Nucleotide-binding oligomerization domain 2 signaling promotes hyperresponsive macrophages and colitis in IL-10-deficient mice

Journal of Immunology

Volumn 190, Issue 6, 2013, Pages 2948-2958

  Jamontt, Joanna ^a   Petit, Stephanie ^b   Clark, Natalie ^a   Parkinson, Scott J ^a,b   Smith, Philip ^a,b  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 84874896525     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201332     Document Type: Article

References (74)

1. Kaser, A., S. Zeissig, and R. S. Blumberg. 2010. Inflammatory bowel disease. Annu. Rev. Immunol. 28: 573-621.
2. Chen, G., M. H. Shaw, Y. G. Kim, and G. Nunez. 2009. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 4: 365-398.
3. Girardin, S. E., I. G. Boneca, J. Viala, M. Chamaillard, A. Labigne, G. Thomas, D. J. Philpott, and P. J. Sansonetti. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278: 8869- 8872.
4. 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.
5. Yang, S., R. Tamai, S. Akashi, O. Takeuchi, S. Akira, S. Sugawara, and H. Takada. 2001. Synergistic effect of muramyldipeptide with lipopolysaccharide or lipoteichoic acid to induce inflammatory cytokines in human monocytic cells in culture. Infect. Immun. 69: 2045-2053.
6. Park, J. H., Y. G. Kim, C. McDonald, T. D. Kanneganti, M. Hasegawa, M. Body- Malapel, N. Inohara, and G. Núnez. 2007. RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs. J. Immunol. 178: 2380-2386.
7. Tada, H., S. Aiba, K. Shibata, T. Ohteki, and H. Takada. 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.
8. Ferwerda, G., M. Kramer, D. de Jong, A. Piccini, L. A. Joosten, I. Devesaginer, S. E. Girardin, G. J. Adema, J. W. van der Meer, B. J. Kullberg, et al. 2008. Engagement of NOD2 has a dual effect on proIL-1beta mRNA transcription and secretion of bioactive IL-1beta. Eur. J. Immunol. 38: 184-191.
9. Uehara, A., S. Yang, Y. Fujimoto, K. Fukase, S. Kusumoto, K. Shibata, S. Sugawara, and H. Takada. 2005. Muramyldipeptide and diaminopimelic acidcontaining 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.
10. Abbott, D. W., Y. Yang, J. E. Hutti, S. Madhavarapu, M. A. Kelliher, and L. C. Cantley. 2007. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell. Biol. 27: 6012-6025.
11. Wolfert, M. A., T. F. Murray, G. J. Boons, and J. N. Moore. 2002. The origin of the synergistic effect of muramyl dipeptide with endotoxin and peptidoglycan. J. Biol. Chem. 277: 39179-39186.
12. Hugot, J. P., M. Chamaillard, H. Zouali, S. Lesage, J. P. Cézard, J. Belaiche, S. Almer, 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.
13. Franke, A., D. P. B. McGovern, J. C. Barrett, K. Wang, G. L. Radford-Smith, T. Ahmad, C. W. Lees, T. Balschun, J. Lee, R. Roberts, et al. 2010. Genomewide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42: 1118-1125.
14. van Heel, D. A., S. Ghosh, K. A. Hunt, C. G. Mathew, A. Forbes, D. P. Jewell, and R. J. Playford. 2005. Synergy between TLR9 and NOD2 innate immune responses is lost in genetic Crohn's disease. Gut 54: 1553-1557.
15. van Heel, D. A., S. Ghosh, M. Butler, K. A. Hunt, A. M. Lundberg, T. Ahmad, D. P. McGovern, C. Onnie, K. Negoro, S. Goldthorpe, et al. 2005. Muramyl dipeptide and Toll-like receptor sensitivity in NOD2-associated Crohn's disease. Lancet 365: 1794-1796.
16. Netea, M. G., G. Ferwerda, D. J. de Jong, T. Jansen, L. Jacobs, M. Kramer, T. H. Naber, J. P. Drenth, S. E. Girardin, B. J. Kullberg, et al. 2005. Nucleotidebinding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. J. Immunol. 174: 6518-6523.
17. Kullberg, B. J., G. Ferwerda, D. J. de Jong, J. P. H. Drenth, L. A. B. Joosten, J. W. Van der Meer, and M. G. Netea. 2008. Crohn's disease patients homozygous for the 3020insC NOD2 mutation have a defective NOD2/TLR4 crosstolerance to intestinal stimuli. Immunology 123: 600-605.
18. Murray, P. J. 2006. Understanding and exploiting the endogenous interleukin-10/ STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6: 379- 386.
19. Takakura, R., T. Kiyohara, Y. Murayama, Y. Miyazaki, Y. Miyoshi, Y. Shinomura, and Y. Matsuzawa. 2002. Enhanced macrophage responsiveness to lipopolysaccharide and CD40 stimulation in a murine model of inflammatory bowel disease: IL-10-deficient mice. Inflamm. Res. 51: 409-415.
20. 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.
21. Liu, B., S. L. Tonkonogy, and R. B. Sartor. 2011. Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice. Gastroenterology 141: 653-662.e4.
22. Schreiber, S., T. Heinig, H.-G. Thiele, and A. Raedler. 1995. Immunoregulatory role of interleukin 10 in patients with inflammatory bowel disease. Gastroenterology 108: 1434-1444.
23. Netea, M. G., B. J. Kullberg, D. J. de Jong, B. Franke, T. Sprong, T. H. Naber, J. P. Drenth, and J. W. Van der Meer. 2004. NOD2 mediates anti-inflammatory signals induced by TLR2 ligands: implications for Crohn's disease. Eur. J. Immunol. 34: 2052-2059.
24. Noguchi, E., Y. Homma, X. Kang, M. G. Netea, and X. Ma. 2009. A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1. Nat. Immunol. 10: 471-479.
25. Correa, I., M. Veny, M. Esteller, J. M. Piqué, J. Yagüe, J. Panés, and A. Salas. 2009. Defective IL-10 production in severe phenotypes of Crohn's disease. J. Leukoc. Biol. 85: 896-903.
26. Franke, A., T. Balschun, T. H. Karlsen, J. Sventoraityte, S. Nikolaus, G. Mayr, F. S. Domingues, M. Albrecht, M. Nothnagel, D. Ellinghaus, et al IBSEN Study Group. 2008. Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat. Genet. 40: 1319-1323.
27. Glocker, E.-O., D. Kotlarz, K. Boztug, E. M. Gertz, A. A. Schäffer, F. Noyan, M. Perro, J. Diestelhorst, A. Allroth, D. Murugan, et al. 2009. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 361: 2033-2045.
28. Biswas, A., J. Wilmanski, H. Forsman, T. Hrncir, L. Hao, H. Tlaskalova- Hogenova, and K. S. Kobayashi. 2011. Negative regulation of Toll-like receptor signaling plays an essential role in homeostasis of the intestine. Eur. J. Immunol. 41: 182-194.
29. Matharu, K. S., E. Mizoguchi, C. A. Cotoner, D. D. Nguyen, B. Mingle, O. I. Iweala, M. E. McBee, A. T. Stefka, G. Prioult, K. M. Haigis, et al. 2009. Toll-like receptor 4-mediated regulation of spontaneous Helicobacter-dependent colitis in IL-10-deficient mice. Gastroenterology 137: 1380-1390.e3.
30. Messlik, A., S. Schmechel, S. Kisling, S. Bereswill, M. M. Heimesaat, A. Fischer, U. Göbel, and D. Haller. 2009. Loss of Toll-like receptor 2 and 4 leads to differential induction of endoplasmic reticulum stress and proapoptotic responses in the intestinal epithelium under conditions of chronic inflammation. J. Proteome Res. 8: 4406-4417.
31. Saunders, S. P., J. L. Barlow, C. M. Walsh, A. Bellsoi, P. Smith, and A. N. J. McKenzie. 2010. C-type lectin SIGN-R1 has a role in experimental colitis and responsiveness to lipopolysaccharide. J. Immunol. 184: 2627-2637.
32. Cario, E., G. Gerken, and D. K. Podolsky. 2007. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132: 1359-1374.
33. Rachmilewitz, D., K. Katakura, F. Karmeli, T. Hayashi, C. Reinus, B. Rudensky, S. Akira, K. Takeda, J. Lee, K. Takabayashi, and E. Raz. 2004. Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 126: 520-528.
34. Smith, P., J. Siddharth, R. Pearson, N. Holway, M. Shaxted, M. Butler, N. Clark, J. Jamontt, R. P. Watson, D. Sanmugalingam, and S. J. Parkinson. 2012. Host genetics and environmental factors regulate ecological succession of the mouse colon tissue-associated microbiota. PLoS One 7: e30273.
35. Watanabe, T., N. Asano, P. J. Murray, K. Ozato, P. Tailor, I. J. Fuss, A. Kitani, and W. Strober. 2008. Muramyl dipeptide activation of nucleotide-binding oligomerization domain 2 protects mice from experimental colitis. J. Clin. Invest. 118: 545-559.
36. Shaw, M. H., T. Reimer, C. Sánchez-Valdepenas, N. Warner, Y. G. Kim, M. Fresno, and G. Nunez. 2009. T cell-intrinsic role of Nod2 in promoting type 1 immunity to Toxoplasma gondii. Nat. Immunol. 10: 1267-1274.
37. Watanabe, T., A. Kitani, P. J. Murray, and W. Strober. 2004. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat. Immunol. 5: 800-808.
38. Spencer, D. M., G. M. Veldman, S. Banerjee, J. Willis, and A. D. Levine. 2002. Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology 122: 94-105.
39. Davidson, N. J., M. W. Leach, M. M. Fort, L. Thompson-Snipes, R. Kühn, W. Müller, D. J. Berg, and D. M. Rennick. 1996. T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J. Exp. Med. 184: 241-251.
40. Schwartz, R. H. 2003. T cell anergy. Annu. Rev. Immunol. 21: 305-334.
41. Smith, P., C. M. Walsh, N. E. Mangan, R. E. Fallon, J. R. Sayers, A. N. McKenzie, and P. G. Fallon. 2004. Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. J. Immunol. 173: 1240-1248.
42. Magalhaes, J. G., J. H. Fritz, L. Le Bourhis, G. Sellge, L. H. Travassos, T. Selvanantham, S. E. Girardin, J. L. Gommerman, and D. J. Philpott. 2008. Nod2-dependent Th2 polarization of antigen-specific immunity. J. Immunol. 181: 7925-7935.
43. Powrie, F., R. Correa-Oliveira, S. Mauze, and R. L. Coffman. 1994. Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 179: 589-600.
44. Mottet, C., H. H. Uhlig, and F. Powrie. 2003. Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J. Immunol. 170: 3939-3943.
45. Asseman, C., S. Read, and F. Powrie. 2003. Colitogenic Th1 cells are present in the antigen-experienced T cell pool in normal mice: control by CD4+ regulatory T cells and IL-10. J. Immunol. 171: 971-978.
46. Josefowicz, S. Z., and A. Rudensky. 2009. Control of regulatory T cell lineage commitment and maintenance. Immunity 30: 616-625.
47. Fiorentino, D. F., A. Zlotnik, P. Vieira, T. R. Mosmann, M. Howard, K. W. Moore, and A. O'Garra. 1991. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146: 3444-3451.
48. 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-kappaB. J. Biol. Chem. 276: 4812-4818.
49. Fritz, J. H., S. E. Girardin, C. Fitting, C. Werts, D. Mengin-Lecreulx, M. Caroff, J. M. Cavaillon, D. J. Philpott, and M. Adib-Conquy. 2005. Synergistic stimulation of human monocytes and dendritic cells by Toll-like receptor 4 and NOD1- and NOD2-activating agonists. Eur. J. Immunol. 35: 2459-2470.
50. Moreira, L. O., K. C. El Kasmi, A. M. Smith, D. Finkelstein, S. Fillon, Y. G. Kim, G. Núnez, E. Tuomanen, and P. J. Murray. 2008. The TLR2-MyD88- NOD2-RIPK2 signalling axis regulates a balanced pro-inflammatory and IL-10- mediated anti-inflammatory cytokine response to Gram-positive cell walls. Cell. Microbiol. 10: 2067-2077.
51. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Mü ller. 1993. Interleukin- 10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
52. Spencer, S. D., F. Di Marco, J. Hooley, S. Pitts-Meek, M. Bauer, A. M. Ryan, B. Sordat, V. C. Gibbs, and M. Aguet. 1998. The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor. J. Exp. Med. 187: 571-578.
53. Takeda, K., B. E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Förster, 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.
54. Glocker, E., D. Kotlarz, K. Boztug, E. Gertz, A. Schaffer, S. Koletzko, N. Shah, S. Snapper, B. Grimbacher, and C. Klein. 2009. Early-onset inflammatory bowel disease caused by loss-of-function mutations in the IL10-receptor genes. Inflamm. Bowel Dis. 15: S56.
55. Anderson, C. A., D. C. Massey, J. C. Barrett, N. J. Prescott, M. Tremelling, S. A. Fisher, R. Gwilliam, J. Jacob, E. R. Nimmo, H. Drummond, et al Wellcome Trust Case Control Consortium. 2009. Investigation of Crohn's disease risk loci in ulcerative colitis further defines their molecular relationship. Gastroenterology 136: 523-529.e3.
56. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
57. Rakoff-Nahoum, S., L. Hao, and R. Medzhitov. 2006. Role of Toll-like receptors in spontaneous commensal-dependent colitis. Immunity 25: 319-329.
58. Kobayashi, M., M. N. Kweon, H. Kuwata, R. D. Schreiber, H. Kiyono, K. Takeda, and S. Akira. 2003. Toll-like receptor-dependent production of IL- 12p40 causes chronic enterocolitis in myeloid cell-specific Stat3-deficient mice. J. Clin. Invest. 111: 1297-1308.
59. 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.
60. 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-kappaB activity and IL-1beta processing. [Published erratum appears in 2005 Science 308: 633 and 2011 Science 333: 288.] Science 307: 734-738.
61. Kim, Y. G., M. H. Shaw, N. Warner, J. H. Park, F. Chen, Y. Ogura, and G. Núnez. 2011. Cutting edge: Crohn's disease-associated Nod2 mutation limits production of proinflammatory cytokines to protect the host from Enterococcus faecalisinduced lethality. J. Immunol. 187: 2849-2852.
62. Netea, M. G., G. Ferwerda, D. J. de Jong, S. E. Girardin, B. J. Kullberg, and J. W. van der Meer. 2005. NOD2 3020insC mutation and the pathogenesis of Crohn's disease: impaired IL-1beta production points to a loss-of-function phenotype. Neth. J. Med. 63: 305-308.
63. Inohara, N., Y. Ogura, A. Fontalba, O. Gutierrez, F. Pons, J. Crespo, K. Fukase, S. Inamura, S. Kusumoto, M. Hashimoto, et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2: implications for Crohn's disease. J. Biol. Chem. 278: 5509-5512.
64. Kramer, M., M. G. Netea, D. J. de Jong, B. J. Kullberg, and G. J. Adema. 2006. Impaired dendritic cell function in Crohn's disease patients with NOD2 3020insC mutation. J. Leukoc. Biol. 79: 860-866.
65. Wehkamp, J., J. Harder, M. Weichenthal, M. Schwab, E. Schäffeler, M. Schlee, K. R. Herrlinger, A. Stallmach, F. Noack, P. Fritz, et al. 2004. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alphadefensin expression. Gut 53: 1658-1664.
66. Cantó, E., E. Moga, E. Ricart, O. Garcia-Bosch, E. Garcia-Planella, C. Juarez, and S. Vidal. 2009. MDP-induced selective tolerance to TLR4 ligands: impairment in NOD2 mutant Crohn's disease patients. Inflamm. Bowel Dis. 15: 1686- 1696.
67. Hedl, M., J. Li, J. H. Cho, and C. Abraham. 2007. Chronic stimulation of Nod2 mediates tolerance to bacterial products. Proc. Natl. Acad. Sci. USA 104: 19440- 19445.
68. Meinzer, U., S. Esmiol-Welterlin, F. Barreau, D. Berrebi, M. Dussaillant, S. Bonacorsi, F. Chareyre, M. Niwa-Kawakita, C. Alberti, G. Sterkers, et al. 2008. Nod2 mediates susceptibility to Yersinia pseudotuberculosis in mice. PLoS One 3: e2769.
69. Barreau, F., U. Meinzer, F. Chareyre, D. Berrebi, M. Niwa-Kawakita, M. Dussaillant, B. Foligne, V. Ollendorff, M. Heyman, S. Bonacorsi, et al. 2007. CARD15/NOD2 is required for Peyer's patches homeostasis in mice. PLoS One 2: e523.
70. Macho Fernandez, E., V. Valenti, C. Rockel, C. Hermann, B. Pot, I. G. Boneca, and C. Grangette. 2011. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60: 1050-1059.
71. Lee, C. G., K. H. Kang, J. S. So, H. K. Kwon, J. S. Son, M. K. Song, A. Sahoo, H. J. Yi, K. C. Hwang, T. Matsuyama, et al. 2009. A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol. Immunol. 46: 613-621.
72. Lee, C. G., W. Hwang, K. E. Maeng, H. K. Kwon, J. S. So, A. Sahoo, S. H. Lee, Z. Y. Park, and S. H. Im. 2011. IRF4 regulates IL-10 gene expression in CD4(+) T cells through differential nuclear translocation. Cell. Immunol. 268: 97-104.
73. Hedl, M., and C. Abraham. 2011. Secretory mediators regulate Nod2-induced tolerance in human macrophages. Gastroenterology 140: 231-241.
74. Watanabe, N., K. Ikuta, K. Okazaki, H. Nakase, Y. Tabata, M. Matsuura, H. Tamaki, C. Kawanami, T. Honjo, and T. Chiba. 2003. Elimination of local macrophages in intestine prevents chronic colitis in interleukin-10-deficient mice. Dig. Dis. Sci. 48: 408-414.