IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis

Journal of Experimental Medicine

Volumn 203, Issue 11, 2006, Pages 2485-2494

  Kullberg, Marika C ^a,b   Jankovic, Dragana ^a   Feng, Carl G ^a   Hue, Sophie ^c   Gorelick, Peter L ^d   McKenzie, Brent S ^e   Cua, Daniel J ^e   Powrie, Fiona ^c   Cheever, Allen W ^f   Maloy, Kevin J ^c   Sher, Alan ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NATIONAL CANCER INSTITUTE   (United States)

^e Schering Plough Biopharma ^*  (United States)

^f BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; MONOCLONAL ANTIBODY; PROTEIN P40;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; COLITIS; CONTROLLED STUDY; ENTERITIS; ENTEROPATHY; FEMALE; HELICOBACTER HEPATICUS; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; CELLS, CULTURED; COLITIS; FEMALE; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; INTERLEUKIN-12 SUBUNIT P35; INTERLEUKIN-23; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-10; T-LYMPHOCYTES;

EID: 33750530394     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061082     Document Type: Article

References (51)

1. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
2. Oppmann, B., R. Lesley, B. Blom, J.C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 13:715-725.
3. Cua, D.J., J. Sherlock, Y. Chen, C.A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:744-748.
4. Langrish, C.L., Y. Chen, W.M. Blumenschein, J. Mattson, B. Basham, J.D. Sedgwick, T. McClanahan, R.A. Kastelein, and D.J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240.
5. Murphy, C.A., C.L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R.A. Kastelein, J.D. Sedgwick, and D.J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198:1951-1957.
6. Parham, C., M. Chirica, J. Timans, E. Vaisberg, M. Travis, J. Cheung, S. Pflanz, R. Zhang, K.P. Singh, F. Vega, et al. 2002. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rβ1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168:5699-5708.
7. Aggarwal, S., N. Ghilardi, M.H. Xie, F.J. de Sauvage, and A.L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910-1914.
8. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
9. Park, H., Z. Li, X.O. Yang, S.H. Chang, R. Nurieva, Y.H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133-1141.
10. Kolls, J.K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity. 21:467-476.
11. Parronchi, P., P. Romagnani, F. Annunziato, S. Sampognaro, A. Becchio, L. Giannarini, E. Maggi, C. Pupilli, F. Tonelli, and S. Romagnani. 1997. Type 1 T-helper cell predominance and interleukin-12 expression in the gut of patients with Crohn's disease. Am. J. Pathol. 150:823-832.
12. Monteleone, G., L. Biancone, R. Marasco, G. Morrone, O. Marasco, F. Luzza, and F. Pallone. 1997. Interleukin 12 is expressed and actively released by Crohn's disease intestinal lamina propria mononuclear cells. Gastroenterology. 112:1169-1178.
13. Becker, C., S. Wirtz, M. Blessing, J. Pirhonen, D. Strand, O. Bechthold, J. Frick, P.R. Galle, I. Autenrieth, and M.F. Neurath. 2003. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J. Clin. Invest. 112:693-706.
14. Schmidt, C., T. Giese, B. Ludwig, I. Mueller-Molaian, T. Marth, S. Zeuzem, S.C. Meuer, and A. Stallmach. 2005. 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. 11:16-23.
15. Mannon, P.J., I.J. Fuss, L. Mayer, C.O. Elson, W.J. Sandborn, D. Present, B. Dolin, N. Goodman, C. Groden, R.L. Hornung, et al. 2004. Anti-interleukin-12 antibody for active Crohn's disease. N. Engl. J. Med. 351:2069-2079.
16. Fuss, I.J., C. Becker, Z. Yang, C. Groden, R.L. Hornung, F. Heller, M.F. Neurath, W. Strober, and P.J. Mannon. 2006. Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody. Inflamm. Bowel Dis. 12:9-15.
17. Neurath, M.F., I. Fuss, B.L. Kelsall, E. Stuber, and W. Strober. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 182:1281-1290.
18. Duchmann, R., E. Schmitt, P. Knolle, K.H. Meyer zum Buschenfelde, and M. Neurath. 1996. Tolerance towards resident intestinal flora in mice is abrogated in experimental colitis and restored by treatment with interleukin-10 or antibodies to interleukin-12. Eur. J. Immunol. 26:934-938.
19. Davidson, N.J., S.A. Hudak, R.E. Lesley, S. Menon, M.W. Leach, and D.M. Rennick. 1998. IL-12, but not IFN-γ, plays a major role in sustaining the chronic phase of colitis in IL-10-deficient mice. J. Immunol. 161:3143-3149.
20. Kullberg, M.C., J.M. Ward, P.L. Gorelick, P. Caspar, S. Hieny, A. Cheever, D. Jankovic, and A. Sher. 1998. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66:5157-5166.
21. Kullberg, M.C., A.G. Rothfuchs, D. Jankovic, P. Caspar, T.A. Wynn, P.L. Gorelick, A.W. Cheever, and A. Sher. 2001. Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation. Infect. Immun. 69:4232-4241.
22. + T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196:505-515.
23. Langrish, C.L., B.S. McKenzie, N.J. Wilson, R. de Waal Malefyt, R.A. Kastelein, and D.J. Cua. 2004. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol. Rev. 202:96-105.
24. Belladonna, M.L., J.C. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona, M.C. Fioretti, U. Grohmann, and P. Puccetti. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168:5448-5454.
25. Hue, S., P. Ahern, S. Buonocore, M.C. Kullberg, D.J. Cua, B.S. McKenzie, F. Powrie, and K.J. Maloy. 2006. IL-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203:2473-2483.
26. Weaver, C.T., L.E. Harrington, P.R. Mangan, M. Gavrieli, and K.M. Murphy. 2006. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity. 24:677-688.
27. McKenzie, B.S., R.A. Kastelein, and D.J. Cua. 2006. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27:17-23.
28. Chen, Y., C.L. Langrish, B. McKenzie, B. Joyce-Shaikh, J.S. Stumhofer, T. McClanahan, W. Blumenschein, T. Churakovsa, J. Low, L. Presta, et al. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116:1317-1326.
29. Veldhoen, M., R.J. Hocking, C.J. Atkins, R.M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 24:179-189.
30. H17 lineage. Nature. 441:231-234.
31. H17 and regulatory T cells. Nature. 441:235-238.
32. Happel, K.I., P.J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L.J. Quinton, A.R. Odden, J.E. Shellito, G.J. Bagby, S. Nelson, and J.K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202:761-769.
33. Willenborg, D.O., S. Fordham, C.C. Bernard, W.B. Cowden, and I.A. Ramshaw. 1996. IFN-γ plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157:3223-3227.
34. Ferber, I.A., S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C.G. Fathman. 1996. Mice with a disrupted IFN-γ gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156:5-7.
35. Krakowski, M., and T. Owens. 1996. Interferon-γ confers resistance to experimental allergic encephalomyelitis. Eur. J. Immunol. 26:1641-1646.
36. Vermeire, K., H. Heremans, M. Vandeputte, S. Huang, A. Billiau, and P. Matthys. 1997. Accelerated collagen-induced arthritis in IFN-γ receptor-deficient mice. J. Immunol. 158:5507-5513.
37. Guedez, Y.B., K.B. Whittington, J.L. Clayton, L.A. Joosten, F.A. van de Loo, W.B. van den Berg, and E.F. Rosloniec. 2001. Genetic ablation of interferon-γ up-regulates interleukin-1β expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum. 44:2413-2424.
38. + T cells. Immunity. 1:553-562.
39. + TH1-like responses. J. Clin. Invest. 98:1010-1020.
40. Yen, D., J. Cheung, H. Scheerens, F. Poulet, T. McClanahan, B. McKenzie, M.A. Kleinschek, A. Owyang, J. Mattson, W. Blumenschein, et al. 2006. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116:1310-1316.
41. R cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119.
42. Cooper, A.M., A. Kipnis, J. Turner, J. Magram, J. Ferrante, and I.M. Orme. 2002. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J. Immunol. 168:1322-1327.
43. Khader, S.A., J.E. Pearl, K. Sakamoto, L. Gilmartin, G.K. Bell, D.M. Jelley-Gibbs, N. Ghilardi, F. deSauvage, and A.M. Cooper. 2005. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-γ responses if IL-12p70 is available. J. Immunol. 175:788-795.
44. Russell, T.D., Q. Yan, G. Fan, A.P. Khalifah, D.K. Bishop, S.L. Brody, and M.J. Walter. 2003. IL-12 p40 homodimer-dependent macrophage chemotaxis and respiratory viral inflammation are mediated through IL-12 receptor β1. J. Immunol. 171:6866-6874.
45. Pahan, K., F.G. Sheikh, X. Liu, S. Hilger, M. McKinney, and T.M. Petro. 2001. Induction of nitric-oxide synthase and activation of NF-κB by interleukin-12 p40 in microglial cells. J. Biol. Chem. 276:7899-7905.
46. Jana, M., S. Dasgupta, R.N. Saha, X. Liu, and K. Pahan. 2003. Induction of tumor necrosis factor-alpha (TNF-α) by interleukin-12 p40 monomer and homodimer in microglia and macrophages. J. Neurochem. 86:519-528.
47. Khader, S.A., S. Partida-Sanchez, G. Bell, D.M. Jelley-Gibbs, S. Swain, J.E. Pearl, N. Ghilardi, F.J. Desauvage, F.E. Lund, and A.M. Cooper. 2006. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J. Exp. Med. 203:1805-1815.
48. Ward, J.M., J.G. Fox, M.R. Anver, D.C. Haines, C.V. George, M.J. Collins Jr., P.L. Gorelick, K. Nagashima, M.A. Gonda, R.V. Gilden, et al. 1994. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl. Cancer Inst. 86:1222-1227.
49. Fox, J.G., F.E. Dewhirst, J.G. Tully, B.J. Paster, L. Yan, N.S. Taylor, M.J. Collins Jr., P.L. Gorelick, and J.M. Ward. 1994. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J. Clin. Microbiol. 32:1238-1245.
50. + lymphocytes with a Th2 cytokine profile. J. Immunol. 164:3047-3055.
51. Ge, Z., D.A. White, M.T. Whary, and J.G. Fox. 2001. Fluorogenic PCR-based quantitative detection of a murine pathogen, Helicobacter hepaticus. J. Clin. Microbiol. 39:2598-2602.