Pivotal roles of interleukin-6 in transmural inflammation in murine T cell transfer colitis

Journal of Leukocyte Biology

Volumn 76, Issue 6, 2004, Pages 1111-1117

  Kitamura, Kazuya ^a   Nakamoto, Yasunari ^a   Kaneko, Shuichi ^a   Mukaida, Naofumi ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

Animal model; Chemokine; Inflammatory bowel disease; Matrix metalloproteinase

Indexed keywords

CD4 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CX3C CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNITY; INFLAMMATION; INTESTINE FISTULA; INTESTINE STENOSIS; LYMPHOCYTE TRANSFER; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; MUCOSA INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; T LYMPHOCYTE; T LYMPHOCYTE TRANSFER COLITIS; WILD TYPE;

ANIMALS; ANTIGENS, CD45; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; COLITIS; CROHN DISEASE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION MEDIATORS; INTERLEUKIN-6; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; RECEPTORS, CHEMOKINE; UP-REGULATION;

ANIMALIA; MURINAE;

EID: 10044264634     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0604328     Document Type: Article

References (49)

1. Podolsky, D. K. (1991) Inflammatory bowel disease (first of two parts). N. Engl. J. Med. 325, 928-937.
2. Fiocchi, C. (1998) Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115, 182-205.
3. Elson, C. O., Sartor, R. B., Tennyson, G. S., Riddell, R. H. (1995) Experimental models of inflammatory bowel disease. Gastroenterology. 109, 1344-1367.
4. Mahida, Y. R., Kurlac, L., Gallagher, A., Hawkey, C. J. (1991) High circulating concentrations of interleukin-6 in active Crohn's disease but not ulcerative colitis. Gut 32, 1531-1534.
5. Gross, V., Andus, T., Caesar, I., Roth, M., Schölmerich, J. (1992) Evidence for continuous stimulation of interleukin-6 production in Crohn's disease. Gastroenterology 102, 514-519.
6. Rutgeeerts, P. (2002) A critical assessment of new therapies in inflammatory bowel disease. J. Gastroenterol. Hepatol. 17, S176-S185.
7. Targan, S. R., Hanauer, S. B., van Deventer, S. J. H., Mayer, L., Present, D. H., Braakman, T., DeWoody, K. L., Schaible, T. F., Rutgeerts, P. J. (1997) A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor α for Crohn's disease. N. Engl. J. Med. 337, 1029-1035.
8. Hanauer, S. B., Feagan, B. G., Lichienstein, G. R., Mayer, L. F., Schreiber, S., Colombel, J. F., Rachmilewitz, D., Wolf, D. C., Olson, A., Bao, W., Rutgeerts, P. (2002) Maintenance infliximab for Crohn's disease: the ACCENT I randomized trial. Lancet 359, 1541-1549.
9. Ito, H., Takazoe, M., Fukuda, Y., Hibi, T., Kusugami, K., Andoh, A., Matsumoto, T., Yamamura, T., Azuma, J., Nishimoto, N., Yoshizaki, K., Shimoyama, T., Kishimoto, T. (2004) A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease. Gastroenterology 126, 989-996.
10. Bhan, A. K., Mizoguchi, E., Smith, R. N., Mizoguchi, A. (1999) Colitis in transgenic and knockout animals as models of human inflammatory bowel disease. Immunol. Rev. 169, 195-207.
11. Boismenu, R., Chen, Y. (2000) Insights from mouse models of colitis. J. Leukoc. Biol. 67, 267-278.
12. + T cells. J. Exp. Med. 178, 237-244.
13. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5, 1461-1471.
14. + T cells. Immunity 1, 553-562.
15. + T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 179, 589-600.
16. + T cells. Am. J. Pathol. 148, 1503-1515.
17. Yamamoto, M., Yoshizaki, K., Kishimoto, T., Ito, H. (2000) IL-6 is required for the development of Th1 cell-mediated murine colitis. J. Immunol. 164, 4878-4882.
18. Atreya, R., Mudter, J., Finotto, S., Müllberg, J., Jostock, T., Wirtz, S., Schütz, M., Bartsch, B., Holtmann, M., Becker, C., Strand, D., Czaja, J., Schlaak, J. F., Lehr, H. A., Autschbach, F., Schurmann, G., Nishimoto, N., Yoshizaki, K., Ito, H., Kishimoto, T., Galle, P. R., Rose-John, S., Neurath, M. F. (2000) Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6, 583-588.
19. Suzuki, A., Hanada, T., Mitsuyama, K., Yoshida, T., Kamizono, S., Hoshino, T., Kubo, M., Yamashita, A., Okabe, M., Takeda, K., Akira, S., Matsumoto, S., Toyonaga, A., Sata, M., Yoshimura, A. (2001) C1S3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193, 471-481.
20. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., Köhler, G. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368, 339-342.
21. Natsume, M., Tsuji, H., Harada, A., Akiyama, M., Yano, T., Ishikura, H., Nakanishi, I., Matsushima, K., Kaneko, S., Mukaida, N. (1999) Attenuated liver fibrosis and depressed serum albumin levels in carbon tetrachloride-treated IL-6-deficient mice. J. Leukoc. Biol. 66, 601-608.
22. Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L., Powrie, F. (1999) An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190, 995-1003.
23. Kitamura, K., Nakamoto, Y., Akiyama, M., Fujii, C., Kondo, T., Kobayashi, K., Kaneko, S., Mukaida, N. (2002) Pathogenic roles of tumor necrosis factor receptor p55-mediated signals in dimethylnitrosamine-induced murine liver fibrosis. Lab. Invest. 82, 571-583.
24. Bregenholt, S., Claesson, M. H. (1998) Increased intracellular Th1 cytokines in scid mice with inflammatory bowel disease. Eur. J. Immunol. 28, 379-389.
25. Isaacs, K. L., Sartor, R. B., Haskill, S. (1992) Cytokine messenger RNA profiles in inflammatory bowel disease mucosa detected by polymerase chain reaction amplification. Gastroenterology 103, 1587-1595.
26. + T cells from IFN-γ knockout mice do not induce wasting disease. J. Autoimmun. 10, 455-459.
27. Simpson, S. J., Shah, S., Comiskey, M., de Jong, Y. P., Wang, B., Mizoguchi, E., Bhan, A. K., Terhorst, C. (1998) T cell-mediated pathology in two models of experimental colitis depends predominantly on the interleukin 12/signal transducer and activator of transcription (Stat)-4 pathway, but is not conditional on interferon γ expression by T cells. J. Exp. Med. 187, 1225-1234.
28. Diehl, S., Rincon, M. (2002) The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39, 531-536.
29. Samoilova, E. B., Horton, J. L., Hilliard, B., Liu, T. S. T., Chen, Y. (1998) IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J. Immunol. 161, 6480-6486.
30. + T helper cell 1 development in interleukin 6-deficient mice infected with Candida albicans. J. Exp. Med. 183, 1345-1355.
31. high T cells. Eur. J. Immunol. 31, 1465-1474.
32. Fort, M. M., Lesley, R., Davidson, N. J., Menon, S., Brombacher, F., Leach, M. W., Rennick, D. M. (2001) IL-4 exacerbates disease in a Th1 cell transfer model of colitis. J. Immunol. 166, 2793-2800.
33. Qin, S., Rottman, J. B., Myers, P., Kassam, N., Weinblatt, M., Loetscher, M., Koch, A. E., Moser, B., Mackay, C. R. (1998) The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101, 746-754.
34. Luther, S. A., Cyster, J. G. (2001) Chemokines as regulators of T cell differentiation. Nat. Immunol. 2, 102-107.
35. Annunziato, F., Cosmi, L., Galli, G., Beltrame, C., Romagnani, P., Manetti, R., Romagnani, S., Maggi, E. (1999) Assessment of chemokine receptor expression by human Th1 and Th2 cells in vitro and in vivo. J. Leukoc. Biol. 65, 691-699.
36. Romano, M., Sironi, M., Toniatti, C., Polentarutti, N., Fruscella, P., Ghezzi, P., Faggioni, R., Luini, W., van Hinsbergh, V., Sozzani, S., Bussolino, F., Poli, V., Ciliberto, G., Mantovani, A. (1997) Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6, 315-325.
37. Shaffer, A. L., Yu, X., He, Y., Boldrick, J., Chan, E. P., Staudt, L. M. (2000) BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13, 199-212.
38. Toney, L. M., Cattoretti, G., Graf, J. A., Merghoub, T., Pandolfi, P. P., Dalla-Favera, R., Ye, B. H., Dent, A. L. (2000) BCL-6 regulates chemokine gene transcription in macrophages. Nat. Immunol. 1, 214-220.
39. Podolsky, D. K. (1991) Inflammatory bowel disease (second of two parts). N. Engl. J. Med. 325, 1008-1016.
40. Present, D. H., Rutgeerts, P., Targan, S., Hanauer, S. B., Mayer, L., van Hogezand, R. A., Podolsky, D. K., Sands, B. E., Braakman, T., deWoody, K. L., Schaible, T. F., van Deventer, S. J. H. (1999) Infliximab for the treatment of fistulas in patients with Crohn's disease. N. Engl. J. Med. 340, 1398-1405.
41. Goetzl, E. J., Banda, M. J., Leppert, D. (1996) Martix metalloproteinases in immunity. J. Immunol. 156, 1-4.
42. Nagase, H., Woessner Jr., J. F. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494.
43. Pender, S. L. F., Tickle, S. P., Docherty, A. J. P., Howie, D., Wathen, N. C., MacDonald, T. T. (1997) A major role for matrix metalloproteinases in T cell injury in the gut. J. Immunol. 158, 1582-1590.
44. Baugh, M. D., Perry, M. J., Hollander, A. P., Davies, D. R., Cross, S. S., Lobo, A. J., Taylor, C. J., Evans, G. S. (1999) Matrix metalloproteinase levels are elevated in inflammatory bowel disease. Gastroenterology 117, 814-822.
45. von Lampe, B., Barthel, B., Coupland, S. E., Riecken, E. O., Rosewicz, S. (2000) Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease. Gut 47, 63-73.
46. Uthoff, S. M. S., Eichenberger, M. R., Lewis, R. K., Fox, M. P., Hamilton, C. J., Mcauliffe, T. L., Grimes, H. L., Galandiuk, S. (2001) Identification of candidate genes in ulcerative colitis and Crohn's disease using cDNA array technology. Int. J. Oncol. 19, 803-810.
47. Tarlton, J. F., Whiting, C. V., Tunmore, D., Bregenholt, S., Reimann, J., Claesson, M. H., Bland, P. W. (2000) The role of up-regulated serine proteinases and matrix metalloproteinases in the pathogenesis of a murine model of colitis. Am. J. Pathol. 157, 1927-1935.
48. Kusano, K., Miyaura, C., Inada, M., Tamura, T., Ito, A., Nagase, H., Kamoi, K., Suda, T. (1998) Regulation of matrix metalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology 139, 1338-1345.
49. Kossakowska, A. E., Edwards, D. R., Prusinkiewicz, C., Zhang, M. C., Guo, D., Urbanski, S. J., Grogan, T., Marquez, L. A., Janowska-Wieczorek, A. (1999) Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMPA) expression in malignant non-Hodgkin's lymphomas. Blood 94, 2080-2089.