Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice

Gastroenterology

Volumn 141, Issue 2, 2011, Pages

  Liu, Bo ^a,b   Tonkonogy, Susan L ^a,b,c   Sartor, R Balfour ^b  

^a JILIN UNIVERSITY   (China)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Immune Response; Inflammatory Bowel Disease; Microbiota; Mouse Model

Indexed keywords

BACTERIUM LYSATE; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; MESSENGER RNA; RAG2 PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; SMAD PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; COCULTURE; COLITIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; GERMFREE ANIMAL; HOMEOSTASIS; IMMUNOREGULATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; WILD TYPE;

EID: 80051486126     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.04.053     Document Type: Article

References (47)

1. R.J. Xavier, and D.K. Podolsky Unraveling the pathogenesis of inflammatory bowel disease Nature 448 2007 427 434 (Pubitemid 47123518)
2. R.B. Sartor Microbial influences in inflammatory bowel diseases Gastroenterology 134 2008 577 594 (Pubitemid 351173057)
3. C. Abraham, and J.H. Cho Inflammatory bowel disease N Engl J Med 361 2009 2066 2078
4. C.L. Maynard, and C.T. Weaver Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation Immunol Rev 226 2008 219 233
5. I.J. Fuss, M. Boirivant, and B. Lacy The interrelated roles of TGF-beta and IL-10 in the regulation of experimental colitis J Immunol 168 2002 900 908 (Pubitemid 34049594)
6. R. Kuhn, J. Lohler, and D. Rennick Interleukin-10-deficient mice develop chronic enterocolitis Cell 75 1993 263 274 (Pubitemid 23320290)
7. S.D. Spencer, F. Di Marco, and J. Hooley The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor J Exp Med 187 1998 571 578 (Pubitemid 28093359)
8. D.J. Berg, N. Davidson, and R. Kuhn Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses J Clin Invest 98 1996 1010 1020 (Pubitemid 26293320)
9. H.H. Herfarth, S.P. Mohanty, and H.C. Rath Interleukin 10 suppresses experimental chronic, granulomatous inflammation induced by bacterial cell wall polymers Gut 39 1996 836 845 (Pubitemid 27049087)
10. L. Steidler, W. Hans, and L. Schotte Treatment of murine colitis by Lactococcus lactis secreting interleukin-10 Science 289 2000 1352 1355 (Pubitemid 30656052)
11. K.L. Madsen, S.A. Lewis, and M.M. Tavernini Interleukin 10 prevents cytokine-induced disruption of T84 monolayer barrier integrity and limits chloride secretion Gastroenterology 113 1997 151 159 (Pubitemid 27281769)
12. A. Franke, T. Balschun, and T.H. Karlsen Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility Nat Genet 40 2008 1319 1323
13. E.O. Glocker, D. Kotlarz, and K. Boztug Inflammatory bowel disease and mutations affecting the interleukin-10 receptor N Engl J Med 361 2009 2033 2045
14. L. Williams, L. Bradley, and A. Smith Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages J Immunol 172 2004 567 576 (Pubitemid 38020514)
15. M. de Waal, J. Haanen, and H. Spits Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression J Exp Med 174 1991 915 924
16. D.F. Fiorentino, A. Zlotnik, and T.R. Mosmann IL-10 inhibits cytokine production by activated macrophages J Immunol 147 1991 3815 3822
17. L. Ding, P.S. Linsley, and L.Y. Huang IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression J Immunol 151 1993 1224 1234 (Pubitemid 23219258)
18. R. de Waal Malefyt, H. Yssel, and J.E. de Vries Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells Specific inhibition of IL-2 production and proliferation J Immunol 150 1993 4754 4765 (Pubitemid 23150343)
19. L. Schandene, C. Alonso-Vega, and F. Willems B7/CD28-dependent IL-5 production by human resting T cells is inhibited by IL-10 J Immunol 152 1994 4368 4374
20. K. Taga, H. Mostowski, and G. Tosato Human interleukin-10 can directly inhibit T-cell growth Blood 81 1993 2964 2971 (Pubitemid 23162114)
21. C. Asseman, S. Mauze, and M.W. Leach An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation J Exp Med 190 1999 995 1004
22. H.H. Uhlig, J. Coombes, and C. Mottet Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis J Immunol 177 2006 5852 5860
23. A. Roers, L. Siewe, and E. Strittmatter T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation J Exp Med 200 2004 1289 1297 (Pubitemid 39552570)
24. Y.P. Rubtsov, J.P. Rasmussen, and E.Y. Chi Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces Immunity 28 2008 546 558
25. Y. Cong, C.T. Weaver, and A. Lazenby Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora J Immunol 169 2002 6112 6119 (Pubitemid 36903454)
26. A. Mizoguchi, E. Mizoguchi, and H. Takedatsu Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation Immunity 16 2002 219 230 (Pubitemid 34211962)
27. M.M. Kane, and D.M. Mosser The role of IL-10 in promoting disease progression in leishmaniasis J Immunol 166 2001 1141 1147 (Pubitemid 32060273)
28. R. Lang, R.L. Rutschman, and D.R. Greaves Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter J Immunol 168 2002 3402 3411 (Pubitemid 34250404)
29. M. Murai, O. Turovskaya, and G. Kim Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis Nat Immunol 10 2009 1178 1184
30. C. Veltkamp, S.L. Tonkonogy, and Y.P. de Jong Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tg(epsilon26) mice Gastroenterology 120 2001 900 913 (Pubitemid 32193187)
31. R.K. Sellon, S. Tonkonogy, and M. Schultz Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice Infect Immun 66 1998 5224 5231 (Pubitemid 29044613)
32. H. Groux, F. Cottrez, and M. Rouleau A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells J Immunol 162 1999 1723 1729 (Pubitemid 29307051)
33. H. De Winter, D. Elewaut, and O. Turovskaya Regulation of mucosal immune responses by recombinant interleukin 10 produced by intestinal epithelial cells in mice Gastroenterology 122 2002 1829 1841 (Pubitemid 34651428)
34. R.K. Agarwal, R. Horai, and A.M. Viley Abrogation of anti-retinal autoimmunity in IL-10 transgenic mice due to reduced T cell priming and inhibition of disease effector mechanisms J Immunol 180 2008 5423 5429
35. S. Gregori, D. Tomasoni, and V. Pacciani Differentiation of type 1 T regulatory (Tr1) cells by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway Blood 116 2010 935 944
36. D.D. Nguyen, E.K. Boden, and M.H. Maillard Abnormal innate immune cells can induce colitogenicity in normal adaptive immune cells Gastroenterology 134 Suppl 1 2008 A43
37. A. Hagenbaugh, S. Sharma, and S.M. Dubinett Altered immune responses in interleukin 10 transgenic mice J Exp Med 185 1997 2101 2110 (Pubitemid 27265994)
38. C.L. Maynard, L.E. Harrington, and K.M. Janowski Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10 Nat Immunol 8 2007 931 941 (Pubitemid 47300007)
39. G. Darrasse-Jeze, S. Deroubaix, and H. Mouquet Feedback control of regulatory T cell homeostasis by dendritic cells in vivo J Exp Med 206 2009 1853 1862
40. M. Hesse, C.A. Piccirillo, and Y. Belkaid The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells J Immunol 172 2004 3157 3166 (Pubitemid 38263706)
41. C.A. Albright, R.B. Sartor, and S.L. Tonkonogy Endogenous antigen presenting cell-derived IL-10 inhibits T lymphocyte responses to commensal enteric bacteria Immunol Lett 123 2009 77 87
42. F. Hoentjen, S.L. Tonkonogy, and B. Liu Adoptive transfer of nontransgenic mesenteric lymph node cells induces colitis in athymic HLA-B27 transgenic nude rats Clin Exp Immunol 143 2006 474 483
43. M. Breban, R.E. Hammer, and J.A. Richardson Transfer of the inflammatory disease of HLA-B27 transgenic rats by bone marrow engraftment J Exp Med 178 1993 1607 1616 (Pubitemid 23318439)
44. C.L. Maynard, R.D. Hatton, and W.S. Helms Contrasting roles for all-trans retinoic acid in TGF-beta-mediated induction of Foxp3 and IL-10 genes in developing regulatory T cells J Exp Med 206 2009 343 357
45. B.F. Qian, S.L. Tonkonogy, and R.B. Sartor Reduced responsiveness of HLA-B27 transgenic rat cells to TGF-β and IL-10-mediated regulation of IFN-γ production Inflamm Bowel Dis 14 2008 921 930
46. C. Veltkamp, S.L. Tonkonogy, and Y.P. de Jong Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tg(epsilon26) mice Gastroenterology 120 2001 900 913 (Pubitemid 32193187)
47. Y. Cong, C.T. Weaver, and A. Lazenby Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora J Immunol 169 2002 6112 6119 (Pubitemid 36903454)