Endogenous antigen presenting cell-derived IL-10 inhibits T lymphocyte responses to commensal enteric bacteria

Immunology Letters

Volumn 123, Issue 1, 2009, Pages 77-87

  Albright, Carol A ^a,b   Sartor, R Balfour ^a,b   Tonkonogy, Susan L ^a,c  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Antigen presenting cells; Cytokine regulation; IL 10 deficient mice

Indexed keywords

BACTERIUM LYSATE; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23;

ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CECUM; CELL CULTURE; COMMENSAL; CONTROL GROUP; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTEROBACTERIACEAE; FLOW CYTOMETRY; GERMFREE ANIMAL; IMMUNE RESPONSE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; COLITIS; COLON; ENTEROBACTERIACEAE; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-23; MICE; MICE, KNOCKOUT;

EID: 63749103662     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2009.02.010     Document Type: Article

References (56)

1. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology 134 (2008) 577-594
2. Xavier R.J., and Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448 (2007) 427-434
3. Duchmann R., May E., Heike M., Knolle P., Neurath M., and Meyer zum Buschenfelde K.H. T cell specificity and cross reactivity towards Enterobacteria, Bacteroides, Bifidobacterium, and antigens from resident intestinal flora in humans. Gut 44 (1999) 812-818
4. Landers C.J., Cohavy O., Misra R., Yang H., Lin Y.C., Braun J., et al. Selected loss of tolerance evidenced by Crohn's disease-associated immune responses to auto- and microbial antigens. Gastroenterology 123 (2002) 689-699
5. Elson C.O. Genes, microbes, and T cells-new therapeutic targets in Crohn's disease. N Engl J Med 346 (2002) 614-616
6. Schmidt C., Giese T., Ludwig B., Mueller-Molaian I., Marth T., Zeuzem S., et al. Expression of interleukin-12-related cytokine transcripts in inflammatory bowel disease: elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis. Inflamm Bowel Dis 11 (2005) 16-23
7. Monteleone G., Biancone L., Marasco R., Morrone G., Marasco O., Luzza F., et al. Interleukin 12 is expressed and actively released by Crohn's disease intestinal lamina propria mononuclear cells. Gastroenterology 112 (1997) 1169-1178
8. Monteleone G., Trapasso F., Parrello T., Biancone L., Stella A., Iuliano R., et al. Bioactive IL-18 expression is up-regulated in Crohn's disease. J Immunol 163 (1999) 143-147
9. + lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. J Immunol 157 (1996) 1261-1270
10. Seiderer J., Elben I., Diegelmann J., Glas J., Stallhofer J., Tillack C., et al. Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): upregulated colonic IL-17F expression in active Crohn's disease and analysis of the IL17F p.His161Arg polymorphism in IBD. Inflamm Bowel Dis 14 (2008) 437-445
11. Fujino S., Andoh A., Bamba S., Ogawa A., Hata K., Araki Y., et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52 (2003) 65-70
12. Murch S.H., Braegger C.P., Walker-Smith J.A., and MacDonald T.T. Location of tumour necrosis factor α by immunohistochemistry in chronic inflammatory bowel disease. Gut 34 (1993) 1705-1709
13. Targan S.R., Hanauer S.B., van Deventer S.J., Mayer L., Present D.H., Braakman T., et al. A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor α for Crohn's disease. N Engl J Med 337 (1997) 1029-1035
14. Mannon P.J., Fuss I.J., Mayer L., Elson C.O., Sandborn W.J., Present D., et al. Anti-interleukin-12 antibody for active Crohn's disease. N Engl J Med 351 (2004) 2069-2079
15. Colombel J.F., Cortot A., and Van Kruiningen H.J. Antibiotics in Crohn's disease. Gut 48 (2001) 647
16. Sartor R.B. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126 (2004) 1620-1633
17. Strober W., Fuss I.J., and Blumberg R.S. The immunology of mucosal models of inflammation. Annu Rev Immunol 20 (2002) 495-549
18. Ma A., Datta M., Margosian E., Chen J., and Horak I. T cells, but not B cells, are required for bowel inflammation in interleukin 2-deficient mice. J Exp Med 182 (1995) 1567-1572
19. Mizoguchi A., Mizoguchi E., Takedatsu H., Blumberg R.S., and Bhan A.K. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16 (2002) 219-230
20. Elson C.O., Cong Y., McCracken V.J., Dimmitt R.A., Lorenz R.G., and Weaver C.T. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 206 (2005) 260-276
21. Mizoguchi A., and Bhan A.K. A case for regulatory B cells. J Immunol 176 (2006) 705-710
22. Spencer D.M., Veldman G.M., Banerjee S., Willis J., and Levine A.D. Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology 122 (2002) 94-105
23. Yen D., Cheung J., Scheerens H., Poulet F., McClanahan T., McKenzie B., et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 116 (2006) 1310-1316
24. Izcue A., Hue S., Buonocore S., Arancibia-Cárcamo C.V., Ahern P.P., Iwakura Y., et al. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28 (2008) 559-570
25. Sellon R.K., Tonkonogy S.L., Schultz M., Dieleman L.A., Grenther W., Balish E., et al. 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
26. Veltkamp C., Tonkonogy S.L., de Jong Y.P., Albright C., Grenther W.B., Balish E., et al. Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tgε26 mice. Gastroenterology 120 (2001) 900-913
27. Taurog J.D., Richardson J.A., Croft J.T., Simmons W.A., Zhou M., Fernandez-Sueiro J.L., et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 180 (1994) 2359-2364
28. + T cells reactive to enteric bacterial antigens in spontaneously colitic C3H/HeJBir mice: increased T helper cell type 1 response and ability to transfer disease. J Exp Med 187 (1998) 855-864
29. + T cells that respond to bacterial antigens. J Immunol 162 (1999) 1884-1888
30. Lodes M.J., Cong Y., Elson C.O., Mohamath R., Landers C.J., Targan S.R., et al. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113 (2004) 1296-1306
31. Dieleman L.A., Hoentjen F., Qian B.-F., Sprengers D., Tjwa E., Torres M.F., et al. Reduced ratio of protective versus proinflammatory cytokine responses to commensal bacteria in HLA-B27 transgenic rats. Clin Exp Immunol 136 (2004) 30-39
32. Maloy K.J., and Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol 2 (2001) 816-822
33. Kuhn R., Lohler J., Rennick D., Rajewsky K., and Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75 (1993) 263-274
34. Dieleman L.A., Arends A., Tonkonogy S.L., Goerres M.S., Craft D.W., Grenther W., et al. Helicobacter hepaticus does not induce or potentiate colitis in interleukin-10-deficient mice. Infect Immun 68 (2000) 5107-5113
35. Moore K.W., de Waal Malefyt R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19 (2001) 683-765
36. Grutz G. New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J Leukoc Biol 77 (2005) 3-15
37. Chirdo F.G., Millington O.R., Beacock-Sharp H., and Mowat A.M. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol 35 (2005) 1831-1840
38. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5 (1993) 1461-1471
39. Asseman C., Mauze S., Leach M.W., Coffman R.L., and Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 190 (1999) 995-1004
40. Cong Y., Weaver C.T., Lazenby A., and Elson C.O. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J Immunol 169 (2002) 6112-6119
41. Akbari O., DeKruyff R.H., and Umetsu D.T. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2 (2001) 725-731
42. Chen C.C., Louie S., McCormick B.A., Walker W.A., and Shi H.N. Helminth-primed dendritic cells alter the host response to enteric bacterial infection. J Immunol 176 (2006) 472-483
43. Bradley L.M., Duncan D.D., Tonkonogy S., and Swain S.L. Characterization of antigen-specific CD4+ effector T cells in vivo: immunization results in a transient population of MEL-14-, CD45RB- helper cells that secretes interleukin 2 (IL-2), IL-3, IL-4, and interferon gamma. J Exp Med 174 (1991) 547-559
44. Phillips J.M., Parish N.M., Drage M., and Cooke A. Interactions through the IL-10 receptor regulate autoimmune diabetes. J Immunol 167 (2001) 6087-6091
45. Couper K.N., Blount D.G., and Riley E.M. IL-10: the master regulator of immunity to infection. J Immunol 180 (2008) 5771-5777
46. Liu B., Holt L., and Sartor R.B. APC regulate Th1/Th17-mediated colitis in IL-10 deficient mice. Gastroenterology 132 (2007) A33
47. Gu Y., Yang J., Ouyang X., Liu W., Li H., Yang J., et al. Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur J Immunol 38 (2008) 1807-1813
48. Sansom D.M., Manzotti C.N., and Zheng Y. What's the difference between CD80 and CD86?. Trends Immunol 24 (2003) 314-319
49. He Q., Moore T.T., Eko F.O., Lyn D., Ananaba G.A., Martin A., et al. Molecular basis for the potency of IL-10-deficient dendritic cells as a highly efficient APC system for activating Th1 response. J Immunol 174 (2005) 4860-4869
50. Spencer S.D., Di Marco F., Hooley J., Pitts-Meek S., Bauer M., Ryan A.M., et al. The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor. J Exp Med 187 (1998) 571-578
51. Takeda K., Clausen B.E., Kaisho T., Tsujimura T., Terada N., Forster I., et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10 (1999) 39-49
52. Jarry A., Bossard C., Bou-Hanna C., Masson D., Espaze E., Denis M.G., et al. Mucosal IL-10 and TGF-β play crucial roles in preventing LPS-driven, IFN-γ-mediated epithelial damage in human colon explants. J Clin Invest 118 (2008) 1132-1142
53. Hoentjen F., Sartor R.B., Ozaki M., and Jobin C. STAT3 regulates NF-κB recruitment to the IL-12p40 promoter in dendritic cells. Blood 105 (2005) 689-696
54. Monteleone I., Platt A.M., Jaensson E., Agace W.W., and Mowat A.M. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur J Immunol 38 (2008) 1533-1547
55. +, and double-negative Peyer's patch dendritic cells. J Immunol 166 (2001) 4884-4890
56. Mauri C., Gray D., Mushtaq N., and Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 197 (2003) 489-501