Innate immunity

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CCR6 and NK1.1 distinguish between IL-17A and IFN-γ-producing γδ effector T cells

  1. Jan D. Haas1,
  2. Frano H. Malinarich González1,2,
  3. Susanne Schmitz1,
  4. Vijaykumar Chennupati1,
  5. Lisa Föhse1,
  6. Elisabeth Kremmer3,
  7. Reinhold Förster1,
  8. Immo Prinz1,*

Article first published online: 14 OCT 2009

DOI: 10.1002/eji.200939922

Issue

European Journal of Immunology

European Journal of Immunology

Volume 39, Issue 12, pages 3488–3497, December 2009

Additional Information

How to Cite

Haas, J. D., González, F. H. M., Schmitz, S., Chennupati, V., Föhse, L., Kremmer, E., Förster, R. and Prinz, I. (2009), CCR6 and NK1.1 distinguish between IL-17A and IFN-γ-producing γδ effector T cells. Eur. J. Immunol., 39: 3488–3497. doi: 10.1002/eji.200939922

Author Information

  1. 1

    Hannover Medical School, Institute for Immunology, Hannover, Germany

  2. 2

    Disciplinary Program of Immunology, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Santiago, Chile

  3. 3

    Institute of Molecular Immunology, Helmholtz Center Munich, Munich, Germany

*Hannover Medical School, Institute for Immunology, Carl-Neuberg-Str. 1, 30625 Hannover, Germany Fax: +49-5115329722

Publication History

  1. Issue published online: 1 DEC 2009
  2. Article first published online: 14 OCT 2009
  3. Manuscript Accepted: 8 SEP 2009
  4. Manuscript Received: 21 AUG 2009

Funded by

  • Deutsche Forschungsgemeinschaft. Grant Numbers: PR727/2-1, SFB621-A14

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References

  • 1
    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.
  • 2
    O'Brien, R. L., Roark, C. L. and Born, W. K., IL-17-producing gammadelta T cells. Eur. J. Immunol. 2009. 39: 662–666.
  • 3
    Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S. and Ley, K., Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005. 22: 285–294.
  • 4
    Shibata, K., Yamada, H., Hara, H., Kishihara, K. and Yoshikai, Y., Resident Vdelta1+gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 2007. 178: 4466–4472.
  • 5
    Peng, M. Y., Wang, Z. H., Yao, C. Y., Jiang, L. N., Jin, Q. L., Wang, J. and Li, B. Q., Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell Mol. Immunol. 2008. 5: 203–208.
  • 6
    Romani, L., Fallarino, F., De Luca, A., Montagnoli, C., D'Angelo, C., Zelante, T., Vacca, C. et al., Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 2008. 451: 211–215.
  • 7
    Lockhart, E., Green, A. M. and Flynn, J. L., IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 2006. 177: 4662–4669.
  • 8
    Hamada, S., Umemura, M., Shiono, T., Tanaka, K., Yahagi, A., Begum, M. D., Oshiro, K. et al., IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J. Immunol. 2008. 181: 3456–3463.
  • 9
    Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K., Suda, T. et al., IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 2007. 178: 3786–3796.
  • 10
    Roark, C. L., French, J. D., Taylor, M. A., Bendele, A. M., Born, W. K. and O'Brien, R. L., Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J. Immunol. 2007. 179: 5576–5583.
  • 11
    Simonian, P. L., Roark, C. L., Diaz del Valle, F., Palmer, B. E., Douglas, I. S., Ikuta, K., Born, W. K. et al., Regulatory role of gammadelta T cells in the recruitment of CD4+and CD8+ T cells to lung and subsequent pulmonary fibrosis. J. Immunol. 2006. 177: 4436–4443.
  • 12
    Spahn, T. W., Issazadah, S., Salvin, A. J. and Weiner, H. L., Decreased severity of myelin oligodendrocyte glycoprotein peptide 33 - 35-induced experimental autoimmune encephalomyelitis in mice with a disrupted TCR delta chain gene. Eur. J. Immunol. 1999. 29: 4060–4071.
  • 13
    Wohler, J. E., Smith, S. S., Zinn, K. R., Bullard, D. C. and Barnum, S. R., Gammadelta T cells in EAE: early trafficking events and cytokine requirements. Eur. J. Immunol. 2009. 39: 1516–1526.
  • 14
    Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L. and Kuchroo, V. K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006. 441: 235–238.
  • 15
    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. et al., Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006. 441: 231–234.
  • 16
    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.
  • 17
    Jensen, K. D., Su, X., Shin, S., Li, L., Youssef, S., Yamasaki, S., Steinman, L. et al., Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 2008. 29: 90–100.
  • 18
    Shibata, K., Yamada, H., Nakamura, R., Sun, X., Itsumi, M. and Yoshikai, Y., Identification of CD25+gamma delta T cells as fetal thymus-derived naturally occurring IL-17 producers. J. Immunol. 2008. 181: 5940–5947.
  • 19
    Ribot, J. C., deBarros, A., Pang, D. J., Neves, J. F., Peperzak, V., Roberts, S. J., Girardi, M. et al., CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat. Immunol. 2009. 10: 427–436.
  • 20
    Kisielow, J., Kopf, M. and Karjalainen, K., SCART scavenger receptors identify a novel subset of adult gammadelta T cells. J. Immunol. 2008. 181: 1710–1716.
  • 21
    Jensen, K. D. and Chien, Y. H., Thymic maturation determines gammadelta T cell function, but not their antigen specificities. Curr. Opin. Immunol. 2009. 21: 140–145.
  • 22
    Deknuydt, F., Scotet, E. and Bonneville, M., Review modulation of inflammation through IL-17 production by gammadelta T cells: mandatory in the mouse, dispensable in humans? Immunol. Lett. 2009.
  • 23
    Prinz, I., Sansoni, A., Kissenpfennig, A., Ardouin, L., Malissen, M. and Malissen, B., Visualization of the earliest steps of gammadelta T cell development in the adult thymus. Nat. Immunol. 2006. 7: 995–1003.
  • 24
    Passoni, L., Hoffman, E. S., Kim, S., Crompton, T., Pao, W., Dong, M. Q., Owen, M. J. and Hayday, A. C., Intrathymic delta selection events in gammadelta cell development. Immunity 1997. 7: 83–95.
  • 25
    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.
  • 26
    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.
  • 27
    Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E. et al., Phenotypic and functional features of human Th17 cells. J. Exp. Med. 2007. 204: 1849–1861.
  • 28
    Wurbel, M. A., Malissen, M., Guy-Grand, D., Meffre, E., Nussenzweig, M. C., Richelme, M., Carrier, A. and Malissen, B., Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 2001. 98: 2626–2632.
  • 29
    Jensen, K. D., Shin, S. and Chien, Y. H., Cutting edge: Gammadelta intraepithelial lymphocytes of the small intestine are not biased toward thymic antigens. J. Immunol. 2009. 182: 7348–7351.
  • 30
    Roark, C. L., Simonian, P. L., Fontenot, A. P., Born, W. K. and O'Brien, R. L., gammadelta T cells: an important source of IL-17. Curr. Opin. Immunol. 2008. 20: 353–357.
  • 31
    Qureshi, M. H., Zhang, T., Koguchi, Y., Nakashima, K., Okamura, H., Kurimoto, M. and Kawakami, K., Combined effects of IL-12 and IL-18 on the clinical course and local cytokine production in murine pulmonary infection with Cryptococcus neoformans. Eur. J. Immunol. 1999. 29: 643–649.
  • 32
    Laurence, A., Tato, C. M., Davidson, T. S., Kanno, Y., Chen, Z., Yao, Z., Blank, R. B. et al., Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007. 26: 371–381.
  • 33
    Stewart, C. A., Walzer, T., Robbins, S. H., Malissen, B., Vivier, E. and Prinz, I., Germ-line and rearranged Tcrd transcription distinguish bona fide NK cells and NK-like gammadelta T cells. Eur. J. Immunol. 2007. 37: 1442–1452.
  • 34
    Ley, K., Smith, E. and Stark, M. A., IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol. Res. 2006. 34: 229–242.
  • 35
    Reboldi, A., Coisne, C., Baumjohann, D., Benvenuto, F., Bottinelli, D., Lira, S., Uccelli, A. et al., C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009. 10: 514–523.
  • 36
    Azuara, V., Lembezat, M. P. and Pereira, P., The homogeneity of the TCRdelta repertoire expressed by the Thy-1dull gammadelta T cell population is due to cellular selection. Eur. J. Immunol. 1998. 28: 3456–3467.
  • 37
    Azuara, V., Levraud, J. P., Lembezat, M. P. and Pereira, P., A novel subset of adult gamma delta thymocytes that secretes a distinct pattern of cytokines and expresses a very restricted T cell receptor repertoire. Eur. J. Immunol. 1997. 27: 544–553.
  • 38
    Vicari, A. P., Mocci, S., Openshaw, P., O'Garra, A. and Zlotnik, A., Mouse gamma delta TCR+NK1.1+thymocytes specifically produce interleukin-4, are major histocompatibility complex class I independent, and are developmentally related to alpha beta TCR+NK1.1+thymocytes. Eur. J. Immunol. 1996. 26: 1424–1429.
  • 39
    Lees, R. K., Ferrero, I. and MacDonald, H. R., Tissue-specific segregation of TCRgamma delta+NKT cells according to phenotype TCR repertoire and activation status: parallels with TCR alphabeta+NKT cells. Eur. J. Immunol. 2001. 31: 2901–2909.
  • 40
    Koenecke, C., Chennupati, V., Schmitz, S., Malissen, B., Forster, R. and Prinz, I., In vivo application of mAb directed against the gammadelta TCR does not deplete but generates “invisible” gammadelta T cells. Eur. J. Immunol. 2009. 39: 372–379.
  • 41
    Rachitskaya, A. V., Hansen, A. M., Horai, R., Li, Z., Villasmil, R., Luger, D., Nussenblatt, R. B. and Caspi, R. R., Cutting Edge: NKT Cells Constitutively Express IL-23 Receptor and RORgammat and Rapidly Produce IL-17 upon Receptor Ligation in an IL-6-Independent Fashion. J. Immunol. 2008. 180: 5167–5171.
  • 42
    Coquet, J. M., Chakravarti, S., Kyparissoudis, K., McNab, F. W., Pitt, L. A., McKenzie, B. S., Berzins, S. P. et al., Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc. Natl. Acad. Sci. USA 2008. 105: 11287–11292.
  • 43
    Lee, K. A., Kang, M. H., Lee, Y. S., Kim, Y. J., Kim, D. H., Ko, H. J. and Kang, C. Y., A distinct subset of natural killer T cells produces IL-17, contributing to airway infiltration of neutrophils but not to airway hyperreactivity. Cell. Immunol. 2008. 251: 50–55.
  • 44
    Kreslavsky, T., Savage, A. K., Hobbs, R., Gounari, F., Bronson, R., Pereira, P., Pandolfi, P. P. et al., TCR-inducible PLZF transcription factor required for innate phenotype of a subset of gammadelta T cells with restricted TCR diversity. Proc. Natl. Acad. Sci. USA 2009. 106: 12453–12458.
  • 45
    Martin, B., Hirota, K., Cua, D. J., Stockinger, B. and Veldhoen, M., Interleukin-17-Producing gammadelta T Cells Selectively Expand in Response to Pathogen Products and Environmental Signals. Immunity 2009. 31: 321–330.
  • 46
    Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C. and Mills, K. H., Interleukin-1 and IL-23 Induce Innate IL-17 Production from gammadelta T Cells, Amplifying Th17 Responses and Autoimmunity. Immunity 2009. 31: 331–341.
  • 47
    Bendelac, A., Bonneville, M. and Kearney, J. F., Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 2001. 1: 177–186.
  • 48
    Pabst, O., Ohl, L., Wendland, M., Wurbel, M. A., Kremmer, E., Malissen, B. and Forster, R., Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine. J. Exp. Med. 2004. 199: 411–416.
  • 49
    Prinz, I., Klemm, U., Kaufmann, S. H. and Steinhoff, U., Exacerbated colitis associated with elevated levels of activated CD4+T cells in TCRalpha chain transgenic mice. Gastroenterology 2004. 126: 170–181.
  • 50
    Ceredig, R. and Rolink, T., A positive look at double-negative thymocytes. Nat. Rev. Immunol. 2002. 2: 888–897.
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