ICOS promotes IL-17 synthesis in colonic intraepithelial lymphocytes in IL-10-/- mice

Journal of Leukocyte Biology

Volumn 87, Issue 2, 2010, Pages 301-308

  Schaefer, Jeremy S ^a   Montufar Solis, Dina ^a   Vigneswaran, Nadarajah ^a   Klein, John R ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Cytokines; Inflammation; Knockout; Mucosa; Rodent

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; INDUCIBLE COSTIMULATORY MOLECULE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 23; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL POPULATION; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTERITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FLOW CYTOMETRY; GRANULOCYTE; IMMUNOSTIMULATION; IN VIVO STUDY; INFLAMMATION; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; STAINING; TH17 CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD80; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COLON; GENE EXPRESSION REGULATION; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-17; INTESTINAL MUCOSA; LECTINS, C-TYPE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT;

MUS; RODENTIA;

EID: 76149097491     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0409238     Document Type: Article

References (47)

1. Fiorentino, D. F., Bond, M. W., Mosmann, T. R. (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med. 170, 2081-2095.
2. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., Muller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274.
3. Donnelly, R. P., Dickensheets, H., Finbloom, D. S. (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J. Interferon Cytokine Res. 19, 563-573.
4. Strober, W., Fuss, I. J., Blumberg, R. S. (2002) The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20, 495-549.
5. Rouvier, E., Luciani, M. F., Mattei, M. G., Denizot, F., Golstein, P. (1993) CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J. Immunol. 150, 5445-5456.
6. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., Stockinger, B. (2006) TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189.
7. Korn, T., Bettelli, E., Gao, W., Awasthi, A., Jager, A., Strom, T. B., Oukka, M., Kuchroo, V. K. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448, 484-487.
8. Nurieva, R., Yang, X. O., Martinez, G., Zhang, Y., Panopoulos, A. D., Ma, L., Schluns, K., Tian, Q., Watowich, S. S., Jetten, A. M., Dong, C. (2007) Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448, 480-483.
9. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R., Weaver, C. T. (2006) Transforming growth factor-β induces development of the T(H)17 lineage. Nature 441, 231-234.
10. Chen, Z., O'Shea, J. J. (2008) Regulation of IL-17 production in human lymphocytes. Cytokine 41, 71-78.
11. Koenders, M. I., Joosten, L. A., van den Berg, W. B. (2006) Potential new targets in arthritis therapy: interleukin (IL)-17 and its relation to tumor necrosis factor and IL-1 in experimental arthritis. Ann. Rheum. Dis. 65 (Suppl. 3), iii29-iii33.
12. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y., Hood, L., Zhu, Z., Tian, Q., Dong, C. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141.
13. Fujino, S., Andoh, A., Bamba, S., Ogawa, A., Hata, K., Araki, Y., Bamba, T., Fujiyama, Y. (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52, 65-70.
14. Koenders, M. I., Lubberts, E., van de Loo, F. A., Oppers-Walgreen, B., van den Bersselaar, L., Helsen, M. M., Kolls, J. K., Di Padova, F. E., Joosten, L. A., van den Berg, W. B. (2006) Interleukin-17 acts independently of TNF-α under arthritic conditions. J. Immunol. 176, 6262-6269.
15. Montufar-Solis, D., Schaefer, J., Hicks, M. J., Klein, J. R. (2008) Massive but selective cytokine dysregulation in the colon of IL-10-/- mice revealed by multiplex analysis. Int. Immunol. 20, 141-154.
16. Hue, S., Ahern, P., Buonocore, S., Kullberg, M. C., Cua, D. J., McKenzie, B. S., Powrie, F., Maloy, K. J. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
17. Duerr, R. H., Taylor, K. D., Brant, S. R., Rioux, J. D., Silverberg, M. S., Daly, M. J., Steinhart, A. H., Abraham, C., Regueiro, M., Griffiths, A., Dassopoulos, T., Bitton, A., Yang, H., Targan, S., Datta, L. W., Kistner, E. O., Schumm, L. P., Lee, A. T., Gregersen, P. K., Barmada, M. M., Rotter, J. I., Nicolae, D. L., Cho, J. H. (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314, 1461-1463.
18. Leppkes, M., Becker, C., Ivanov, I. I., Hirth, S., Wirtz, S., Neufert, C., Pouly, S., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Becher, B., Littman, D. R., Neurath, M. F. (2009) RORγ-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 136, 257-267.
19. Sato, T., Kanai, T., Watanabe, M., Sakuraba, A., Okamoto, S., Nakai, T., Okazawa, A., Inoue, N., Totsuka, T., Yamazaki, M., Kroczek, R. A., Fukushima, T., Ishii, H., Hibi, T. (2004) Hyperexpression of inducible costimulator and its contribution on lamina propria T cells in inflammatory bowel disease. Gastroenterology 126, 829-839.
20. Hutloff, A., Dittrich, A. M., Beier, K. C., Eljaschewitsch, B., Kraft, R., Anagnostopoulos, I., Kroczek, R. A. (1999) ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 397, 263-266.
21. Dong, C., Juedes, A. E., Temann, U. A., Shresta, S., Allison, J. P., Ruddle, N. H., Flavell, R. A. (2001) ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409, 97-101.
22. McAdam, A. J., Chang, T. T., Lumelsky, A. E., Greenfield, E. A., Boussiotis, V. A., Duke-Cohan, J. S., Chernova, T., Malenkovich, N., Jabs, C., Kuchroo, V. K., Ling, V., Collins, M., Sharpe, A. H., Freeman, G. J. (2000) Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. J. Immunol. 165, 5035-5040.
23. Nurieva, R. I., Treuting, P., Duong, J., Flavell, R. A., Dong, C. (2003) Inducible costimulator is essential for collagen-induced arthritis. J. Clin. Invest. 111, 701-706.
24. Nurieva, R. I. (2005) Regulation of immune and autoimmune responses by ICOS-B7h interaction. Clin. Immunol. 115, 19-25.
25. Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J., Littman, D. R. (2006) The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133.
26. Elliott, D. E., Metwali, A., Leung, J., Setiawan, T., Blum, A. M., Ince, M. N., Bazzone, L. E., Stadecker, M. J., Urban Jr., J. F., Weinstock, J. V. (2008) Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J. Immunol. 181, 2414-2419.
27. Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N., Schuler, G. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92.
28. Montufar-Solis, D., Garza, T., Teng, B. B., Klein, J. R. (2006) Upregulation of ICOS on CD43+ CD4+ murine small intestinal intraepithelial lymphocytes during acute reovirus infection. Biochem. Biophys. Res. Commun. 342, 782-790.
29. Montufar-Solis, D., Wang, H. C., Klein, J. R. (2007) Stimulatory and costimulatory effects of IL-18 directed to different small intestinal CD43 T cell subsets. J. Leukoc. Biol. 82, 1166-1173.
30. -△△CT method. Methods 25, 402-408.
31. Nelson, A. J., Dunn, R. J., Peach, R., Aruffo, A., Farr, A. G. (1996) The murine homolog of human Ep-CAM, a homotypic adhesion molecule, is expressed by thymocytes and thymic epithelial cells. Eur. J. Immunol. 26, 401-408.
32. Farr, A., Nelson, A., Truex, J., Hosier, S. (1991) Epithelial heterogeneity in the murine thymus: a cell surface glycoprotein expressed by subcapsular and medullary epithelium. J. Histochem. Cytochem. 39, 645-653.
33. Totsuka, T., Kanai, T., Iiyama, R., Uraushihara, K., Yamazaki, M., Okamoto, R., Hibi, T., Tezuka, K., Azuma, M., Akiba, H., Yagita, H., Okumura, K., Watanabe, M. (2003) Ameliorating effect of anti-inducible costimulator monoclonal antibody in a murine model of chronic colitis. Gastroenterology 124, 410-421.
34. Nancey, S., Holvoet, S., Graber, I., Joubert, G., Philippe, D., Martin, S., Nicolas, J. F., Desreumaux, P., Flourie, B., Kaiserlian, D. (2006) CD8+ cytotoxic T cells induce relapsing colitis in normal mice. Gastroenterology 131, 485-496.
35. Tajima, M., Wakita, D., Noguchi, D., Chamoto, K., Yue, Z., Fugo, K., Ishigame, H., Iwakura, Y., Kitamura, H., Nishimura, T. (2008) IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J. Exp. Med. 205, 1019-1027.
36. De Jong, Y. P., Rietdijk, S. T., Faubion, W. A., Abadia-Molina, A. C., Clarke, K., Mizoguchi, E., Tian, J., Delaney, T., Manning, S., Gutierrez-Ramos, J. C., Bhan, A. K., Coyle, A. J., Terhorst, C. (2004) Blocking inducible co-stimulator in the absence of CD28 impairs Th1 and CD25+ regulatory T cells in murine colitis. Int. Immunol. 16, 205-213.
37. Pot, C., Jin, H., Awasthi, A., Liu, S. M., Lai, C. Y., Madan, R., Sharpe, A. H., Karp, C. L., Miaw, S. C., Ho, I. C., Kuchroo, V. K. (2009) Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J. Immunol. 183, 797-801.
38. Nakayama, T., Kasprowicz, D. J., Yamashita, M., Schubert, L. A., Gillard, G., Kimura, M., Didierlaurent, A., Koseki, H., Ziegler, S. F. (2002) The generation of mature, single-positive thymocytes in vivo is dysregulated by CD69 blockade or overexpression. J. Immunol. 168, 87-94.
39. Rosen, H., Sanna, M. G., Cahalan, S. M., Gonzalez-Cabrera, P. J. (2007) Tipping the gatekeeper: S1P regulation of endothelial barrier function. Trends Immunol. 28, 102-107.
40. Feng, C., Woodside, K. J., Vance, B. A., El-Khoury, D., Canelles, M., Lee, J., Gress, R., Fowlkes, B. J., Shores, E. W., Love, P. E. (2002) A potential role for CD69 in thymocyte emigration. Int. Immunol. 14, 535-544.
41. Aranda, R., Sydora, B. C., McAllister, P. L., Binder, S. W., Yang, H. Y., Targan, S. R., Kronenberg, M. (1997) Analysis of intestinal lymphocytes in mouse colitis mediated by transfer of CD4+, CD45RBhigh T cells to SCID recipients. J. Immunol. 158, 3464-3473.
42. Bagriacik, E. U., Okabe, M., Klein, J. R. (2000) Origins of intestinal intraepithelial lymphocytes: direct evidence for a thymus-derived γ δ T cell component. Immunol. Lett. 75, 77-83.
43. Lefrancois, L. (1991) Phenotypic complexity of intraepithelial lymphocytes of the small intestine. J. Immunol. 147, 1746-1751.
44. Bagriacik, E. U., Armstrong, M. D., Okabe, M., Klein, J. R. (1999) Differential expression of CD43 isoforms on murine T cells and their relationship to acute intestinal graft versus host disease: studies using enhancedgreen fluorescent protein transgenic mice. Int. Immunol. 11, 1651-1662.
45. Ibraghimov, A. R., Lynch, R. G. (1994) Heterogeneity and biased T cell receptor α/β repertoire of mucosal CD8+ cells from murine large intestine: implications for functional state. J. Exp. Med. 180, 433-444.
46. Klein, J. R. (2004) T-cell activation in the curious world of the intestinal intraepithelial lymphocyte. Immunol. Res. 30, 327-337.
47. Montufar-Solis, D., Garza, T., Klein, J. R. (2007) T-cell activation in the intestinal mucosa. Immunol. Rev. 215, 189-201.