Flagellin-induced tolerance of the Toll-like receptor 5 signaling pathway in polarized intestinal epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 3, 2007, Pages

  Sun, Jun ^a   Fegan, Pamela E ^a   Desai, Anjali S ^a   Madara, James L ^a   Hobert, Michael E ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Inflammation

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SALMONELLA; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE, TUMOR; CELL POLARITY; CYCLOHEXIMIDE; DOGS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAGELLIN; HUMANS; I-KAPPA B PROTEINS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-8; INTESTINAL MUCOSA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; ONCOGENE PROTEIN V-AKT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33947306877     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00447.2006     Document Type: Article

References (52)

1. Abreu MT, Vora P, Faure E, Thomas LS, Arnold ET, Arditi M. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J Immunol 167: 1609-1616, 2001.
2. Akira S. Mammalian Toll-like receptors. Curr Opin Immunol 15: 5-11, 2003.
3. Amsler K, Kuwada SK. Membrane receptor location defines receptor interaction with signaling proteins in a polarized epithelium. Am J Physiol Cell Physiol 276: C91-C101, 1999.
4. Araki A, Kanai T, Ishikura T, Makita S, Uraushihara K, Iiyama R, Totsuka T, Takeda K, Akira S, Watanabe M. MyD88-deficient mice develop severe intestinal inflammation in dextran sodium sulfate colitis. J Gastroenterol 40: 16-23, 2005.
5. Bambou JC, Giraud A, Menard S, Begue B, Rakotobe S, Heyman M, Taddei F, Cerf-Bensussan N, Gaboriau-Routhiau V. In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 279: 42984-42992, 2004.
6. Burns K, Janssens S, Brissoni B, Olivos N, Beyaert R, Tschopp J. Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J Exp Med 197: 263-268, 2003.
7. Cario E, Brown D, McKee M, Lynch-Devaney K, Gerken G, Podolsky DK. Commensal-associated molecular patterns induce selective toll-like receptor-trafficking from apical membrane to cytoplasmic compartments in polarized intestinal epithelium. Am J Pathol 160: 165-173, 2002.
8. Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol 164: 966-972, 2000.
9. Diamond JM. Twenty-first Bowditch lecture. The epithelial junction: bridge, gate, and fence. Physiologist 20: 10-18, 1977.
10. Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, Ren T, Cody MJ, Michalek SM, Rice NR, Vogel SN. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" vs. " heterotolerance" on NF-kappa B signaling pathway components. J Immunol 170: 508-519, 2003.
11. Eaves-Pyles T, Murthy K, Liaudet L, Virâag L, Ross G, Soriano FG, Szabâo C, Salzman AL. Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166: 1248-1260, 2001.
12. Fukao T, Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol 24: 358-363, 2003.
13. Garcia-del Portillo F, Stein MA, Finlay BB. Release of lipopolysaccharide from intracellular compartments containing Salmonella typhimurium to vesicles of the host epithelial cell. Infect Immun 65: 24-34, 1997.
14. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885, 2001.
15. Gewirtz AT, Simon PO Jr, Schmitt CK, Taylor LJ, Hagedorn CH, O'Brien AD, Neish AS, Madara JL. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107: 99-109, 2001.
16. Gumbiner B. Structure, biochemistry, and assembly of epithelial tight junctions. Am J Physiol Cell Physiol 253: C749-C758, 1987.
17. Hatao F, Muroi M, Hiki N, Ogawa T, Mimura Y, Kaminishi M, Tanamoto K. Prolonged Toll-like receptor stimulation leads to downregulation of IRAK-4 protein. J Leukoc Biol 76: 904-908, 2004.
18. Hershberg RM. The epithelial cell cytoskeleton and intracellular trafficking. V. Polarized compartmentalization of antigen processing and Toll-like receptor signaling in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 283: G833-G839, 2002.
19. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 195: 559-570, 2002.
20. Huang FC, Li Q, Cherayil BJ. A phosphatidyl-inositol-3-kinase- dependent anti-inflammatory pathway activated by Salmonella in epithelial cells. FEMS Microbiol Lett 243: 265-270, 2005.
21. Iwami KI, Matsuguchi T, Masuda A, Kikuchi T, Musikacharoen T, Yoshikai Y. Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J Immunol 165: 6682-6686, 2000.
22. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15-23, 1994.
23. Kuwada SK, Lund KA, Li XF, Cliften P, Amsler K, Opresko LK, Wiley HS. Differential signaling and regulation of apical vs. basolateral EGFR in polarized epithelial cells. Am J Physiol Cell Physiol 275: C1419-C1428, 1998.
24. LeBouder E, Rey-Nores JE, Rushmere NK, Grigorov M, Lawn SD, Affolter M, Griffin GE, Ferrara P, Schiffrin EJ, Morgan BP, Labéta MO. Soluble forms of Toll-like receptor (TLR)2 capable of modulating TLR2 signaling are present in human plasma and breast milk. J Immunol 171: 6680-6689, 2003.
25. Lee SK, Il Kim T, Kim YK, Choi CH, Yang KM, Chae B, Kim WH. Cellular differentiation-induced attenuation of LPS response in HT-29 cells is related to the down-regulation of TLR4 expression. Biochem Biophys Res Commun 337: 457-463, 2005.
26. Lehner MD, Morath S, Michelsen KS, Schumann RR, Hartung T. Induction of cross-tolerance by lipopolysaccharide and highly purified lipoteichoic acid via different Toll-like receptors independent of paracrine mediators. J Immunol 166: 5161-5167, 2001.
27. Li L, Cousart S, Hu J, McCall CE. Characterization of interleukin-1 receptor-associated kinase in normal and endotoxin-tolerant cells. J Biol Chem 275: 23340-23345, 2000.
28. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 5: 446-458, 2005.
29. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, Targan SR, Fort M, Hershberg RM. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113: 1296-1306, 2004.
30. Madara JL, Parkos C, Colgan S, MacLeod RJ, Nash S, Matthews J, Delp C, Lencer W. Cl- secretion in a model intestinal epithelium induced by a neutrophil-derived secretagogue. J Clin Invest 89: 1938-1944, 1992.
31. McCall CE, Grosso-Wilmoth LM, LaRue K, Guzman RN, Cousart SL. Tolerance to endotoxin-induced expression of the interleukin-1 beta gene in blood neutrophils of humans with the sepsis syndrome. J Clin Invest 91: 853-861, 1993.
32. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907, 1993.
33. McCormick BA, Franklin DP, Laux DC, Cohen PS. Type 1 pili are not necessary for colonization of the streptomycin-treated mouse large intestine by type 1-piliated Escherichia coli F-18 and E. coli K-12. Infect Immun 57: 3022-3029, 1989.
34. McCormick BA, Miller SI, Carnes D, Madara JL. Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect Immun 63: 2302-2309, 1995.
35. Medvedev AE, Kopydlowski KM, Vogel SN. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: dysregulation of cytokine, chemokine, and toll-like receptor 2 and 4 gene expression. J Immunol 164: 5564-5574, 2000.
36. Mizel SB, Snipes JA. Gram-negative flagellin-induced self-tolerance is associated with a block in interleukin-1 receptor-associated kinase release from toll-like receptor 5. J Biol Chem 277: 22414-22420, 2002.
37. Moors MA, Li L, Mizel SB. Activation of interleukin-1 receptor-associated kinase by gram-negative flagellin. Infect Immun 69: 4424-4429, 2001.
38. Naik S, Kelly EJ, Meijer L, Pettersson S, Sanderson IR. Absence of Toll-like receptor 4 explains endotoxin hyporesponsiveness in human intestinal epithelium. J Pediatr Gastroenterol Nutr 32: 449-453, 2001.
39. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K, Akira S. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 164: 3476-3479, 2000.
40. Oshitani N, Watanabe K, Nakamura S, Fujiwara Y, Higuchi K, Arakawa T. Dislocation of tight junction proteins without F-actin disruption in inactive Crohn's disease. Int J Mol Med 15: 407-410, 2005.
41. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126: 1054-1070, 2004.
42. Reed KA, Hobert ME, Kolenda CE, Sands KA, Rathman M, O'Connor M, Lyons S, Gewirtz AT, Sansonetti PJ, Madara JL. The Salmonella typhimurium flagellar basal body protein FliE is required for flagellin production and to induce a proinflammatory response in epithelial cells. J Biol Chem 277: 13346-13353, 2002.
43. Sato S, Nomura F, Kawai T, Takeuchi O, Mèuhlradt PF, Takeda K, Akira S. Synergy and cross-tolerance between toll-like receptor (TLR) 2-and TLR4-mediated signaling pathways. J Immunol 165: 7096-7101, 2000.
44. Sato S, Takeuchi O, Fujita T, Tomizawa H, Takeda K, Akira S. A variety of microbial components induce tolerance to lipopolysaccharide by differentially affecting MyD88-dependent and -independent pathways. Int Immunol 14: 783-791, 2002.
45. Söderholm JD, Olaison G, Lindberg E, Hannestad U, Vindels A, Tysk C, Järnerot G, Sjödahl R. Different intestinal permeability patterns in relatives and spouses of patients with Crohn's disease: an inherited defect in mucosal defence? Gut 44: 96-100, 1999.
46. Söderholm JD, Olaison G, Peterson KH, Franzén LE, Lindmark T, Wirén M, Tagesson C, Sjödahl R. Augmented increase in tight junction permeability by luminal stimuli in the non-inflamed ileum of Crohn's disease. Gut 50: 307-313, 2002.
47. Sitaraman SV, Klapproth JM, Moore DA 3rd, Landers C, Targan S, Williams IR, Gewirtz AT. Elevated flagellin-specific immunoglobulins in Crohn's disease. Am J Physiol Gastrointest Liver Physiol 288: G403-G406, 2005.
48. Takeda K, Akira S. TLR signaling pathways. Semin Immunol 16: 3-9, 2004.
49. Tallant T, Deb A, Kar N, Lupica J, de Veer MJ, DiDonato JA. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol 4: 33, 2004.
50. Wiley HS, Herbst JJ, Walsh BJ, Lauffenburger DA, Rosenfeld MG, Gill GN. The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor. J Biol Chem 266: 11083-11094, 1991.
51. Yoza B, LaRue K, McCall C. Molecular mechanisms responsible for endotoxin tolerance. Prog Clin Biol Res 397: 209-215, 1998.
52. Yu Y, Zeng H, Lyons S, Carlson A, Merlin D, Neish AS, Gewirtz AT. TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am J Physiol Gastrointest Liver Physiol 285: G282-G290, 2003.