Toll-like receptor (TLR) 2 agonists ameliorate indomethacin-induced murine ileitis by suppressing the TLR4 signaling

Journal of Gastroenterology and Hepatology (Australia)

Volumn 30, Issue 11, 2015, Pages 1610-1617

  Narimatsu, Kazuyuki ^a   Higashiyama, Masaaki ^a   Kurihara, Chie ^a   Takajo, Takeshi ^a   Maruta, Koji ^a   Yasutake, Yuichi ^a   Sato, Hirokazu ^a   Okada, Yoshikiyo ^a   Watanabe, Chikako ^a   Komoto, Shunsuke ^a   Tomita, Kengo ^a   Nagao, Shigeaki ^a   Miura, Soichiro ^a   Hokari, Ryota ^a  

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

Author keywords

Lipoarabinomannan; Lipoteichoic acid; Nonsteroidal anti inflammatory agents; Toll like receptors

Indexed keywords

INDOMETACIN; INTERLEUKIN 12P40; LIPOARABINOMANNAN; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; MESSENGER RNA; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; PADGEM PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE; NONSTEROID ANTIINFLAMMATORY AGENT; TEICHOIC ACID; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL LABELING; CONTROLLED STUDY; DISEASE ACTIVITY; FLUORESCENCE; HISTOLOGY; ILEITIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INCUBATION TIME; LEUKOCYTE MIGRATION; MACROPHAGE; MALE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; CELL MOTION; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; LEUKOCYTE; METABOLISM; RAW 264.7 CELL LINE;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL MIGRATION ASSAYS, LEUKOCYTE; CELL MOVEMENT; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; ILEITIS; INDOMETHACIN; INFLAMMATION MEDIATORS; INJECTIONS, INTRAPERITONEAL; LEUKOCYTES; LIPOPOLYSACCHARIDES; MICE; RAW 264.7 CELLS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84943605447     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.12980     Document Type: Article

References (46)

1. Goldstein JL, Eisen GM, Lewis B etal. Video capsule endoscopy to prospectively assess small bowel injury with celecoxib, naproxen plus omeprazole, and placebo. Clin. Gastroenterol. Hepatol. 2005; 3: 133-141.
2. Fujimori S, Gudis K, Takahashi Y etal. Distribution of small intestinal mucosal injuries as a result of NSAID administration. Eur. J. Clin. Invest. 2010; 40: 504-510.
3. Graham DY, Opekun AR, Willingham FF, Qureshi WA. Visible small-intestinal mucosal injury in chronic NSAID users. Clin. Gastroenterol. Hepatol. 2005; 3: 55-59.
4. Bjarnason I, Hayllar J, Smethurst P, Price A, Gumpel MJ. Metronidazole reduces intestinal inflammation and blood loss in non-steroidal anti-inflammatory drug induced enteropathy. Gut 1992; 33: 1204-1208.
5. Shah K, Price AB, Talbot IC etal. Effect of longterm misoprostol coadministration with non-steroidal anti-inflammatory drugs: a histological study. Gut 1995; 37: 195-198.
6. Niwa Y, Nakamura M, Ohmiya N etal. Efficacy of rebamipide for diclofenac-induced small-intestinal mucosal injuries in healthy sublects: a prospective, randomized, double-blinded, placebo-controlled, cross-over study. J. Gastroenterol. 2008; 43: 270-276.
7. Kamei K, Kobo Y, Kato N etal. Prophylactic effect of irsogladine maleate against indomethacin-induced small intestinal lesions in rats. Dig. Dis. Sci. 2008; 53: 2657-2666.
8. Bjarnason I, Fehilly B, Smethurst P, Menzies IS, Levi AJ. Importance of local versus systemic effects of non-steroidal anti-inflammatory drugs in increasing small intestinal permeability in man. Gut 1991; 32: 275-277.
9. Reuter BK, Davies NM, Wallace JL. Nonsteroidal anti-inflammatory drug enteropathy in rats: role of permeability, bacteria, and enterohepatic circulation. Gastroenterology 1997; 112: 109-117.
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: 43-51.
11. Watanabe T, Higuchi K, Kobata A etal. Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut 2008; 57: 181-187.
12. Bertrand V, GuimBaud R, Tulliez M etal. Increase in tumor necrosis factor-α production linked to the toxicity of indomethacin for the rat small intestine. Br. J. Pharmacol. 1998; 124: 1385-1394.
13. Morise Z, Granger DN, Fuseler JW, Anderson DC, Grisham MB. Indomethacin induced gastropathy in CD18, intercellular adhesion molecule 1, or P-selectin deficient mice. Gut 1999; 45: 523-528.
14. Beck PL, Xavier R, Lu N etal. Mechanisms of NSAID-induced gastrointestinal injury defined using mutant mice. Gastroenterology 2000; 119: 699-705.
15. Higashiyama M, Hokari R, Kurihara C etal. Indomethacin-induced small intestinal injury is ameliorated by cilostazol, a specific PDE-3 inhibitor. Scand. J. Gastroenterol. 2012; 47: 993-1002.
16. Robert A, Asano T. Resistance of germ free rats to indomethacin-induced intestinal lesions. Prostaglandins 1977; 14: 333-341.
17. Konaka A, Kato S, Tanaka A etal. Roles of enterobacteria, nitric oxide, and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats. Pharmacol. Res. 1999; 40: 517-524.
18. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140: 805-820.
19. Fujiyama Y, Hokari R, Miura S etal. Butter feeding enhances TNF-a production from macrophages and lymphocyte adherence in murine small intestinal microvessels. J. Gastroenterol. Hepatol. 2007; 22: 1838-1845.
20. Watanabe C, Miura S, Hokari R etal. Spatial heterogeneity of TNF-α-induced T cell migration to colonic mucosa is mediated by MAdCAM-1 and VCAM-1. Am. J. Physiol. Gastrointest. Liver Physiol. 2002; 283: G1379-1387.
21. Underhill DM, Ozinsky A, Smith KD, Aderem A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. U.S.A. 1999; 96: 14459-14463.
22. Dobrovolskaia MA, Medvedev AE, Thomas KE etal. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-κB signaling pathway components. J. Immunol. 2003; 170: 508-519.
23. Sato S, Nomura F, Kawai T etal. Synergy and cross-tolerance between Toll-like receptor (TLR) 2- and TLR4-mediated signaling pathways. J. Immunol. 2000; 165: 7096-7101.
24. Takebayashi K, Hokari R, Kurihara C etal. Oral tolerance induced by enterobacteria altered the process of lymphocyte recruitment to intestinal microvessels: roles of endothelial cell adhesion molecules, TGF-beta and negative regulators of TLR signaling. Microcirculation 2009; 16: 251-264.
25. De Vos AF, Pater JM, van den Pangaart PS etal. In vivo lipopolysaccharide exposure of human blood leukocytes induces cross-tolerance to multiple TLR ligands. J. Immunol. 2009; 183: 533-542.
26. Nahid MA, Yao B, Dominguez-Gutierrez PR etal. Regulation of TLR2-mediated tolerance and cross-tolerance through IRAK4 modulation by miR-132 and miR-212. J. Immunol. 2013; 190: 1250-1263.
27. Kim HG, Kim NR, Gim MG etal. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-α production in THP-1 cells and endotoxin shock in mice. J. Immunol. 2008; 180: 2553-2561.
28. Scott KGE, Yu LCH, Buret AG. Role of CD8+ and CD4+ T lymphocytes in jejunal mucosal injury during murine giardiasis. Infect. Immun. 2004; 72: 3536-3542.
29. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch. Surg. 1970; 101: 478-483.
30. Silva MA, Jury J, Porras M, Vergara P, Perdue MH. Intestinal epithelial barrier dysfunction and dendritic cell redistribution during early stages of inflammation in the rat: role for TLR-2 and -4 blockage. Inflamm. Bowel Dis. 2008; 14: 632-644.
31. Takeuchi O, Hoshino K, Kawai T etal. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999; 11: 443-451.
32. Weller A, Isenmann S, VestWeber D. Cloning of the mouse endothelial selectins. J. Biol. Chem. 1992; 21: 15176-15183.
33. Hirotani T, Lee PY, Kuwata H etal. The nuclear IκBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J. Immunol. 2005; 174: 3650-3657.
34. Zhang G, Ghosh S. Negative regulation of Toll-like receptor-mediated signaling by Tollip. J. Biol. Chem. 2002; 277: 7059-7065.
35. Kobayashi K, Hernandez LD, Galan JE etal. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002; 110: 191-202.
36. Baetz A, Frey M, Heeg K, Dalpke AH. Suppressor of cytokine signaling (SOCS) proteins indirectly regulate Toll-like receptor signaling in innate immune cells. J. Biol. Chem. 2004; 279: 54708-54715.
37. Yamazaki S, Muta T, Takeshige K. A novel IkappaB protein, IkappaB-zeta, induced by proinflammatory stimuli, negatively regulates nuclear factor-kappaB in the nuclei. J. Biol. Chem. 2001; 276: 27657-27662.
38. Brasier AR, Lu M, Hai T, Lu Y, Boldogh I. NF-κB-inducible BCL-3 expression is an autoregulatory loop controlling nuclear p50/NF-κB1 residence. J. Biol. Chem. 2001; 276: 32080-32093.
39. Kraus TA, Mayer L. Oral tolerance and inflammatory bowel disease. Curr. Opin. Gastroenterol. 2005; 21: 692-696.
40. Pathak SK, Basu S, Bhattacharyya A etal. Mycobacterium tuberculosis lipoarabinomannan-mediated IRAK-M induction negatively regulates Toll-like receptor-dependent interleukin-12p40 production in macrophages. J. Biol. Chem. 2005; 280: 42794-42800.
41. Spierings ELH, Fujii H, Sun B, Walshe T. A phase I study of the safety of the nutritional supplement, active hexose correlated compound, AHCC, in healthy volunteers. J. Nutr. Sci. Vitaminol. (Tokyo) 2007; 53: 536-539.
42. Foligne B, Dessein R, Marceau M etal. Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein. Gastroenterology 2007; 133: 862-874.
43. Round JL, Lee SM, Li J etal. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011; 332: 974-977.
44. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 2007; 132: 1359-1374.
45. Fan J, Frey RS, Malik AB. TLR 4 signaling induces TLR 2 expression in endothelial cells via neutrophil NADPH oxidase. J. Clin. Invest. 2003; 112: 1234-1243.
46. Faure E, Thomas L, Xu H etal. Bacterial lipopolysaccharide and IFN-γ induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-κB activation. J. Immunol. 2001; 166: 2018-2024.