Activation of α7 nicotinic acetylcholine receptors ameliorates indomethacin-induced small intestinal ulceration in mice

European Journal of Pharmacology

Volumn 650, Issue 1, 2011, Pages 411-417

  Kawahara, Ryoji ^a   Yasuda, Masashi ^a   Hashimura, Hiroshi ^a   Amagase, Kikuko ^a   Kato, Shinichi ^a   Takeuchi, Koji ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

7 Nicotinic acetylcholine receptor; Indomethacin; Inducible nitric oxide synthase (iNOS); Neutrophil; Nicotine; Small intestinal ulceration

Indexed keywords

4 CHLORO N (3 QUINUCLIDINYL)BENZAMIDE; BUNGAROTOXIN RECEPTOR; INDOMETACIN; INDUCIBLE NITRIC OXIDE SYNTHASE; METHYLLYCACONITINE; MYELOPEROXIDASE; NICOTINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL MIGRATION; CONTROLLED STUDY; DISEASE SEVERITY; DOSE RESPONSE; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOHISTOCHEMISTRY; INTESTINE INJURY; INTESTINE MUCOSA; INTESTINE ULCER; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPEATED DRUG DOSE; SMALL INTESTINE HEMORRHAGE; SUBMUCOSA;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BENZAMIDES; BICYCLO COMPOUNDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INDOMETHACIN; INTESTINE, SMALL; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; NICOTINE; NICOTINIC AGONISTS; NITRIC OXIDE SYNTHASE TYPE II; PEROXIDASE; RECEPTORS, NICOTINIC; RNA, MESSENGER; TYROSINE; ULCER;

EID: 78649736860     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.10.031     Document Type: Article

References (45)

1. J.S. Beckman, T.W. Beckman, J. Chen, P.A. Marshall, and B.A. Freeman Apparent hydroxyl radicals production by peroxyl radical production by peroxynitrite: implication for endothelial injury from nitric oxide and superoxide Proc. Natl Acad. Sci. USA 87 1990 1620 1624
2. T.R. Bernik, S.G. Friedman, M. Ochani, R. DiRaimo, S. Susarla, C.J. Czura, and K.J. Tracey Cholinergic antiinflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion J. Vasc. Surg. 36 2002 1231 1236
3. L.V. Borovikova, S. Ivanova, M. Zhang, H. Yang, G.I. Botchina, L.R. Watkins, H. Wang, N. Abumrad, J.W. Eaton, and K.J. Tracey Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin Nature 405 2000 458 462
4. N. Boughton-Smith, S.M. Evans, F. Laszlo, B.J.R. Whittle, and S. Moncada The induction of nitric oxide synthase and intestinal vascular permeability by endotoxin in the rat Br. J. Pharmacol. 110 1993 1189 1195 (Pubitemid 24005259)
5. P.P. Bradley, D.A. Priebat, R.D. Christensen, and G. Rothstein Measurement of cutaneous inflammation. Estimation of neutrophil content with an enzyme marker J. Invest. Dermatol. 78 1982 206 220
6. W.J. de Jonge, and L. Ulloa The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation Br. J. Pharmacol. 151 2007 915 929
7. R. Eliakim, F. Karmeli, D. Rachmilewitz, P. Cohen, and A. Fich Effect of chronic nicotine administration on trinitrobenzene sulphonic acid-induced colitis Eur. J. Gastroenterol. Hepatol. 10 1998 1013 1019
8. W.F. Fang, A. Broughton, and E.D. Jacobson Indomethacin induced intestinal inflammation Am. J. Dig. Dis. 22 1977 749 760
9. S. Fujimori, T. Seo, K. Gudis, A. Ehara, T. Kobayashi, K. Mitsui, M. Yonezawa, S. Tanaka, A. Tatsuguchi, and C. Sakamoto Prevention of nonsteroidal anti-inflammatory drug-induced small-intestinal injury by prostaglandin: a pilot randomized controlled trial evaluated by capsule endoscopy Gastrointest. Endosc. 69 2009 1339 1346
10. M. Fujisawa, T. Murata, M. Hori, and H. Ozaki The 5-HT4 receptor agonist mosapride attenuates NSAID-induced gastric mucosal damage J. Gastroenterol. 45 2010 179 186
11. J.E. Ghia, P. Blennerhassett, H. Kumar-Ondiveeran, E.F. Verdu, and S.M. Collins The vagus nerve: a tonic inhibitory influence associated with inflammatory bowel disease in a murine model Gastroenterology 131 2006 1122 1130
12. J.L. Goldstein, G.M. Eisen, B. Lewis, I.M. Gralnek, S. Zlotnick, J.G. Fort Investigators Video capsule endoscopy to prospectively assess small bowel injury with celecoxib, naproxen plus omeprazole, and placebo Clin. Gastroenterol. Hepatol. 3 2005 133 141
13. C. Gotti, and F. Clementi Neuronal nicotinic receptors: from structure to pathology Prog. Neurobiol. 74 2004 363 396
14. D.Y. Graham, A.R. Opekun, F.F. Willingham, and W.A. Qureshi Visible small-intestinal mucosal injury in chronic NSAID users Clin. Gastroenterol. Hepatol. 3 2005 55 59
15. S. Kato, H. Nishio, M. Ogura, and K. Takeuchi Tacrolimus (FK506), an immunosuppressive agent, prevents indomethacin-induced small intestinal ulceration in the rat: inhibition of inducible nitric oxide synthase expression J. Pharmacol. Sci. 103 2007 40 47
16. A. Konaka, S. Kato, A. Tanaka, T. Kunikata, R. Korolkiewicz, and K. Takeuchi Roles of enterobacteria, nitric oxide and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats Pharmacol. Res. 40 1999 517 524
17. H.W. Kosterlitz, and G.M. Lees Pharmacological analysis of intrinsic intestinal reflexes Pharmacol. Rev. 16 1964 301 339
18. F.L. Lanza Endoscopic studies of gastric and duodenal injury after the use of ibuprofen, aspirin and other nonsteroidal antiinflammatory agents Am. J. Med. 13 1984 19 24
19. J. Lindstrom Nicotinic acetylcholine receptors in health and disease Mol. Neurobiol. 15 1997 193 222
20. L. Maiden, B. Thjodleifsson, A. Theodors, J. Gonzalez, and I. Bjarnason A quantitative analysis of NSAID-induced small bowel pathology by capsule enteroscopy Gastroenterology 128 2005 1172 1178
21. T. Matsumoto, T. Kubo, M. Esaki, T. Yano, H. Yamamoto, C. Sakamoto, H. Goto, H. Nakase, S. Tanaka, T. Matsui, K. Sugano, and M. Iida Prevalence of non-steroidal anti-inflammatory drug-induced enteropathy determined by double-balloon endoscopy: a Japanese multicenter study Scand. J. Gastroenterol. 43 2008 490 496 (Pubitemid 351450993)
22. M.J. Miller, J.H. Thompson, X.J. Zhang, H. Sadowska-Krowicka, J.L. Kakkis, U.K. Munshi, M. Sandoval, J.L. Rossi, S. Eloby-Childress, J.S. Beckman, Y.Z. Ye, C.P. Rodi, P.T. Manning, M.G. Currie, and D.A. Clark Role of inducible nitric oxide synthase expression and peroxynitrite formation in guinea pig ileitis Gastroenterology 109 1995 1475 1483
23. V.A. Pavlov, and K.J. Tracey The cholinergic anti-inflammatory pathway Brain Behav. Immun. 19 2005 493-439
24. A. Robert, and T. Asano Resistance of germ-free rats to indomethacin-induced intestinal inflammation Prostaglandins 14 1977 333 341
25. S.A. Saeed, R.U. Simjee, F. Mahmood, and N.N. Rahman Dual inhibition of platelet-activating factor and arachidonic acid metabolism by ajmaline and effect on carrageenan-induced rat paw oedema J. Pharm. Pharmacol. 45 1993 715 719
26. P.B. Sargent The diversity of neuronal nicotinic acetylcholine receptors Annu. Rev. Neurosci. 16 1993 403 443
27. X. Su, M.A. Matthay, and A.B. Malik Requisite role of the cholinergic alpha7 nicotinic acetylcholine receptor pathway in suppressing Gram-negative sepsis-induced acute lung inflammatory injury J. Immunol. 184 2010 401 410
28. A.P. Sykes, C. Brampton, S. Klee, C.L. Chander, C. Whelan, and M.E. Parsons An investigation into the effect and mechanisms of action of nicotine in inflammatory bowel disease Inflamm. Res. 49 2000 311 319
29. K. Takeuchi, T. Miyazawa, A. Tanaka, S. Kato, and T. Kunikata Pathogenic importance of intestinal hypermotility in NSAID-induced small intestinal damage in rats Digestion 66 2002 30 41
30. F.O. The, G.E. Boeckxstaens, S.A. Snoek, J.L. Cash, R. Bennink, G.J. Larosa, R.M. van den Wijngaard, D.R. Greaves, and W.J. de Jonge Activation of the cholinergic anti-inflammatory pathway ameliorates postoperative ileus in mice Gastroenterology 133 2007 1219 1228
31. K.J. Tracy The inflammatory reflex Nature 420 2002 853 859
32. L. Ulloa The vagus nerve and the nicotinic anti-inflammatory pathway Nat. Rev. Drug Discov. 4 2005 673 684
33. M.A. van Maanen, M.C. Lebre, T. van der Poll, G.J. LaRosa, D. Elbaum, M.J. Vervoordeldonk, and P.P. Tak Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice Arthritis Rheum. 60 2009 114 122
34. D.J. van Westerloo, I.A. Giebelen, S. Florquin, M.J. Bruno, G.J. Larosa, L. Ulloa, K.J. Tracey, and T. van der Poll The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice Gastroenterology 130 2006 1822 1830
35. Y. Wang, E.F. Pereira, A.D. Maus, N.S. Ostlie, D. Navaneetham, S. Lei, E.X. Albuquerque, and B.M. Conti-Fine Human bronchial epithelial and endothelial cells express α7 nicotinic acetylcholine receptors Mol. Pharmacol. 60 2001 1201 1209
36. H. Wang, M. Yu, M. Ochani, C.A. Amella, M. Tanovic, S. Susarla, J.H. Li, H. Wang, H. Yang, L. Ulloa, Y. Al-Abed, C.J. Czura, and K.J. Tracey Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation Nature 421 2003 384 388
37. H. Wang, H. Liao, M. Ochani, M. Justiniani, X. Lin, L. Yang, Y. Al-Abed, H. Wang, C. Metz, E.J. Miller, K.J. Tracey, and L. Ulloa Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis Nat. Med. 10 2004 1216 1221
38. T. Watanabe, K. Higuchi, A. Kobata, H. Nishio, T. Tanigawa, M. Shiba, K. Tominaga, Y. Fujiwara, N. Oshitani, T. Asahara, K. Komoto, K. Takeuchi, and T. Arakawa Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent Gut 57 2008 181 187
39. U. Weissenborn, S. Maedge, D. Buettner, and K.F. Sewing Indomethacin-increased gastrointestinal lesions in relation to tissue concentration, food intake and bacterial invasion in the rat Pharmacology 30 1985 32 39
40. B.J.R. Whittle Temporal relationship between cyclooxygenase inhibition as measured by prostacyclin biosynthasus and the gastrointestinal damage induced by indomethacin in rat Gastroenterology 80 1981 94 98
41. B.J.R. Whittle, F. Laszlo, S.M. Evans, and S. Moncada Induction of nitric oxide synthase and microvascular injury in the rat jejunum provoked by indomethacin Br. J. Pharmacol. 116 1995 2286 2290
42. T. Yamada, E. Deitch, R.D. Specian, M.A. Perry, R.B. Sartor, and M.B. Grisham Mechanisms of acute and chronic intestinal inflammation induced by indomethacin Inflammation 17 1993 641 662
43. T. Yasuhiro, H. Ukawa, S. Kato, and K. Takeuchi Involvement of nitric oxide (NO) and inducible NO synthase in the pathogenesis of inflammatory gastric lesions induced by compound 48/80 in rats J. Physiol. Paris 91 1997 131 138
44. N. Yoshida, H. Omoya, M. Oka, K. Furukawa, T. Ito, and T. Karasawa AS-4370, a novel gastrokinetic agent free of dopamine D2 receptor antagonist properties Arch. Int. Pharmacodyn. Thér. 300 1989 51 67
45. H. Yoshikawa, M. Kurokawa, N. Ozaki, K. Nara, K. Atou, E. Takada, H. Kamochi, and N. Suzuki Nicotine inhibits production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha7 Clin. Exp. Immunol. 146 2006 116 123