Muramyl dipeptide activation of nucleotide-binding oligomerization domain 2 protects mice from experimental colitis

Journal of Clinical Investigation

Volumn 118, Issue 2, 2008, Pages 545-559

  Watanabe, Tomohiro ^a,b   Asano, Naoki ^a   Murray, Peter J ^c   Ozato, Keiko ^d   Tailor, Prafullakumar ^d   Fuss, Ivan J ^a   Kitani, Atsushi ^a   Strober, Warren ^a  

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

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; INTERFERON REGULATORY FACTOR 4; MURAMYL DIPEPTIDE; RNA; TOLL LIKE RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STIMULATION; CELLULAR IMMUNITY; COLITIS; DENDRITIC CELL; DISEASE PREDISPOSITION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTESTINE FLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA TRANSLATION; TH1 CELL;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; COLITIS; CROHN DISEASE; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; DOWN-REGULATION; IMMUNITY, NATURAL; INTERFERON REGULATORY FACTORS; LIGANDS; MICE; MICE, MUTANT STRAINS; NOD2 SIGNALING ADAPTOR PROTEIN; RNA, SMALL INTERFERING; TOLL-LIKE RECEPTORS; TRINITROBENZENESULFONIC ACID;

EID: 38849163741     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI33145     Document Type: Article

References (48)

1. Strober, W., Murray, P.J., Kitani, A., and Watanabe, T. 2006. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6:9-20.
2. Watanabe, T., Kitani, A., and Strober, W. 2005. NOD2 regulation of Toll-like receptor responses and the pathogenesis of Crohn's disease. Gut. 54:1515-1518.
3. Inohara, Chamaillard, McDonald, C., and Nunez, G. 2005. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74:355-383.
4. Hugot, J.P., et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature. 411:599-603.
5. Ogura, Y., et al. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature. 411:603-606.
6. Inohara, N., et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278:5509-5512.
7. Girardin, S.E., et al. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278:8869-8872.
8. Marks, D.J., et al. 2006. Defective acute inflammation in Crohn's disease: a clinical investigation. Lancet. 367:668-678.
9. Dziarski, R., and Gupta, D. 2005. Staphylococcus aureus peptidoglycan is a toll-like receptor 2 activator: a reevaluation. Infect. Immun. 73:5212-5216.
10. Akira, S., Takeda, K., and Kaisho, T. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2:675-680.
11. Watanabe, T., Kitani, A., Murray, P.J., and Strober, W. 2004. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat. Immunol. 5:800-808.
12. Bouma, G., and Strober, W. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3:521-533.
13. Strober, W., Fuss, I.J., and Blumberg, R.S. 2002. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20:495-549.
14. Mannon, P.J., et al. 2004. Anti-interleukin-12 antibody for active Crohn's disease. N. Engl. J. Med. 351:2069-2079.
15. Uehara, A., et al. 2005. Muramyldipeptide and diaminopimelic acid-containing desmuramylpeptides in combination with chemically synthesized Toll-like receptor agonists synergistically induced production of interleukin-8 in a NOD2- and NOD1-dependent manner, respectively, in human monocytic cells in culture. Cell. Microbiol. 7:53-61.
16. Netea, M.G., et al. 2005. Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. J. Immunol. 174:6518-6523.
17. van Heel, D.A., et al. 2005. Muramyl dipeptide and toll-like receptor sensitivity in NOD2-associated Crohn's disease. Lancet. 365:1794-1796.
18. Watanabe, T., et al. 2006. Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis. Immunity. 25:473-485.
19. Negishi, H., et al. 2005. Negative regulation of Toll-like-receptor signaling by IRF-4. Proc. Natl. Acad. Sci. U. S. A. 102:15989- 15994.
20. Honma, K., et al. 2005. Interferon regulatory factor 4 negatively regulates the production of proinflammatory cytokines by macrophages in response to LPS. Proc. Natl. Acad. Sci. U. S. A. 102:16001-16006.
21. Yang, Z., et al 2007. NOD2 transgenic mice exhibit enhanced MDP-mediated down-regulation of TLR2 responses and resistance to colitis induction. Gastroenterology. 133:1510-1521.
22. Langenkamp, A., Messi, M., Lanzavecchia, A., and Sallusto, F. 2000. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1:311-316.
23. Kobayashi, K., et al. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell. 110:191-202.
24. Gingras, S., Parganas, E., de Pauw, A., Ihle, J.N., and Murray, P.J. 2004. Re-examination of the role of suppressor of cytokine signaling 1 (SOCS1) in the regulation of toll-like receptor signaling. J. Biol. Chem. 279:54702-54707.
25. Lehtonen, A., et al. 2005. Differential expression of IFN regulatory factor 4 gene in human monocyte-derived dendritic cells and macrophages. J. Immunol. 175:6570-6579.
26. Gutierrez, O., et al. 2002. Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kappa B activation. J. Biol. Chem. 277:41701-41705.
27. McDonald, C., et al. 2005. A role for Erbin in the regulation of Nod2-dependent NF-kappaB signaling. J. Biol. Chem. 280:40301- 40309.
28. Yoshida, K., et al. 2005. Active repression of IFN regulatory factor-1-mediated transactivation by IFN regulatory factor-4. Int. Immunol. 17:1463-1471.
29. Tamura, T., et al. 2005. IFN regulatory factor-4 and - 8 govern dendritic cell subset development and their functional diversity. J. Immunol. 174:2573-2581.
30. Kobayashi, K.S., et al. 2005. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science. 307:731-734.
31. Maeda, S., et al. 2005. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science. 307:734-738.
32. Tada, H., Aiba, S., Shibata, K., Ohteki, T., and Takada, H. 2005. Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect. Immun. 73:7967-7976.
33. Uehori, J., et al. 2005. Dendritic cell maturation induced by muramyl dipeptide (MDP) derivatives: monoacylated MDP confers TLR2/TLR4 activation. J. Immunol. 174:7096-7103.
34. Katakura, K., et al. 2005. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J. Clin. Invest. 115:695-702.
35. Vijay-Kumar, M., et al. 2007. Activation of toll-like receptor 3 protects against DSS-induced acute colitis. Inflamm. Bowel Dis. 13:856-864.
36. Rakoff-Nahoum, S., Hao, L., and Medzhitov, R. 2006. Role of toll-like receptors in spontaneous commensal-dependent colitis. Immunity. 25:319-329.
37. Chedid, L., et al. 1979. Enhancement of certain biological activities of muramyl dipeptide derivatives after conjugation to a multi-poly (DL-alanine)-poly (L-lysine) carrier. Proc. Natl. Acad. Sci. U. S. A. 76:6557-6561.
38. Tsujimoto, M., Kotani, S., Shiba, T., and Kusumoto, S. 1986. Adjuvant activity of 6-O-acyl-muramyldipeptides to enhance primary cellular and humoral immune responses in guinea pigs: dose-response and local reactions observed with selected compounds. Infect. Immun. 53:517-521.
39. Parant, M., et al. 1990. Priming effect of muramyl peptides for induction by lipopolysaccharide of tumor necrosis factor production in mice. J. Leukoc. Biol. 47:164-169.
40. Koga, T., et al. 1986. Muramyl dipeptide induces acute joint inflammation in the mouse. Microbiol. Immunol. 30:717-723.
41. Fichtner-Feigl, S., Fuss, I.J., Preiss, J.C., Strober, W., and Kitani, A. 2005. Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-kappa B decoy oligonucleotides. J. Clin. Invest. 115:3057- 3071.
42. Watanabe, T., Yamori, M., Kita, T., Chiba, T., and Wakatsuki, Y. 2005. CD4+CD25+ T cells regulate colonic localization of CD4 T cells reactive to a microbial antigen. Inflamm. Bowel Dis. 11:541-550.
43. Pauleau, A.L., and Murray, P.J. 2003. Role of nod2 in the response of macrophages to toll-like receptor agonists. Mol. Cell. Biol. 23:7531-7539.
44. Watanabe, T., et al. 2003. A liver tolerates a portal antigen by generating CD11c+ cells, which select Fas ligand+ Th2 cells via apoptosis. Hepatology. 38:403-412.
45. Kondrack, R.M., et al. 2003. Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 198:1797-1806.
46. Watanabe, T., et al. 2002. Administration of an antigen at a high dose generates regulatory CD4+ T cells expressing CD95 ligand and secreting IL-4 in the liver. J. Immunol. 168:2188-2199.
47. Obermeier, F., et al. 1999. Interferon-gamma (IFN-gamma)- and tumour necrosis factor (TNF)-induced nitric oxide as toxic effector molecule in chronic dextran sulphate sodium (DSS)-induced colitis in mice. Clin. Exp. Immunol. 116:238-245.
48. Neurath, M.F., Fuss, I., Kelsall, B.L., Stuber, E., and Strober, W. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 182:1281-1290.