Inhibition of Helicobacter hepaticus-induced colitis by IL-10 requires the p50/p105 subunit of NF-κB

Journal of Immunology

Volumn 177, Issue 10, 2006, Pages 7332-7339

  Tomczak, Michal F ^a   Erdman, Susan E ^b   Davidson, Anne ^c   Wang, Yan Yan ^a   Nambiar, Prashant M ^b   Rogers, Arlin B ^b   Rickman, Barry ^b   Luchetti, David ^b   Fox, James G ^b   Horwitz, Bruce H ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 12P40; LIPOPOLYSACCHARIDE; PROTEIN P50; RAG2 PROTEIN; SYNAPTOTAGMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; GENE EXPRESSION; HELICOBACTER HEPATICUS; HEMATOPOIETIC CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; RADIATION CHIMERA;

EID: 33750838717     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.10.7332     Document Type: Article

References (44)

1. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3: 521-533.
2. Podolsky, D. K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347: 417-429.
3. Erdman, S., J. G. Fox, C. A. Dangler, D. Feldman, and B. H. Horwitz. 2001. Typhlocolitis in NF-κB-deficient mice. J. Immunol. 166: 1443-1447.
4. 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.
5. Strober, W., I. J. Fuss, and R. S. Blumberg. 2002. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20: 495-549.
6. 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.
7. 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 γ interferon-dependent mechanism. Infect. Immun. 66: 5157-5166.
8. Rogers, A. B., and J. G. Fox. 2004 Inflammation and cancer. I. Rodent models of infectious gastrointestinal and liver cancer. Am. J. Physiol. 286: G361-G366.
9. Cahill, R. J., C. J. Foltz, J. G. Fox, C. A. Dangler, F. Powrie, and D. B. Schauer. 1997. Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect. Immun. 65: 3126-3131.
10. + regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am. J. Pathol. 162: 691-702.
11. Von Freeden-Jeffry, U., N. Davidson, R. Wiler, M. Fort, S. Burdach, and R. Murray. 1998. IL-7 deficiency prevents development of a non-T cell non-B cell-mediated colitis. J. Immunol. 161: 5673-5680.
12. Li, X., J. G. Fox, M. T. Whary, L. Yan, B. Shames, and Z. Zhao. 1998. SCID/NCr mice naturally infected with Helicobacter hepaticus develop progressive hepatitis, proliferative typhlitis, and colitis. Infect. Immun. 66: 5477-5484.
13. Tomczak, M. F., S. E. Erdman, T. Poutahidis, A. B. Rogers, H. Holcombe, B. Plank, J. G. Fox, and B. H. Horwitz. 2003. NF-κB is required within the innate immune system to inhibit microflora-induced colitis and expression of IL-12 p40. J. Immunol. 171: 1484-1492.
14. + regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res. 63: 6042-6050.
15. + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms, J. Exp. Med. 197: 111-119.
16. Li, Q., and I. M. Verma. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2: 725-734.
17. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
18. Fichtner-Feigl, S., I. J. Fuss, J. C. Preiss, W. Strober, and A. Kitani. 2005. Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-κB decoy oligonucleotides. J. Clin. Invest. 115: 3057-3071.
19. Neurath, M. F., S. Pettersson, K. H. Meyer zum Buschenfelde, and W. Strober. 1996. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-κB abrogates established experimental colitis in mice. Nat. Med. 2: 998-1004.
20. Gadjeva, M., M. F. Tomczak, M. Zhang, Y. Y. Wang, K. Dull, A. B. Rogers, S. E. Erdman, J. G. Fox, M. Carroll, and B. H. Horwitz. 2004. A role for NF-κB subunits p50 and p65 in the inhibition of lipopolysaccharide-induced shock. J. Immunol. 173: 5786-5793.
21. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376: 167-170.
22. Reddy, B., S. Gupta, Y. Chuzhin, A. M. Kalergis, L. Budhai, M. Zhang, G. Droguett, M. S. Horwitz, J. R. Chowdhury, S. G. Nathenson, and A. Davidson. 2001. The effect of CD28/B7 blockade on alloreactive T and B cells after liver cell transplantation. Transplantation 71: 801-811.
23. Fox, J. G., L. Yan, B. Shames, J. Campbell, J. C. Murphy, and X. Li. 1996. Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus. Infect. Immun. 64: 3673-3681.
24. 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.
25. Cattaruzza, M., W. Slodowski, M. Stojakovic, R. Krzesz, and M. Hecker. 2003. Interleukin-10 induction of nitric-oxide synthase expression attenuates CD40-mediated interleukin-12 synthesis in human endothelial cells. J. Biol. Chem. 278: 37874-37880.
26. MacDermott, R. P. 1999. Chemokines in the inflammatory bowel diseases. J. Clin. Immunol. 19: 266-272.
27. - T cell activation in the presence of T regulatory cells. J. Immunol. 175: 641-645.
28. Driessler, F., K. Venstrom, R. Sabat, K. Asadullah, and A. J. Schottelius. 2004. Molecular mechanisms of interleukin-10-mediated inhibition of NF-κB activity: a role for p50. Clin. Exp. Immunol 135: 64-73.
29. Takeda, K., B. E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Forster, and S. Akira. 1999. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10: 39-49.
30. Wehinger, J., F. Gouilleux, B. Groner, J. Finke, R. Mertelsmann, and R. M. Weber-Nordt. 1996. IL-10 induces DNA binding activity of three STAT proteins (Stat1, Stat3, and Stat5) and their distinct combinatorial assembly in the promoters of selected genes. FEBS Lett. 394: 365-370.
31. Williams, L., L. Bradley, A. Smith, and B. Foxwell. 2004. 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: 567-576.
32. Kuwata, H., Y. Watanabe, H. Miyoshi, M. Yamamoto, T. Kaisho, K. Takeda, and S. Akira. 2003. IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-α production in macrophages. Blood 102: 4123-4129.
33. Lang, R., D. Patel, J. J. Morris, R. L. Rutschman, and P. J. Murray. 2002. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 169: 2253-2263.
34. + T cells. J. Biol. Chem. 279: 8460-8468.
35. Wessells, J., M. Baer, H. A. Young, E. Claudio, K. Brown, U. Siebenlist, and P. F. Johnson. 2004. BCL-3 and NF-κB p50 attenuate lipopolysaccharide-induced inflammatory responses in macrophages. J. Biol. Chem. 279: 49995-50003.
36. Autschbach, P., J. Braunstein, B. Helmke, I. Zuna, G. Schurmann, Z. I. Niemir, R. Wallich, H. F. Otto, and S. C. Meuer. 1998. In situ expression of interleukin-10 in noninflamed human gut and in inflammatory bowel disease. Am. J. Pathol. 153: 121-130.
37. Colpaert, S., K. Vanstraelen, Z. Liu, F. Penninckx, K. Geboes, P. Rutgeerts, and J. Ceuppens. 2002. Decreased lamina propria effector cell responsiveness to interleukin-10 in ileal Crohn's disease. Clin. Immunol. 102: 68-76.
38. Fedorak, R. N., A. Gangl, C. O. Elson, P. Rutgeerts, S. Schreiber, G. Wild, S. B. Hanauer, A. Kilian, M. Cohard, A. LeBeaut, and B. Feagan. 2000. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease: the Interleukin 10 Inflammatory Bowel Disease Cooperative Study Group. Gastroenterology 119: 1473-1482.
39. Schreiber, S., R. N. Fedorak, O. H. Nielsen, G. Wild, C. N. Williams, S. Nikolaus, M. Jacyna, B. A. Lashner, A. Gangl, P. Rutgeerts, et al. 2000. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease: Crohn's Disease IL-10 Cooperative Study Group. Gastroenterology 119: 1461-1472.
40. Hugot, J. P., M. Chamaillard, H. Zouali, S. Lesage, J. P. Cezard, J. Belaiche, S. Aimer, C. Tysk, C. A. O'Morain, M. Gassull, et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
41. Ogura, Y., D. K. Bonen, N. Inohara, D. L. Nicolae, F. F. Chen, R. Ramos, H. Britton, T. Moran, R. Karaliuskas, R. H. Duerr, et al. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
42. Kobayashi, K. S., M. Chamaillard, Y. Ogura, O. Henegariu, N. Inohara, G. Nunez, and R. A. Flavell. 2005. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307: 731-734.
43. Maeda, S., L. C. Hsu, H. Liu, L. A. Bankston, M. Iimura, M. F. Kagnoff, L. Eckmann, and M. Karin. 2005. Nod2 mutation in Crohn's disease potentiates NF-κB activity and IL-1β processing. Science 307: 734-738.
44. Ogura, Y., N. Inohara, A. Benito, F. F. Chen, S. Yamaoka, and G. Nunez. 2001. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-κB. J. Biol. Chem. 276: 4812-4818.