Abnormally differentiated subsets of intestinal macrophage play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria

Journal of Immunology

Volumn 175, Issue 10, 2005, Pages 6900-6908

  Kamada, Nobuhiko ^a   Hisamatsu, Tadakazu ^a   Okamoto, Susumu ^a   Sato, Toshiro ^a   Matsuoka, Katsuyoshi ^a   Arai, Kumiko ^a   Nakai, Takaaki ^a   Hasegawa, Akira ^a   Inoue, Nagamu ^a   Watanabe, Noriaki ^b   Akagawa, Kiyoko S ^c   Hibi, Toshifumi ^a  

^a KEIO UNIVERSITY   (Japan)

^b KITASATO INSTITUTE HOSPITAL   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CD11B ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 23;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL STIMULATION; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; INFLAMMATION; INTESTINE FLORA; LAMINA PROPRIA; MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SPLEEN; TH1 CELL;

EID: 27744437941     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.10.6900     Document Type: Article

References (41)

1. Janeway, C. A, Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
2. Sieling, P. A., and R. L. Modlin. 2002. Toll-like receptors: mammalian "taste receptors" for a smorgasbord of microbial invaders. Curr. Opin. Microbiol. 5: 70-75.
3. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
4. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
5. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686.
6. Mosser, D. M. 2003. The many faces of macrophage activation. J. Leukocyte Biol. 73: 209-212.
7. Podolsky, D. K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347: 417-429.
8. 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.
9. Hugot, J. P., M. Chamaillard, H. Zouali, S. Lesage, J. P. Cezard, 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.
10. 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.
11. Mahida, Y. R. 2000. The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm. Bowel Dis. 6: 21-33.
12. Regler, G. 2004. Update in inflammatory bowel disease pathogenesis. Curr. Opin. Gastroenterol. 20: 311-317.
13. Eckmann, L. 2004. Innate immunity and mucosal bacterial interactions in the intestine. Curr. Opin. Gastroenterol. 20: 82-88.
14. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
15. Sellon, R. K., S. Tonkonogy, M. Schultz, L. A. Dieleman, W. Grenther, E. Balish, D. M. Rennick, and R. B. Sartor. 1998. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66: 5224-5231.
16. Madsen, K. L., J. S. Doyle, M. M. Tavernini, L. D. Jewell, R. P. Rennie, and R. N. Fedorak. 2000. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology 118: 1094-1105.
17. Hoentjen, F., H. J. Harmsen, H. Braat, C. D. Torrice, B. A. Mann, R. B. Sartor, L. A. Dieleman, K. L. Madsen, J. S. Doyle, M. M. Tavernini, et al. 2003. Antibiotics with a selective aerobic or anaerobic spectrum have different therapeutic activities in various regions of the colon in interleukin 10 gene deficient mice. Gut 52: 1721-1727.
18. Igietseme, J. U., G. A. Ananaba, J. Bolier, S. Bowers, T. Moore, T. Belay, F. O. Eko, D. Lyn, and C. M. Black. 2000. Suppression of endogenous IL-10 gene expression in dendritic cells enhances antigen presentation for specific Th1 induction: potential for cellular vaccine development. J. Immunol. 164: 4212-4219.
19. Hickman, S. P., J. Chan, and P. Salgame. 2002. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J. Immunol. 168: 4636-4642.
20. 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.
21. 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.
22. 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.
23. 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.
24. Hirotani, T., P. Y. Lee, H. Kuwata, M. Yamamoto, M. Matsumoto, I. Kawase, S. Akira, and K. Takeda. 2005. The nuclear IκB protein IκBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J. Immunol. 174: 3650-3657.
25. Kanai, T., M. Watanabe, A. Okazawa, T. Sato, M. Yamazaki, S. Okamoto, H. Ishii, T. Totsuka, R. Iiyama, R. Okamoto, et al. 2001. Macrophage-derived IL-18-mediated intestinal inflammation in the murine model of Crohn's disease. Gastroenterology 121: 875-888.
26. Chelvarajan, R. L., S. M. Collins, J.'M. Van Willigen, and S. Bondada. 2005. The unresponsiveness of aged mice to polysaccharide antigen is a result of a defect in macrophage function. J. Leukocyte Biol. 77: 503-512.
27. Akagawa, K. S. 2002. Functional heterogeneity of colony-stimulating factor-induced human monocyte-derived macrophages. Int. J. Hematol 76: 27-34.
28. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
29. Verreck, F. A., T. de Boer, D. M. Langenberg, M. A. Hoeve, M. Kramer, E. Vaisberg, R. Kastelein, A. Kolk, R. de Waal-Malefyt, and T. H. Ottenhoff. 2004. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. USA 101: 4560-4565.
30. Mochida-Nishimura, K., K. S. Akagawa, and E. A. Rich. 2001. Interleukin-10 contributes development of macrophage suppressor activities by macrophage colony-stimulating factor, but not by granulocyte-macrophage colony-stimulating factor. Cell. Immunol. 214: 81-88.
31. Smith, P. D., L. E. Smythies, M. Mosteller-Barnum, D. A. Sibley, M. W. Russell, M. Merger, M. T. Sellers, J. M. Orenstein, T. Shimada, M. F. Graham, and H. Kubagawa. 2001. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS- and IgA-mediated activities. J. Immunol. 167: 2651-2656.
32. Smythies, L. E., M. Sellers, R. H. Clements, M. Mosteller-Barnum, G. Meng, W. H. Benjamin, J. M. Orenstein, and P. D. Smith. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115: 66-75.
33. Pull, S. L., J. M. Doherty, J. C. Mills, J. I. Gordon, and T. S. Stappenbeck. 2005. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc. Natl. Acad. Sci. USA 102: 99-104.
34. Cecchini, M. G., M. G. Dominguez, S. Mocci, A. Wetterwald, R. Felix, H. Fleisch, O. Chisholm, W. Hofstetter, J. W. Pollard, and E. R. Stanley. 1994. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120: 1357-1372.
35. Klebl, F. H., J. E. Olsen, S. Jain, and W. F. Doe. 2001. Expression of macrophage-colony stimulating factor in normal and inflammatory bowel disease intestine. J. Pathol. 195: 609-615.
36. Liu, J., S. Cao, L. M. Herman, and X. Ma. 2003. Differential regulation of interleukin (IL)-12 p35 and p40 gene expression and interferon (IFN)-γ-primed IL-12 production by IFN regulatory factor 1. J. Exp. Med. 198: 1265-1276.
37. Oliveira, M. A., G. M. Lima, M, T. Shio, P. J. Leenen, and I. A. Abrahamsohn. 2003. Immature macrophages derived from mouse bone marrow produce large amounts of IL-12p40 after LPS stimulation. J. Leukocyte Biol. 74: 857-867.
38. Hoentjen, F., R. B. Sartor, M. Ozaki, and C. Jobin. 2005. STAT3 regulates NF-kappaB recruitment to the IL-12p40 promoter in dendritic cells. Blood 105: 689-696.
39. Zhou, L., A. A. Nazarian, and S. T. Smale. 2004. Interleukin-10 inhibits interleukin-12 p40 gene transcription by targeting a late event in the activation pathway. Mol. Cell. Biol. 24: 2385-2396.
40. 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.
41. Hashimoto, S., M. Yamada, K. Motoyoshi, and K. S. Akagawa. 1997. Enhancement of macrophage colony-stimulating factor-induced growth and differentiation of human monocytes by interleukin-10. Blood 89: 315-321.