Carbon monoxide in human physiology – its role in the gastrointestinal tract

COMMENTARY ON THE LAW

Carbon monoxide in human physiology – its role in the gastrointestinal tract

Katarzyna Jasnos 1 , Marcin Magierowski 1 , Sławomir Kwiecień 1 , Tomasz Brzozowski 1

1. Katedra Fizjologii Uniwersytet Jagielloński Collegium Medicum, Kraków

Published: 2014-01-30
DOI: 10.5604/17322693.1087527
GICID: 01.3001.0003.1184
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2014; 68 : 101-109

 

Abstract

Carbon monoxide (CO) is produced endogenously in the body as a byproduct of heme degradation catalyzed by the action of heme oxygenase (HO) enzymes. An inducible form, HO-1, responds to many factors such as oxidative stress, hypoxia, heme, bacterial endotoxins, proinflammatory cytokines and heavy metals. HO-2 is constitutively expressed under basal conditions in most human tissues including brain and gonads. Recent data show that CO is a gaseous mediator with multidirectional biological activity. It is involved in maintaining cellular homeostasis and many physiological and pathophysiological processes. CO shares many properties with another established vasodilatator and neurotransmitter – nitric oxide (NO). Both CO and NO are involved in neural transmission, modulation of blood vessel function and inhibition of platelet aggregation. The binding to guanylate cyclase, stimulation of the production of cGMP, activation of Ca2+-dependent potassium channels and stimulation of mitogen-activated protein kinases are well known cellular targets of CO action. Since CO is nowadays a subject of extensive investigation in many centers worldwide, the aim of the present study was to present the role of CO in various aspects of human physiology with special focus on its activity in the gastrointestinal tract.

References

  • 1. Baranano D.E., Rao M., Ferris C.D., Snyder S.H.: Biliverdin reductase:a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. USA,2002; 99: 16093-16098
    Google Scholar
  • 2. Bełtowski J., Jamroz A., Borkowska E.: Oksygenaza hemowa i tlenekwęgla w fizjologii i patologii układu krążenia. Postępy Hig. Med.Dośw., 2004; 58: 83-99
    Google Scholar
  • 3. Chłopicki S., Olszanecki R., Marcinkiewicz E., Lomnicka M., MotterliniR.: Carbon monoxide released by CORM-3 inhibits humanplatelets by a mechanism independent of soluble guanylate cyclase.Cardiovasc. Res., 2006; 71: 393-401
    Google Scholar
  • 4. Coburn R.F., Williams W.I., Kahn S.B.: Endogenous carbon monoxideproduction in patients with hemolytic anemia. J. Clin. Invest.,1966; 45: 460-468
    Google Scholar
  • 5. Dulak J., Józkowicz A.: Carbon monoxide – a “new” gaseous modulatorof gene expression. Acta Biochim. Pol., 2003; 50: 31-47
    Google Scholar
  • 6. Gibbons S.J., Farrugia G.: The role of carbon monoxide in thegastrointestinal tract. J. Physiol., 2004; 556: 325-336
    Google Scholar
  • 7. Gill G.: SUMO and ubiquitin in the nucleus: different functions,similar mechanisms? Genes Dev., 2004; 18: 2046-2059
    Google Scholar
  • 8. Gomes A.S., Gadelha G.G., Lima S.J., Garcia J.A., Medeiros J.V.,Havt A., Lima A.A., Ribeiro R.A., Brito G.A., Cunha F.Q., Souza M.H.:Gastroprotective effect of heme-oxygenase 1/biliverdin/CO pathwayin ethanol-induced gastric damage in mice. Eur. J. Pharmacol.,2010; 642: 140-145
    Google Scholar
  • 9. Grisham M.B.: Oxidants and free radicals in inflammatory boweldisease. Lancet, 1994; 344: 859-861
    Google Scholar
  • 10. Haschemi A., Chin B.Y., Jeitler M., Esterbauer H., Wagner O.,Bilban M., Otterbein L.E.: Carbon monoxide induced PPARγ SUMOylationand UCP2 block inflammatory gene expression in macrophages.PLoS One, 2011; 6: e26376
    Google Scholar
  • 11. Ibrahim I., El-Sayed S., Abdel-Hakim S., Hassan M., Aziz N.: Inhibitionof endogenous CO by ZnPP protects against stress-inducedgastric lesion in adult male albino rats. J. Physiol. Biochem., 2012;68: 319-328
    Google Scholar
  • 12. Jaggar J.H., Li A., Parfenova H., Liu J., Umstot E.S., Dopico A.M.,Leffler C.W.: Heme is a carbon monoxide receptor for large-conductanceCa2+-activated K+ channels. Circ. Res., 2005; 97: 805-812
    Google Scholar
  • 13. Jasnos K., Kwiecień S., Magierowski M., Brzozowski B., ŚliwowskiZ., Mitis-Musioł M., Nawrot E., Pawlik M.W., Konturek S., BrzozowskiT.: Importance of reactive oxygen species in experimental models ofgastric mucosa damage. 21th International Symposium: Molecularand Physiological Aspects of Regulatory Processes of the Organism,Kraków, 14-15.06.2012
    Google Scholar
  • 14. Jasnos K., Magierowski M., Kwiecień S., Brzozowski T., KonturekS.: Reaktywne formy tlenu – znaczenie w patomechanizmie eksperymentalnychuszkodzeń błony śluzowej żołądka. Kongres PolskiegoTowarzystwa Gastroenterologicznego, Kraków, 4-6.10.2012
    Google Scholar
  • 15. Kajimura M., Fukuda R., Bateman R.M., Yamamoto T., SuematsuM.: Interactions of multiple gas-transducing systems: hallmarksand uncertainties of CO, NO, and H2S gas biology. Antioxid. RedoxSignal., 2010; 13: 157-192
    Google Scholar
  • 16. Kashyap P.C., Choi K.M., Dutta N., Linden D.R., Szurszewski J.H.,Gibbons S.J., Farrugia G.: Carbon monoxide reverses diabetic gastroparesisin NOD mice. Am. J. Physiol. Gastrointest. Liver Physiol.,2010; 298: G1013-G1019
    Google Scholar
  • 17. Katada K., Bihari A., Mizuguchi S., Yoshida N., Yoshikawa T., FraserD.D., Potter R.F., Cepinskas G.: Carbon monoxide liberated fromCO-releasing molecule (CORM-2) attenuates ischemia/reperfusion(I/R)-induced inflammation in the small intestine. Inflammation,2010; 33: 92-100
    Google Scholar
  • 18. Kharitonov V.G., Sharma V.S., Pilz R.B., Magde D., Koesling D.:Basis of guanylate cyclase activation by carbon monoxide. Proc. Natl.Acad. Sci. USA, 1995; 92: 2568-2571
    Google Scholar
  • 19. Konturek P.C., Brzozowski T., Walter B., Burnat G., Hess T., Hahn E.G.,Konturek S.J.: Ghrelin-induced gastroprotection against ischemia-reperfusioninjury involves an activation of sensory afferent nerves and hyperemiamediated by nitric oxide. Eur. J. Pharmacol., 2006; 536: 171-181
    Google Scholar
  • 20. Konturek S.J.: Choroba wrzodowa – patofizjologia i leczenie.Przew. Lek., 2001; 4: 98-107
    Google Scholar
  • 21. Konturek S.J., Brzozowski T., Bielanski W., Schally A.V.: Role ofendogenous gastrin in gastroprotection. Eur. J. Pharmacol., 1995;278: 203-212
    Google Scholar
  • 22. Konturek S.J., Pawlik W.W., Brzozowski T., Pawlik M.W., KwiecieńS.: Przemiany reaktywnych form tlenu w doświadczalnym, stresowymmodelu uszkodzeń błony śluzowej żołądka. Gastroenterol.Pol., 2010; 17: 234-243
    Google Scholar
  • 23. Krzyżowska M., Świątek W., Fijałkowska B., Niemiałtowski M.,Schollenberger A.: Rola kinaz MAP w odpowiedzi immunologicznej.Postępy Biol. Kom., 2009; 36: 295-308
    Google Scholar
  • 24. Laine L., Takeuchi K., Tarnawski A.: Gastric mucosal defense andcytoprotection: bench to bedside. Gastroenterology, 2008; 135: 41-60
    Google Scholar
  • 25. Liu D.M., Sun B.W., Sun Z.W., Jin Q., Sun Y., Chen X.: Suppressionof inflammatory cytokine production and oxidative stress by COreleasingmolecules-liberated CO in the small intestine of thermallyinjuredmice. Acta Pharmacol. Sin., 2008; 29: 838-846
    Google Scholar
  • 26. Medeiros C.A., Warren C.A., Freire R., Vieira C.A., Lima B.B., ValeM.L., Ribeiro R.A., Souza M.H., Brito G.A.: Role of the haem oxygenase/carbonmonoxide pathway in Clostridium difficile toxin A-inducedenteritis in mice. J. Med. Microbiol., 2011; 60: 1146-1154
    Google Scholar
  • 27. Motawi T.K., Abd Elgawad H.M., Shahin N.N.: Gastroprotectiveeffect of leptin in indomethacin-induced gastric injury. J. Biomed.Sci., 2008; 15: 405-412
    Google Scholar
  • 28. Motterlini R.: Carbon monoxide-releasing molecules (CO-RMs):vasodilatory, anti-ischaemic and anti-inflammatory activities. Biochem.Soc. Trans., 2007; 35: 1142-1146
    Google Scholar
  • 29. Müller S., Hoege C., Pyrowolakis G., Jentsch S.: SUMO, ubiquitin’smysterious cousin. Nat. Rev. Mol. Cell Biol., 2001; 2: 202-210
    Google Scholar
  • 30. Nakao A., Kaczorowski D.J., Sugimoto R., Billiar T.R., McCurryK.R.: Application of heme oxygenase-1, carbon monoxide and biliverdinfor the prevention of intestinal ischemia/reperfusion injury.J. Clin. Biochem. Nutr., 2008; 42: 78-88
    Google Scholar
  • 31. Nakao A., Kimizuka K., Stolz D.B., Neto J.S., Kaizu T., Choi A.M.,Uchiyama T., Zuckerbraun B.S., Nalesnik M.A., Otterbein L.E., MuraseN.: Carbon monoxide inhalation protects rat intestinal grafts fromischemia/reperfusion injury. Am. J. Pathol., 2003; 163: 1587-1598
    Google Scholar
  • 32. Otterbein L.E., Bach F.H., Alam J., Soares M., Lu H.T., Wysk M.,Davis R.J., Flavell R.A., Choi A.M.: Carbon monoxide has anti-inflammatoryeffects involving the mitogen-activated protein kinasepathway. Nat. Med., 2000; 6: 422-428
    Google Scholar
  • 33. Pouokam E., Steidle J., Diener M.: Regulation of colonic iontransport by gasotransmitters. Biol. Pharm. Bull., 2011; 34: 789-793
    Google Scholar
  • 34. Pourcet B., Staels B., Glineur C.: PPAR SUMOylation: some usefulexperimental tips. Methods Mol. Biol., 2013; 952: 145-161
    Google Scholar
  • 35. Ryter S.W., Alam J., Choi A.M.: Heme oxygenase-1/carbon monoxide:from basic science to therapeutic applications. Physiol. Rev.,2006; 86: 583-650
    Google Scholar
  • 36. Ryter S.W., Choi A.M.: Heme oxygenase-1/carbon monoxidefrom metabolism to molecular therapy. Am. J. Respir. Cell Mol. Biol.,2009; 41: 251-260
    Google Scholar
  • 37. Ryter S.W., Otterbein L.E.: Carbon monoxide in biology and medicine.Bioessays, 2004; 26: 270-280
    Google Scholar
  • 38. Ryter S.W., Otterbein L.E., Morse D., Choi A.M.: Heme oxygenase/carbonmonoxide signaling pathways: Regulation and functionalsignificance. Mol. Cell. Biochem., 2002; 234/235: 249-263
    Google Scholar
  • 39. Schwartz D.C., Hochstrasser M.: A superfamily of protein tags:ubiquitin, SUMO and related modfiers. Trends Biochem. Sci., 2003;28: 321-328
    Google Scholar
  • 40. Schwer C.I., Mutschler M., Stoll P., Goebel U., Humar M., HoetzelA., Schmidt R.: Carbon monoxide releasing molecule-2 inhibitspancreatic stellate cell proliferation by activating p38 mitogen-activatedprotein kinase/heme oxygenase-1 signaling. Mol. Pharmacol.,2010; 77: 660-669
    Google Scholar
  • 41. Sibilia V., Rindi G., Pagani F., Rapetti D., Locatelli V., TorselloA., Campanini N., Deghenghi R., Netti C.: Ghrelin protects againstethanol-induced gastric ulcers in rats: studies on the mechanismsof action. Endocrinology, 2003; 144: 353-359
    Google Scholar
  • 42. Singer I.I., Kawka D.W., Scott S., Weidner J.R., Mumford R.A.,Riehl T.E., Stenson W.F.: Expression of inducible nitric oxide synthaseand nitrotyrosine in colonic epithelium in inflammatory boweldisease. Gastroenterology, 1996; 111: 871-885
    Google Scholar
  • 43. Sjöstrand T.: The formation of carbon monoxide by the decompositionof haemoglobin in vivo. Acta Physiol. Scand., 1952; 26:338-344
    Google Scholar
  • 44. Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., Ames B.N.:Bilirubin is an antioxidant of possible physiological importance.Science, 1987; 235: 1043-1046
    Google Scholar
  • 45. Takasuka H., Hayashi S., Koyama M., Yasuda M., Aihara E., AmagaseK., Takeuchi K.: Carbon monoxide involved in modulating HCO3–secretion in rat duodenum. J. Pharmacol. Exp. Ther., 2011; 337:293-300
    Google Scholar
  • 46. Thorup C., Jones C.L., Gross S.S., Moore L.C., Goligorsky M.S.:Carbon monoxide induces vasodilation and nitric oxide release butsuppresses endothelial NOS. Am. J. Physiol., 1999; 277: F882-F889
    Google Scholar
  • 47. Vreman H.J., Wong R.J., Stevenson D.K.: Carbon monoxide inbreath, blood, and other tissues. W: Carbon Monoxide Toxicity, red.Penney D.G., Boca Raton, FL: CRC, 2000: 19-60
    Google Scholar
  • 48. Wang R., Wu L.: Interaction of selective amino acid residuesof KCa channels with carbon monoxide. Exp. Biol. Med., 2003; 228:474-480
    Google Scholar
  • 49. Wang W.P., Guo X., Koo M.W., Wong B.C., Lam S.K., Ye Y.N., ChoC.H.: Protective role of heme oxygenase-1 on trinitrobenzene sulfonicacid-induced colitis in rats. Am. J. Physiol. Gastrointest. LiverPhysiol., 2001; 281: G586-G594
    Google Scholar
  • 50. Wei Y., Chen P., de Bruyn M., Zhang W., Bremer E., Helfrich W.:Carbon monoxide-releasing molecule-2 (CORM-2) attenuates acutehepatic ischemia reperfusion injury in rats. BMC Gastroenterol.,2010; 10: 42
    Google Scholar
  • 51. Wu L., Cao K., Lu Y., Wang R.: Different mechanisms underlyingthe stimulation of K(Ca) channels by nitric oxide and carbon monoxide.J. Clin. Invest., 2002; 110: 691-700
    Google Scholar
  • 52. Wu L., Wang R.: Carbon monoxide: endogenous production, physiologicalfunctions, and pharmacological applications. Pharmacol.Rev., 2005; 57: 585-630
    Google Scholar
  • 53. Xue L., Farrugia G., Miller S.M., Ferris C.D., Snyder S.H., SzurszewskiJ.H.: Carbon monoxide and nitric oxide as coneurotransmittersin the enteric nervous system: evidence from genomicdeletion of biosynthetic enzymes. Proc. Natl. Acad. Sci. USA, 2000;97: 1851-1855
    Google Scholar

Full text

Skip to content