A20 is an early responding negative regulator of Toll-like receptor 5 signalling in intestinal epithelial cells during inflammation

Clinical and Experimental Immunology

Volumn 159, Issue 2, 2010, Pages 185-198

  Oshima, N ^a   Ishihara, S ^a   Rumi, M A K ^c   Aziz, M M ^a   Mishima, Y ^a   Kadota, C ^a   Moriyama, I ^a   Ishimura, N ^a   Amano, Y ^b   Kinoshita, Y ^a  

^a SHIMANE UNIVERSITY   (Japan)

^b SHIMANE UNIVERSITY HOSPITAL   (Japan)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

A20; Intestinal inflammation; Negative regulator; NF B; TLR

Indexed keywords

DEXTRAN SULFATE; FLAGELLIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN A20;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL STIMULATION; CELL STRAIN HT29; COLITIS; COLON; CONTROLLED STUDY; DISEASE MODEL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; KNOCKOUT GENE; MALE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN CULTURE TECHNIQUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; RIBONUCLEASE PROTECTION ASSAY; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CHEMOKINE CXCL2; CYSTEINE ENDOPEPTIDASES; EPITHELIAL CELLS; FLAGELLIN; FLOW CYTOMETRY; GENE EXPRESSION; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTESTINES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5;

EID: 72949102226     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.04048.x     Document Type: Article

References (60)

1. Medzhitov R, Janeway CA Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002 296 : 298 300.
2. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006 124 : 783 801.
3. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000 406 : 782 787.
4. Underhill DM, Ozinsky A. Toll-like receptors: key mediators of microbe detection. Curr Opin Immunol 2002 14 : 103 110.
5. Kopp E, Medzhitov R. Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003 15 : 396 401.
6. Monteleone I, Vavassori P, Biancone L, Monteleone G, Pallone F. Immunoregulation in the gut: success and failures in human disease. Gut 2002 50 : III60 4.
7. 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 2000 164 : 966 972.
8. Cario E. Bacterial interactions with cells of the intestinal mucosa: toll-like receptors and NOD2. Gut 2005 54 : 1182 1193.
9. Hausmann M, Kiessling S, Mestermann S et al. Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 2002 122 : 1987 2000.
10. Ortega-Cava CF, Ishihara S, Rumi MA et al. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol 2003 170 : 3977 3985.
11. Ishihara S, Rumi MA, Kadowaki Y et al. Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 2004 173 : 1406 1416.
12. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004 118 : 229 241.
13. Abreu MT, Fukata M, Arditi M. TLR signaling in the gut in health and disease. J Immunol 2005 174 : 4453 4460.
14. Kawai T, Takeuchi O, Fujita T et al. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 2001 167 : 5887 5894.
15. Horng T, Barton GM, Flavell RA, Medzhitov R. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 2002 420 : 329 333.
16. O'Neill LA, Fitzgerald KA, Bowie AG. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol 2003 24 : 286 290.
17. Li X, Qin J. Modulation of Toll-interleukin 1 receptor mediated signaling. J Mol Med 2005 83 : 258 266.
18. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 2005 5 : 446 458.
19. Shibolet O, Podolsky DK. TLRs in the gut. IV. Negative regulation of Toll-like receptors and intestinal homeostasis: addition by subtraction. Am J Physiol Gastrointest Liver Physiol 2007 292 : G1469 73.
20. Takeda K, Akira S. TLR signaling pathways. Semin Immunol 2004 16 : 3 9.
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 2000 165 : 6682 6686.
22. Brint EK, Xu D, Liu H et al. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat Immunol 2004 5 : 373 379.
23. Divanovic S, Trompette A, Atabani SF et al. Negative regulation of Toll-like receptor 4 signaling by the Toll-like receptor homolog RP105. Nat Immunol 2005 6 : 571 578.
24. Wald D, Qin J, Zhao Z et al. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 2003 4 : 920 927.
25. 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 2003 197 : 263 268.
26. Kinjyo I, Hanada T, Inagaki-Ohara K et al. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 2002 17 : 583 591.
27. Ishihara S, Rumi MA, Ortega-Cava CF et al. Therapeutic targeting of toll-like receptors in gastrointestinal inflammation. Curr Pharm Des 2006 12 : 4215 4228.
28. Beyaert R, Heyninck K, Van Huffel S. A20 and A20-binding proteins as cellular inhibitors of nuclear factor-kappa B-dependent gene expression and apoptosis. Biochem Pharmacol 2000 60 : 1143 1151.
29. Lee EG, Boone DL, Chai S et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000 289 : 2350 2354.
30. Boone DL, Turer EE, Lee EG et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004 5 : 1052 1060.
31. O'Reilly SM, Moynagh PN. Regulation of Toll-like receptor 4 signalling by A20 zinc finger protein. Biochem Biophys Res Commun 2003 303 : 586 593.
32. Gon Y, Asai Y, Hashimoto S et al. A20 inhibits toll-like receptor 2- and 4-mediated interleukin-8 synthesis in airway epithelial cells. Am J Respir Cell Mol Biol 2004 31 : 330 336.
33. Kobayashi K, Hernandez LD, Galan JE, Janeway CA Jr., Medzhitov R, Flavell RA. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002 110 : 191 202.
34. Zhang G, Ghosh S. Negative regulation of toll-like receptor-mediated signaling by Tollip. J Biol Chem 2002 277 : 7059 7065.
35. Rhee SH, Im E, Riegler M, Kokkotou E, O'Brien M, Pothoulakis C. Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci USA 2005 102 : 13610 13615.
36. Poltorak A, He X, Smirnova I et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998 282 : 2085 2088.
37. Baumgart DC, Olivier WA, Reya T, Peritt D, Rombeau JL, Carding SR. Mechanisms of intestinal epithelial cell injury and colitis in interleukin 2 (IL2)-deficient mice. Cell Immunol 1998 187 : 52 66.
38. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 2004 126 : 1054 1070.
39. Turer EE, Tavares RM, Mortier E et al. Homeostatic MyD88-dependent signals cause lethal inflammation in the absence of A20. J Exp Med 2008 205 : 451 464.
40. Vijay-Kumar M, Aitken JD, Gewirtz AT. Toll like receptor-5: protecting the gut from enteric microbes. Semin Immunopathol 2008 30 : 11 21.
41. Uematsu S, Akira S. Immune responses of TLR5(+) lamina propria dendritic cells in enterobacterial infection. J Gastroenterol 2009 44 : 803 811.
42. Mizoguchi A, Mizoguchi E. Inflammatory bowel disease, past, present and future: lessons from animal models. J Gastroenterol 2008 43 : 1 17.
43. 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 2001 167 : 1882 1885.
44. Coornaert B, Carpentier I, Beyaert R. A20: central gatekeeper in inflammation and immunity. J Biol Chem 2009 284 : 8217 8221.
45. Hitotsumatsu O, Ahmad RC, Tavares R et al. The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 2008 28 : 381 390.
46. Mitsuyama K, Matsumoto S, Rose-John S et al. STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 2006 55 : 1263 1269.
47. Suzuki A, Hanada T, Mitsuyama K et al. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J Exp Med 2001 193 : 471 481.
48. Hommes DW, Peppelenbosch MP, van Deventer SJ. Mitogen activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets. Gut 2003 52 : 144 151.
49. Krikos A, Laherty CD, Dixit VM. Transcriptional activation of the tumor necrosis factor alpha-inducible zinc finger protein, A20, is mediated by kappa B elements. J Biol Chem 1992 267 : 17971 17976.
50. Wertz IE, O'Rourke KM, Zhou H et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004 430 : 694 699.
51. Nomura F, Akashi S, Sakao Y et al. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 2000 164 : 3476 3479. (Pubitemid 30169796)
52. Cario E, Podolsky DK. Intestinal epithelial TOLLerance versus inTOLLerance of commensals. Mol Immunol 2005 42 : 887 893.
53. Dalpke AH, Lehner MD, Hartung T, Heeg K. Differential effects of CpG-DNA in Toll-like receptor-2/-4/-9 tolerance and cross-tolerance. Immunology 2005 116 : 203 212.
54. van Aubel RA, Keestra AM, Krooshoop DJ, van Eden W, van Putten JP. Ligand-induced differential cross-regulation of Toll-like receptors 2, 4 and 5 in intestinal epithelial cells. Mol Immunol 2007 44 : 3702 3714.
55. Abreu MT, Arnold ET, Thomas LS et al. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 2002 277 : 20431 20437.
56. Nakayama K, Okugawa S, Yanagimoto S et al. Involvement of IRAK-M in peptidoglycan-induced tolerance in macrophages. J Biol Chem 2004 279 : 6629 6634.
57. Ortis F, Pirot P, Naamane N et al. Induction of nuclear factor-kappaB and its downstream genes by TNF-alpha and IL-1beta has a pro-apoptotic role in pancreatic beta cells. Diabetologia 2008 51 : 1213 1225.
58. Liuwantara D, Elliot M, Smith MW et al. Nuclear factor-kappaB regulates beta-cell death: a critical role for A20 in beta-cell protection. Diabetes 2006 55 : 2491 2501.
59. Li HL, Zhuo ML, Wang D et al. Targeted cardiac overexpression of A20 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction. Circulation 2007 115 : 1885 1894.
60. Song XT, Evel-Kabler K, Shen L, Rollins L, Huang XF, Chen SY. A20 is an antigen presentation attenuator, and its inhibition overcomes regulatory T cell-mediated suppression. Nat Med 2008 14 : 258 265.