
Magierowski M, Magierowska K, Hubalewska-Mazgaj M, Surmiak M, Sliwowski Z, Wierdak M, et al. Cross-talk between hydrogen sulfide and carbon monoxide in the mechanism of experimental gastric ulcers healing, regulation of gastric blood flow and accompanying inflammation. Biochem. Pharmacol. 2018; 149:131-142.
de Araújo S, Oliveira AP, Sousa FBM, Souza LKM, Pacheco G, Filgueiras MC, et al. AMPK activation promotes gastroprotection through mutual interaction with the gaseous mediators H2S, NO, and CO. Nitric Oxide. 2018; 78:60-71.
Magierowski M, Magierowska K, Szmyd J, Surmiak M, Sliwowski Z, Kwiecien S, et al. Hydrogen Sulfide and Carbon Monoxide Protect Gastric Mucosa Compromised by Mild Stress Against Alendronate Injury. Dig. Dis. Sci. 2016; 61(11):3176-3189.
Wallace JL. Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid. Redox Signal. 2010;12(9):1125-33.
Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, et al. Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br. J. Pharmacol. 2007; 150(8):996-1002.
Wallace JL, Vong L, McKnight W, Dicay M, Martin GR. Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology. 2009; 137(2):569-78, 578.e1.
Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat. Rev. Drug. Discov. 2015; 14(5):329-45.
Wallace JL, Caliendo G, Santagada V, Cirino G, Fiorucci S. Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat. Gastroenterology. 2007; 132(1):261-71.
Gugliandolo E, Fusco R, D’Amico R, Militi A, Oteri G, Wallace JL, et al. Anti-inflammatory effect of ATB-352, a H2S -releasing ketoprofen derivative, on lipopolysaccharide-induced periodontitis in rats. Pharmacol. Res. 2018; 132:220-231.
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(6):1236-46.
Wallace JL, Vaughan D, Dicay M, MacNaughton WK, de Nucci G. Hydrogen Sulfide-Releasing Therapeutics: Translation to the Clinic. Antioxid. Redox Signal. 2018; 28(16):1533-1540.
Wallace JL, Nagy P, Feener TD, Allain T, Ditrói T, Vaughan DJ, Muscara MN, de Nucci G, Buret AG. A proof-of-concept, Phase 2 clinical trial of the gastrointestinal safety of a hydrogen sulfide-releasing anti-inflammatory drug. Br. J. Pharmacol. 2020; 177(4):769-777.
Wallace JL, Ianaro A, de Nucci G. Gaseous Mediators in Gastrointestinal Mucosal Defense and Injury. Dig. Dis. Sci. 2017; 62(9):2223-2230.
Wallace JL, Ianaro A, Flannigan KL, Cirino G. Gaseous mediators in resolution of inflammation. Semin. Immunol. 2015; 27(3):227-33.
Costa NRD, Silva RO, Nicolau LAD, Lucetti LT, Santana APM, Aragão KS, 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(1-3):51-9.
Magierowski M, Magierowska K, Hubalewska-Mazgaj M, Adamski J, Bakalarz D, Sliwowski Z, 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.
Takasuka H, Hayashi S, Koyama M, Yasuda M, Aihara E, Amagase K, et al. Carbon monoxide involved in modulating HCO3- secretion in rat duodenum. J. Pharmacol. Exp. Ther. 2011; 337(1):293-300.
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(2):656-62.
Megías 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(8):977-86.
Mancuso C, Preziosi P, Grossman AB, Navarra P. The role of carbon monoxide in the regulation of neuroendocrine function. Neuroimmunomodulation. 1997; 4(5-6):225-9.
Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol. Rev. 2005; 57(4):585-630.
Moustafa A, Habara Y. A novel role for carbon monoxide as a potent regulator of intracellular Ca2+ and nitric oxide in rat pancreatic acinar cells. Am. J. Physiol. Cell. Physiol. 2014; 307(11):C1039-49.
Magierowska K, Magierowski M, Surmiak M, Adamski J, Mazur-Bialy A, Pajdo R, et al. The Protective Role of Carbon Monoxide (CO) Produced by Heme Oxygenases and Derived from the CO-Releasing Molecule CORM-2 in the Pathogenesis of Stress-Induced Gastric Lesions: Evidence for Non-Involvement of Nitric Oxide (NO). Int. J. Mol. Sci. 2016; 17(4):442.
Takagi T, Naito Y, Uchiyama K, Mizuhima K, Suzuki T, Horie R, et al. Carbon monoxide promotes gastric wound healing in mice via the protein kinase C pathway. Free. Radic. Res. 2016; 50(10):1098-1105.
Magierowski M, Magierowska K, Hubalewska-Mazgaj M, Sliwowski Z, Ginter G, Pajdo R, et al. Carbon monoxide released from its pharmacological donor, tricarbonyldichlororuthenium (II) dimer, accelerates the healing of pre-existing gastric ulcers. Br. J. Pharmacol. 2017; 174(20):3654-3668.
Magierowska K, Brzozowski T, Magierowski M. Emerging role of carbon monoxide in regulation of cellular pathways and in the maintenance of gastric mucosal integrity. Pharmacol. Res. 2018; 129:56-64.
Steiger C, Uchiyama K, Takagi T, Mizushima K, Higashimura Y, Gutmann M, et al. Prevention of colitis by controlled oral drug delivery of carbon monoxide. J. Control. Release. 2016; 239:128-36.
Foresti R, Hammad J, Clark JE, Johnson TR, Mann BE, Friebe A, et al. Vasoactive properties of CORM-3, a novel water-soluble carbon monoxide-releasing molecule. Br. J. Pharmacol. 2004; 142(3):453-60.
Copyright (c) 2023 Elizabeth Arlen Pineda-Peña, Aracely Evangelina Chávez-Piña
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
