Nitroso-oxidative stress after activation of 5-HT4 receptors under conditions of colitis in rats

Nataliya Denysenko; Vitaliy Yemelyanenko; Iryna Fomenko; Alexander Sklyarov

doi:10.2478/cipms-2019-0011

Abstract

Serotonin (5-hydroxytryptamine, 5-HT) plays an important role in the regulation of the functioning of the gastrointestinal tract, including that of the colon. The response of smooth muscles, blood vessels and colon mucosa (CM) to 5-HT is realized through the activation of various types of 5-HT receptors, in particular, 5-HT₄ receptors, since the latter are identified on colon cells membranes (enterocytes, smooth muscles and endothelium). The aim of our study was to determine the effect of 5-НT₄ receptors agonist (mosapride) on nitrogen (II) oxide production and lipid peroxidation in CM and colon muscle tissue (CMT) under the conditions of experimental ulcerative colitis (UC).

References

1. Takagi T, Naito Y, Yoshikawa T. Free radicals in inflammatory bowel disease. Free Radical Biology in Digestive Diseases. Front Gastrointest Res. Basel, Karger. 2011;29:128-36.10.1159/000319981
Search in Google Scholar Back to article
2. Kolios G, Valatas V, Ward SG. Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle. Immunology. 2004;113(4):427-37.10.1111/j.1365-2567.2004.01984.x
Search in Google Scholar Back to article
3. Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J. 2012;33(7):829-37.10.1093/eurheartj/ehr304
Search in Google Scholar Back to article
4. Kruidenier L, Kuiper I, Lamers CB, Verspaget HW. Intestinal oxidative damage in inflammatory bowel disease: semiquantification, localization, and association with mucosal antioxidants. J Pathol. 2003;201(1):28-36.10.1002/path.1409
Search in Google Scholar Back to article
5. Garud S., Peppercorn MA. Ulcerative colitis: current treatment strategy and future prospects. Therap Adv Gastroenterol. 2009;2(2): 99-108.10.1177/1756283X09102329
Search in Google Scholar Back to article
6. Savenkova ML, Mueller DM, Heinecke JW. Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J Biol Chem. 1994; 269(32):20394-400.10.1016/S0021-9258(17)32005-7
Search in Google Scholar Back to article
7. De Ponti F. Pharmacology of serotonin: what a clinician should know. Gut. 2004;53(10):1520-35.10.1136/gut.2003.035568177422715361507
Search in Google Scholar Back to article
8. El-Merahbi R, Loffler M, Mayer A, Sumara G. The roles of peripheral serotonin in metabolic homeostasis. FEBS Lett. 2015;589(15):1728-34.10.1016/j.febslet.2015.05.05426070423
Search in Google Scholar Back to article
9. Schimmack S, Svejda B, Lawrence B, Kidd M, Modlin I. The diversity and commonalities of gastroenteropancreatic neuroendocrine tumors. Langenbeck’s Arch Surg. 2011;396:273-98.10.1007/s00423-011-0739-121274559
Search in Google Scholar Back to article
10. Manocha M, Khan WI. Serotonin and GI disorders: an update on clinical and experimental studies. Clin Transl Gastroenterol. 2012;3(4):e13.10.1038/ctg.2012.8336567723238212
Search in Google Scholar Back to article
11. Magro F, Vieira-Coelho MA, Fraga S, Serrao MP, Veloso FT, Ribeiro T et al. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci. 2002;47(1):216-24.10.1023/A:1013256629600
Search in Google Scholar Back to article
12. Faure C, Patey N, Gauthier C, Brooks EM, Mawe GM. Serotonin signaling is altered in irritable bowel syndrome with diarrhea but not in functional dyspepsia in pediatric age patients. Gastroenterol. 2010;139(1):249-58.10.1053/j.gastro.2010.03.032290261420303355
Search in Google Scholar Back to article
13. Coleman NS, Foley S, Dunlop SP, Wheatcroft J, Blackshaw E, Perkins AC et al. Abnormalities of serotonin metabolism and their relation to symptoms in untreated celiac disease. Clin Gastroenterol Hepatol. 2006;4(7):874-81.10.1016/j.cgh.2006.04.01716797248
Search in Google Scholar Back to article
14. Ataee R, Ajdary S, Zarrindast M, Rezayat M, Hayatbakhsh MR. Anti-mitogenic and apoptotic effects of 5-HT1B receptor antagonist on HT29 colorectal cancer cell line. J Cancer Res Clin Oncol. 2010; 136(10):1461-9.10.1007/s00432-010-0801-320306273
Search in Google Scholar Back to article
15. Coogan PF, Strom BL, Rosenberg L. Antidepressant use and colorectal cancer risk. Pharmacoepidemiol Drug Saf. 2009;18(11): 1111-4.10.1002/pds.1808278329019623565
Search in Google Scholar Back to article
16. Costedio MM, Coates MD, Danielson AB, Buttolph TR 3^rd, Blaszyk HJ, Mawe GM, et al. Serotonin signaling in diverticular disease. J Gastrointest Surg. 2008;12(8):1439-45.10.1007/s11605-008-0536-5291090518491196
Search in Google Scholar Back to article
17. Terry N, Margolis GK. Serotonergic mechanisms regulating the GI tract: experimental evidence and therapeutic relevance. Handb Exp Pharmacol. 2017;239:319-42.10.1007/164_2016_103552621628035530
Search in Google Scholar Back to article
18. Mawe1 GM, Hoffman JM. Serotonin signaling in the gastrointestinal tract: functions, dysfunctions, and therapeutic targets. Nat Rev Gastroenterol Hepatol. 2013;10(8):473-86.10.1038/nrgastro.2013.105404892323797870
Search in Google Scholar Back to article
19. Cloez-Tayarani I, Changeux JP. Nicotine and serotonin in immune regulation and inflammatory processes: a perspective. J Leukoc Biol. 2007;81(3):599-606.10.1189/jlb.090654417108054
Search in Google Scholar Back to article
20. Kushnir-Sukhov NM, Brown JM, Wu Y, Kirshenbaum A, Metcalfe DD. Human mast cells are capable of serotonin synthesis and release. J Allergy Clin Immunol. 2007;119(2):498-9.10.1016/j.jaci.2006.09.00317291861
Search in Google Scholar Back to article
21. Nakamura K, Sato T, Ohashi A, Tsurui H, Hasegawa H. Role of a serotonin precursor in development of gut microvilli. Am J Pathol. 2008;172(2):333-4.10.2353/ajpath.2008.070358231235518202184
Search in Google Scholar Back to article
22. O’Connell PJ, Wang X, Leon-Ponte M, Griffiths C, Pingle SC, Ahern GP. A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells. Blood. 2016;107(3):1010-7.10.1182/blood-2005-07-2903
Search in Google Scholar Back to article
23. Bassotti G, Antonelli E, Villanacci V, Baldoni M, Dore MP. Colonic motility in ulcerative colitis. United European Gastroenterol J. 2014; 2(6):457-62.10.1177/2050640614548096
Search in Google Scholar Back to article
24. Spohn SN, Bianco F, Scott RB, Keenan CM, Linton AA, O’Neill CH et al. Protective actions of epithelial 5-hydroxytryptamine 4 receptors in normal and inflamed colon. Gastroenterology. 2016;151(5):933-44.10.1053/j.gastro.2016.07.032
Search in Google Scholar Back to article
25. Hoffman JM, Tyler K, Maceachern SJ, Balemba OB, Johnson AC, Brooks EM et al. Activation of colonic mucosal 5-HT4 receptors accelerates propulsive motility and inhibits visceral hypersensitivity. Gastroenterology. 2012;142(4):844-54.10.1053/j.gastro.2011.12.041
Search in Google Scholar Back to article
26. Kim HS. 5-hydroxytryptamine 4 receptor agonists and colonic motility. J Smooth Muscle Res. 2009;45(1):25-9.10.1540/jsmr.45.25
Search in Google Scholar Back to article
27. Fedorak RN, Empey LR, MacArthur C, Jewell LD. Misoprostol provides a colonic mucosal protective effect during acetic acid-induced colitis in rats. Gastroenterology. 1990;98(3):615-25.10.1016/0016-5085(90)90280-E
Search in Google Scholar Back to article
28. Fomenko IS, Bondarchuk TI, Biletska LP, Panasyuk NB, Sklyarov OY. Study of role of NO-synthase system in gastric mucosa of rats under the influence of non-steroidal anti-inflammatory drugs on the background of adrenaline-induced stress. Bulletin of Problems in Biology and Medicine. 2013;1(3):245-9. (in Ukrainian)
Search in Google Scholar Back to article
29. Timirbulatov MA, Seleznyov EI. Increase intensity method of free oxidation lipid containing blood components and it`s diagnostic value. Laboratory Work. 1981;4:209-11. (in Russian)
Search in Google Scholar Back to article
30. Bradley PP, Christensen RD, Rothstein G. Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood. 1982;60:618-22.10.1182/blood.V60.3.618.618
Search in Google Scholar Back to article
31. Goryachkovskyy AM. Clinical Biochemistry. Second edition, corrected and updated. Odessa; 1998:368. (in Russian)
Search in Google Scholar Back to article
32. Korolyuk MA, Ivanova LI, Mayorova IG. The method of catalase activity determination. Laboratory Work. 1988;1:16-9. (in Russian)
Search in Google Scholar Back to article
33. Ravaeva MY, Chuyan EN. Changes in activity of nitric oxide synthesis system after the action low mm radiation. Scientific Notes of Tavria National University named after V. I. Vernadsky, Series “Biology, Chemistry”. 2011;24(4):201-10. (in Russian)
Search in Google Scholar Back to article
34. Davis RH., Mora JJ. Utilization of exogenous and endogenous ornithine by Neurospora crassa. Bacteriology. 1968;96:383-8.10.1128/jb.96.2.383-388.1968
Search in Google Scholar Back to article
35. Kiselyk IO, Lutsyk MD, Shevchenko LY. Features of the definition of nitrates and nitrites in the peripheral blood of patients with viral hepatitis and jaundice syndrome other etiologies. Laboratory diagnostics. 2001;3:43-5. (in Ukrainian)
Search in Google Scholar Back to article
36. Mourelle M, Vilaseca J, Guarner F, Salas A, Malagelada JR. Toxic dilatation of colon in a rat model of colitis is linked to an inducible form of nitric oxide synthase. Am J Physiol. 1996;270:G425-30.10.1152/ajpgi.1996.270.3.G4258638708
Search in Google Scholar Back to article
37. Vezza T, Algieri F, Rodriguez-Nogales A, Garrido-Mesa J, Utrilla PM, Talhaoui N et al. Immunomodulatory properties of Olea europaea leaf extract in intestinal inflammation. Mol Nutr Food Res. 2017;61(10):1601066.10.1002/mnfr.20160106628731213
Search in Google Scholar Back to article
38. Kang JH, Choi S, Jang JE, Ramalingam P, Ko YT, Kim SY et al. Wasabia japonica is a potential functional food to prevent colitis via inhibiting the NF-κB signaling pathway. Food Funct. 2017;8(8):2865-74.10.1039/C7FO00576H28726958
Search in Google Scholar Back to article
39. Islam J, Koseki T, Watanabe K, Ardiansyah, Budijanto S, Oikawa A et al. Dietary supplementation of fermented rice bran effectively alleviates dextran sodium sulfate-induced colitis in mice. Nutrients. 2017;9(7):E747.10.3390/nu9070747553786128703759
Search in Google Scholar Back to article
40. Shin SK, Cho JH, Kim EJ, Kim EK, Park DK, Kwon KA et al. Anti-inflammatory and anti-apoptotic effects of rosuvastatin by regulation of oxidative stress in a dextran sulfate sodium-induced colitis model. World J Gastroenterol. 2017;23(25):4559-68.10.3748/wjg.v23.i25.4559550437128740344
Search in Google Scholar Back to article
41. Zhao L, Xiao HT, Mu HX, Huang T, Lin ZS, Zhong LLD et al. Magnolol, a natural polyphenol, attenuates dextran sulfate sodium-induced colitis in mice. Molecules. 2017;22(7):E1218.10.3390/molecules22071218615229628726741
Search in Google Scholar Back to article
42. Nieto N. Experimental ulcerative colitis impairs antioxidant defense system in rat intestine. Dig Dis Sci. 2000;45(9):1820-7.10.1023/A:1005565708038
Search in Google Scholar Back to article
43. Dong WG, Mei Q, Yu JP, Xu JM, Xiang L, Xu Y. Effects of melatonin on the expression of iNOS and COX-2 in rat models of colitis. World J Gastroenterol. 2003;9(6):1307-11.10.3748/wjg.v9.i6.1307461180612800246
Search in Google Scholar Back to article
44. Sklyarov AY, Panasyuk NB, Fomenko IS. Role of nitric oxide synthase and cyclooxygenase/lipooxygenase systems in development of experimental ulcerative colitis. J Physiol Pharmacol. 2011;62(1):65-73.
Search in Google Scholar Back to article
45. Cross RK, Keith T, Wilson MD. Nitric oxide in inflammatory bowel disease. Inflamm Bowel Dis. 2003;9(3):179-89.10.1097/00054725-200305000-0000612792224
Search in Google Scholar Back to article
46. Kochar NI, Chandewal AV, Bakal RL, Kochar PN. Nitric oxide and the gastrointestinal tract. Int J Pharm. 2011;7(1):31-9.10.3923/ijp.2011.31.39
Search in Google Scholar Back to article
47. Margolis KG, Stevanovic K, Li Z, Yang QM, Oravecz T, Zambrowicz B et al. Pharmacological reduction of mucosal but not neuronal serotonin opposes inflammation in mouse intestine. Gut. 2014;63(6): 928-37.10.1136/gutjnl-2013-304901403468123749550
Search in Google Scholar Back to article
48. O’Hara JR, Ho W, Linden DR, Mawe GM, Sharkey K A. Enteroendocrine cells and 5-HT availability are altered in mucosa of guinea pigs with TNBS ileitis. Am J Physiol Gastrointest Liver Physiol. 2004;287(5):G998-1007.10.1152/ajpgi.00090.200415231483
Search in Google Scholar Back to article
49. Mawe GM, Hoffman M. Serotonin signaling in the gastrointestinal tract: functions, dysfunctions and therapeutic targets. Nat Rev Gastroenterol Hepatol. 2013;10(8):473-86.10.1038/nrgastro.2013.105404892323797870
Search in Google Scholar Back to article
50. Sklyarov OY, Kosyy YR, Sklyarov YY. Fundamentals of Gastroenterology. Lviv: Quartus; 2011:28. (In Ukrainian)
Search in Google Scholar Back to article

Nitroso-oxidative stress after activation of 5-HT4 receptors under conditions of colitis in rats

Abstract

Paradigm

My account