In vitro-induced Th17 cells fail to induce inflammation in vivo and show an impaired migration into inflamed sites

European Journal of Immunology

Volumn 40, Issue 4, 2010, Pages 1089-1098

  Janke, Marko ^a   Peine, Michael ^a   Nass, Alexia ^b   Morawietz, Lars ^b   Hamann, Alf ^b   Scheffold, Alexander ^a,c  

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MILTENYI BIOTEC GMBH   (Germany)

Author keywords

Cell migration; Inflammation; Th17 cells

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; INTERLEUKIN 23; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH17 CELL;

ADOPTIVE TRANSFER; ANIMALS; ARTHRITIS, EXPERIMENTAL; CELLS, CULTURED; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; HYPERSENSITIVITY, DELAYED; IMMUNIZATION; INTERLEUKIN-17; INTERLEUKIN-23; INTERLEUKIN-6; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, SCID; MICE, TRANSGENIC; OSTEOARTHRITIS, KNEE; OVALBUMIN; PEPTIDE FRAGMENTS; RECEPTORS, CXCR3; T-LYMPHOCYTES, HELPER-INDUCER; TRANSFORMING GROWTH FACTOR BETA;

EID: 77951050922     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939487     Document Type: Article

References (49)

1. Chen, Y., Langrish, C. L., McKenzie, B., Joyce-Shaikh, B., Stumhofer, J. S., McClanahan, T., Blumenschein, W. et al., Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 2006. 116: 1317-1326.
2. Yen, D., Cheung, J., Scheerens, H., Poulet, F., McClanahan, T., McKenzie, B., Kleinschek, M. A. et al., IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 2006. 116: 1310-1316.
3. Ouyang,W., Kolls, J. K. and Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008. 28: 454-467. (Pubitemid 351471762)
4. Iwakura, Y., Nakae, S., Saijo, S. and Ishigame, H., The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev. 2008. 226: 57-79.
5. Sato, K., Suematsu, A., Okamoto, K., Yamaguchi, A., Morishita, Y., Kadono, Y., Tanaka, S. et al., Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J. Exp. Med. 2006. 203: 2673-2682.
6. Fouser, L. A., Wright, J. F., Dunussi-Joannopoulos, K. and Collins, M., Th17 cytokines and their emerging roles in inflammation and autoimmunity. Immunol. Rev. 2008. 226: 87-102.
7. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B., TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006. 24: 179-189. (Pubitemid 43214587)
8. Harrington, L. E., Mangan, P. R. andWeaver, C. T., Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr. Opin. Immunol. 2006. 18: 349-356.
9. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D. et al., Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006. 441: 231-234.
10. Kimura, A., Naka, T. and Kishimoto, T., IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA 2007. 104: 12099-12104.
11. Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A. and Sallusto, F., Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007. 8: 942-949.
12. Yang, X. O., Pappu, B. P., Nurieva, R., Akimzhanov, A., Kang, H. S., Chung, Y., Ma, L. et al., T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008. 28: 29-39.
13. Weaver, C. T., Harrington, L. E., Mangan, P. R., Gavrieli, M. and Murphy, K. M., Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 2006. 24: 677-688. (Pubitemid 43867371)
14. Austrup, F., Vestweber, D., Borges, E., Lohning, M., Brauer, R., Herz, U., Renz, H. et al., P- and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflammed tissues. Nature 1997. 385: 81-83. (Pubitemid 27024558)
15. Ebert, L. M., Schaerli, P. and Moser, B., Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol. Immunol. 2005. 42: 799-809.
16. von Andrian, U. H. and Mackay, C. R., T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 2000. 343: 1020-1034.
17. - phenotype. J. Immunol. 2007. 178: 7525-7529.
18. Acosta-Rodriguez, E. V., Rivino, L., Geginat, J., Jarrossay, D., Gattorno, M., Lanzavecchia, A., Sallusto, F. and Napolitani, G., Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 2007. 8: 639-646.
19. Irmler, I. M., Gajda, M. and Brauer, R., Exacerbation of antigen-induced arthritis in IFN-gamma-deficient mice as a result of unrestricted IL-17 response. J. Immunol. 2007. 179: 6228-6236.
20. Chu, C. Q., Swart, D., Alcorn, D., Tocker, J. and Elkon, K. B., Interferon-gamma regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum. 2007. 56: 1145-1151. (Pubitemid 46608639)
21. Nakae, S., Komiyama, Y., Nambu, A., Sudo, K., Iwase, M., Homma, I., Sekikawa, K. et al., Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002. 17: 375-387. (Pubitemid 35279557)
22. McGeachy, M. J., Bak-Jensen, K. S., Chen, Y., Tato, C. M., Blumenschein, W., McClanahan, T. and Cua, D. J., TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 2007. 8: 1390-1397.
23. Stumhofer, J. S., Silver, J. S., Laurence, A., Porrett, P. M., Harris, T. H., Turka, L. A., Ernst, M. et al., Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 2007. 8: 1363-1371.
24. Fitzgerald, D. C., Zhang, G. X., El-Behi, M., Fonseca-Kelly, Z., Li, H., Yu, S., Saris, C. J. et al., Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 2007. 8: 1372-1379.
25. Yang, Y., Weiner, J., Liu, Y., Smith, A. J., Huss, D. J., Winger, R., Peng, H. et al., T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J. Exp. Med. 2009. 206: 1549-1564.
26. Butcher, E. C. and Ford W. L., Following cellular traffic: methods of labelling lymphocytes and other cells to trace their migration in vivo, in Weir, D. M. (Ed.) Handbook of Experimental Immunology, Blackwell Scientific Publications, Oxford 1986, pp 57.51-57.23.
27. Siegmund, K. a. H., A., Use of labelled lymphocytes to analyze trafficking in vivo, in Hamann, A. a. E., B. (Ed.) Leukocyte Trafficking, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 2005, pp. 497-508.
28. Furuzawa-Carballeda, J., Vargas-Rojas, M. I. and Cabral, A. R., Autoimmune inflammation from the Th17 perspective. Autoimmun. Rev. 2007. 6: 169-175.
29. Wilson, N. J., Boniface, K., Chan, J. R., McKenzie, B. S., Blumenschein, W. M., Mattson, J. D., Basham, B. et al., Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 2007. 8: 950-957.
30. Hoyer, K. K., Kuswanto, W. F., Gallo, E. and Abbas, A. K., Distinct roles of helper T-cell subsets in a systemic autoimmune disease. Blood 2009. 113: 389-395.
31. Stockinger, B. and Veldhoen, M., Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 2007. 19: 281-286.
32. Paunovic, V., Carroll, H. P., Vandenbroeck, K. and Gadina, M., Signalling, inflammation and arthritis: crossed signals: the role of interleukin (IL)-12, -17, -23 and -27 in autoimmunity. Rheumatology (Oxford) 2008. 47: 771-776.
33. Miossec, P., Interleukin-17 in fashion, at last: ten years after its description, its cellular source has been identified. Arthritis Rheum. 2007. 56: 2111-2115. (Pubitemid 47173557)
34. He, D., Wu, L., Kim, H. K., Li, H., Elmets, C. A. and Xu, H., CD8+IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J. Immunol. 2006. 177: 6852-6858. (Pubitemid 44715050)
35. Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E. and Trifilieff, A., IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 2003. 170: 2106-2112. (Pubitemid 36197433)
36. Song, C., Luo, L., Lei, Z., Li, B., Liang, Z., Liu, G., Li, D. et al., IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J. Immunol. 2008. 181: 6117-6124.
37. Wong, P. K., Quinn, J. M., Sims, N. A., van Nieuwenhuijze, A., Campbell, I. K. and Wicks, I. P., Interleukin-6 modulates production of T lymphocyte-derived cytokines in antigen-induced arthritis and drives inflammation-induced osteoclastogenesis. Arthritis Rheum. 2006. 54: 158-168.
38. Hamilton, J. A., Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 2008. 8: 533-544.
39. Yamamura, T., Interleukin 17-producing T-helper cells and autoimmune diseases: time for a paradigm shift? Curr. Rheumatol. Rep. 2007. 9: 93-95.
40. Mills, K. H., Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 2008. 38: 2636-2649.
41. Lexberg, M. H., Taubner, A., Forster, A., Albrecht, I., Richter, A., Kamradt, T., Radbruch, A. and Chang, H. D., Th memory for interleukin-17 expression is stable in vivo. Eur. J. Immunol. 2008. 38: 2654-2664.
42. Shi, G., Cox, C. A., Vistica, B. P., Tan, C., Wawrousek, E. F. and Gery, I., Phenotype switching by inflammation-inducing polarized Th17 cells, but not by Th1 cells. J. Immunol. 2008. 181: 7205-7213.
43. Stummvoll, G. H., DiPaolo, R. J., Huter, E. N., Davidson, T. S., Glass, D., Ward, J. M. and Shevach, E. M., Th1, Th2, and Th17 effector T cell-induced autoimmune gastritis differs in pathological pattern and in susceptibility to suppression by regulatory T cells. J. Immunol. 2008. 181: 1908-1916.
44. Bending, D., De La Pena, H., Veldhoen, M., Phillips, J. M., Uyttenhove, C., Stockinger, B. and Cooke, A., Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 2009. 119: 565-572.
45. Cox, C. A., Shi, G., Yin, H., Vistica, B. P., Wawrousek, E. F., Chan, C. C. and Gery, I., Both Th1 and Th17 are immunopathogenic but differ in other key biological activities. J. Immunol. 2008. 180: 7414-7422.
46. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T. et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005. 201: 233-240.
47. Yamazaki, T., Yang, X. O., Chung, Y., Fukunaga, A., Nurieva, R., Pappu, B., Martin-Orozco, N. et al., CCR6 regulates the migration of inflammatory and regulatory T cells. J. Immunol. 2008. 181: 8391-8401.
48. Hirota, K., Yoshitomi, H., Hashimoto, M., Maeda, S., Teradaira, S., Sugimoto, N., Yamaguchi, T. et al., Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J. Exp. Med. 2007. 204: 2803-2812.
49. Pichavant, M., Goya, S., Meyer, E. H., Johnston, R. A., Kim, H. Y., Matangkasombut, P., Zhu, M. et al., Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 2008. 205: 385-393.