Unique CD14+ intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-γ axis

Journal of Clinical Investigation

Volumn 118, Issue 6, 2008, Pages 2269-2280

  Kamada, Nobuhiko ^a   Hisamatsu, Tadakazu ^a   Okamoto, Susumu ^a   Chinen, Hiroshi ^a   Kobayashi, Taku ^a   Sato, Toshiro ^a   Sakuraba, Atsushi ^a   Kitazume, Mina T ^a   Sugita, Akira ^b   Koganei, Kazutaka ^b   Akagawa, Kiyoko S ^c   Hibi, Toshifumi ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; COMPARATIVE STUDY; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; INTESTINE; MACROPHAGE; MONONUCLEAR CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULCERATIVE COLITIS;

ANTIGENS, CD; ANTIGENS, CD14; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CELL DIFFERENTIATION; CELL SEPARATION; CROHN DISEASE; FLOW CYTOMETRY; HUMANS; INFLAMMATION; INTERFERON TYPE II; INTERLEUKIN-23; INTESTINAL MUCOSA; MACROPHAGES; MODELS, BIOLOGICAL; MONOCYTES; MUCOUS MEMBRANE;

EID: 45749107055     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI34610     Document Type: Article

References (41)

1. Xavier, R.J., and Podolsky, D.K. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 448:427-434.
2. Hibi, T., and Ogata, H. 2006. Novel pathophysiological concepts of inflammatory bowel disease. J. Gastroenterol. 41:10-16.
3. Fuss, I.J., et al. 1996. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 157:1261-1270.
4. Matsuoka, K., et al. 2004. T-bet upregulation and subsequent interleukin 12 stimulation are essential for induction of Th1 mediated immunopathology in Crohn's disease. Gut. 53:1303-1308.
5. Sartor, R.B. 2006. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3:390-407.
6. Gordon, S., and Taylor, P.R. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964.
7. Mantovani, A., et al. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677-686.
8. Mosser, D.M. 2003. The many faces of macrophage activation. J. Leukoc. Biol. 73:209-212.
9. Rogler, G., et al. 1998. Isolation and phenotypic characterization of colonic macrophages. Clin. Exp. Immunol. 112:205-215.
10. Smith, P.D., et al. 2001. Intestinal macrophages lack CD14 and CD89 and consequently are downregulated for LPS- and IgA-mediated activities. J. Immunol. 167:2651-2656.
11. Smythies, L.E., et al. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115:66-75.
12. Denning, T.L., Wang, Y.C., Patel, S.R., Williams, I.R., and Pulendran, B. 2007. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8:1086-1094.
13. Schenk, M., and Mueller, C. 2007. Adaptations of intestinal macrophages to an antigen-rich environment. Semin. Immunol. 19:84-93.
14. Kobayashi, M., et al. 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.
15. Hirotani, T., et al. 2005. The nuclear IkappaB protein IkappaBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J. Immunol. 174:3650-3657.
16. Kanai, T., et al. 2000. Interleukin 18 is a potent proliferative factor for intestinal mucosal lymphocytes in Crohn's disease. Gastroenterology. 119:1514-1523.
17. Kanai, T., et al. 2001. Macrophage-derived IL-18-mediated intestinal inf lammation in the murine model of Crohn's disease. Gastroenterology. 121:875-888.
18. Fuss, I.J., et al. 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.
19. Schenk, M., Bouchon, A., Seibold, F., and Mueller, C. 2007. TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J. Clin. Invest. 117:3097-3106.
20. Kamada, N., et al. 2005. 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. J. Immunol. 175:6900-6908.
21. Grimm, M.C., Pavli, P., Van de Pol, E., and Doe, W.F. 1995. Evidence for a CD14+ population of monocytes in inflammatory bowel disease mucosa - implications for pathogenesis. Clin. Exp. Immunol. 100:291-297.
22. Rugtveit, J., et al. 1997. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastroenterology. 112:1493-1505.
23. Geissmann, F., Jung, S., and Littman, D.R. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82.
24. Mizoguchi, A., et al. 2007. Dependence of intestinal granuloma formation on unique myeloid DC-like cells. J. Clin. Invest. 117:605-615.
25. Kim, S.C., et al. 2005. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 128:891-906.
26. van Beelen, A.J., et al. 2007. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity. 27:660-669.
27. Cua, D.J., et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:744-748.
28. Murphy, C.A., et al. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198:1951-1957.
29. Langrish, C.L., et al. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240.
30. Vaknin-Dembinsky, A., Balashov, K., and Weiner, H.L. 2006. IL-23 is increased in dendritic cells in multiple sclerosis and down-regulation of IL-23 by antisense oligos increases dendritic cell IL-10 production. J. Immunol. 176:7768-7774.
31. Neurath, M.F. 2007. IL-23: a master regulator in Crohn disease. Nat. Med. 13:26-28.
32. Yen, D., 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.
33. Duerr, R.H., et al. 2006. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science. 314:1461-1463.
34. Uhlig, H.H., et al. 2006. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity. 25:309-318.
35. Annunziato, F., et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204:1849-1861.
36. Powrie, F., et al. 1994. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity. 1:553-562.
37. Kullberg, M.C., et al. 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.
38. Hue, S., et al. 2006. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203:2473-2483.
39. Kullberg, M.C., et al. 2006. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203:2485-2494.
40. Chinen, H., et al. 2007. Lamina propria c-kit (+) immune precursors reside in human adult intestine and differentiate into natural killer cells. Gastroenterology. 133:559-573.
41. Ulloa, L., Doody, J., and Massague, J. 1999. Inhibition of transforming growth factor-beta/SMAD signalling by the interferon-gamma/STAT pathway. Nature. 397:710-713.