Thymic Selection Determines γδ T Cell Effector Fate: Antigen-Naive Cells Make Interleukin-17 and Antigen-Experienced Cells Make Interferon γ

Immunity

Volumn 29, Issue 1, 2008, Pages 90-100

  Jensen, Kirk D C ^a   Su, Xiaoqin ^a   Shin, Sunny ^a   Li, Luke ^a   Youssef, Sawsan ^a   Yamasaki, Sho ^b   Steinman, Lawrence ^a   Saito, Takashi ^b   Locksley, Richard M ^c   Davis, Mark M ^a   Baumgarth, Nicole ^d   Chien, Yueh hsiu ^a  

^a STANFORD UNIVERSITY   (United States)

^b RIKEN Center for Integrative Medical Sciences   (Japan)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

CD38 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELL MATURATION; CELL SELECTION; DELTA GAMMA T CELL; EFFECTOR CELL; IMMUNIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THYMUS; VDJ EXON;

ANIMALS; ANTIGENS; ANTIGENS, SURFACE; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; INTERFERON TYPE II; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; THYMUS GLAND;

EID: 46749113368     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.04.022     Document Type: Article

References (60)

1. Adams E.J., Chien Y.H., and Garcia K.C. Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 308 (2005) 227-231
2. Azzam H.S., Grinberg A., Lui K., Shen H., Shores E.W., and Love P.E. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188 (1998) 2301-2311
3. Baccala R., Witherden D., Gonzalez-Quintial R., Dummer W., Surh C.D., Havran W.L., and Theofilopoulos A.N. Gamma delta T cell homeostasis is controlled by IL-7 and IL-15 together with subset-specific factors. J. Immunol. 174 (2005) 4606-4612
4. Bettelli E., Oukka M., and Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8 (2007) 345-350
5. Bonneville M., Ishida I., Itohara S., Verbeek S., Berns A., Kanagawa O., Haas W., and Tonegawa S. Self-tolerance to transgenic gamma delta T cells by intrathymic inactivation. Nature 344 (1990) 163-165
6. Crowley M.P. Characterization of the Ligand Recognition Properties and Function of a Gamma/Delta T cell Receptor and Ligand Pair (1998), Stanford University, Stanford, CA
7. Crowley M.P., Fahrer A.M., Baumgarth N., Hampl J., Gutgemann I., Teyton L., and Chien Y. A population of murine gammadelta T cells that recognize an inducible MHC class Ib molecule. Science 287 (2000) 314-316
8. De Paoli P., Gennari D., Martelli P., Cavarzerani V., Comoretto R., and Santini G. Gamma delta T cell receptor-bearing lymphocytes during Epstein-Barr virus infection. J. Infect. Dis. 161 (1990) 1013-1016
9. Dent A.L., Matis L.A., Hooshmand F., Widacki S.M., Bluestone J.A., and Hedrick S.M. Self-reactive gamma delta T cells are eliminated in the thymus. Nature 343 (1990) 714-719
10. Fahrer A.M., Konigshofer Y., Kerr E.M., Ghandour G., Mack D.H., Davis M.M., and Chien Y.H. Attributes of gammadelta intraepithelial lymphocytes as suggested by their transcriptional profile. Proc. Natl. Acad. Sci. USA 98 (2001) 10261-10266
11. Ferrick D.A., Schrenzel M.D., Mulvania T., Hsieh B., Ferlin W.G., and Lepper H. Differential production of interferon-gamma and interleukin-4 in response to Th1- and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 373 (1995) 255-257
12. Forster R., Schubel A., Breitfeld D., Kremmer E., Renner-Muller I., Wolf E., and Lipp M. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99 (1999) 23-33
13. French J.D., Roark C.L., Born W.K., and O'Brien R.L. {gamma{delta} T cell homeostasis is established in competition with {alpha}{beta}T cells and NK cells. Proc. Natl. Acad. Sci. USA 102 (2005) 14741-14746
14. Haks M.C., Lefebvre J.M., Lauritsen J.P., Carleton M., Rhodes M., Miyazaki T., Kappes D.J., and Wiest D.L. Attenuation of gammadeltaTCR signaling efficiently diverts thymocytes to the alphabeta lineage. Immunity 22 (2005) 595-606
15. Hanke T., Mitnacht R., Boyd R., and Hunig T. Induction of interleukin 2 receptor beta chain expression by self-recognition in the thymus. J. Exp. Med. 180 (1994) 1629-1636
16. Havran W.L., and Allison J.P. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335 (1988) 443-445
17. Havran W.L., Chien Y.H., and Allison J.P. Recognition of self antigens by skin-derived T cells with invariant gamma delta antigen receptors. Science 252 (1991) 1430-1432
18. Hayes S.M., Li L., and Love P.E. TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity 22 (2005) 583-593
19. Hayes S.M., and Love P.E. A retrospective on the requirements for gammadelta T-cell development. Immunol. Rev. 215 (2007) 8-14
20. Hayes S.M., Shores E.W., and Love P.E. An architectural perspective on signaling by the pre-, alphabeta and gammadelta T cell receptors. Immunol. Rev. 191 (2003) 28-37
21. Ho M., Webster H.K., Tongtawe P., Pattanapanyasat K., and Weidanz W.P. Increased gamma delta T cells in acute Plasmodium falciparum malaria. Immunol. Lett. 25 (1990) 139-141
22. Huseby E.S., White J., Crawford F., Vass T., Becker D., Pinilla C., Marrack P., and Kappler J.W. How the T cell repertoire becomes peptide and MHC specific. Cell 122 (2005) 247-260
23. Ito K., Van Kaer L., Bonneville M., Hsu S., Murphy D.B., and Tonegawa S. Recognition of the product of a novel MHC TL region gene (27b) by a mouse gamma delta T cell receptor. Cell 62 (1990) 549-561
24. Jason J., Buchanan I., Archibald L.K., Nwanyanwu O.C., Bell M., Green T.A., Eick A., Han A., Razsi D., Kazembe P.N., et al. Natural T, gammadelta, and NK cells in mycobacterial, Salmonella, and human immunodeficiency virus infections. J. Infect. Dis. 182 (2000) 474-481
25. King D.P., Hyde D.M., Jackson K.A., Novosad D.M., Ellis T.N., Putney L., Stovall M.Y., Van Winkle L.S., Beaman B.L., and Ferrick D.A. Cutting edge: Protective response to pulmonary injury requires gamma delta T lymphocytes. J. Immunol. 162 (1999) 5033-5036
26. Koohsari H., Tamaoka M., Campbell H.R., and Martin J.G. The role of gamma delta T cells in airway epithelial injury and bronchial responsiveness after chlorine gas exposure in mice. Respir. Res. 8 (2007) 21
27. Lefrancois L., and Goodman T. In vivo modulation of cytolytic activity and Thy-1 expression in TCR-gamma delta+ intraepithelial lymphocytes. Science 243 (1989) 1716-1718
28. Lewis J.M., Girardi M., Roberts S.J., Barbee S.D., Hayday A.C., and Tigelaar R.E. Selection of the cutaneous intraepithelial gammadelta+ T cell repertoire by a thymic stromal determinant. Nat. Immunol. 7 (2006) 843-850
29. Ley K., Smith E., and Stark M.A. IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol. Res. 34 (2006) 229-242
30. 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. 177 (2006) 4662-4669
31. Mallick-Wood C.A., Lewis J.M., Richie L.I., Owen M.J., Tigelaar R.E., and Hayday A.C. Conservation of T cell receptor conformation in epidermal gammadelta cells with disrupted primary Vgamma gene usage. Science 279 (1998) 1729-1733
32. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V., Allende M.L., Proia R.L., and Cyster J.G. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427 (2004) 355-360
33. Moore T.A., Moore B.B., Newstead M.W., and Standiford T.J. Gamma delta-T cells are critical for survival and early proinflammatory cytokine gene expression during murine Klebsiella pneumonia. J. Immunol. 165 (2000) 2643-2650
34. Pereira P., Zijlstra M., McMaster J., Loring J.M., Jaenisch R., and Tonegawa S. Blockade of transgenic gamma delta T cell development in beta 2-microglobulin deficient mice. EMBO J. 11 (1992) 25-31
35. 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. 7 (2006) 995-1003
36. 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. 179 (2007) 5576-5583
37. Romani L., Fallarino F., De Luca A., Montagnoli C., D'Angelo C., Zelante T., Vacca C., Bistoni F., Fioretti M.C., Grohmann U., et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451 (2008) 211-215
38. Schild H., Mavaddat N., Litzenberger C., Ehrich E.W., Davis M.M., Bluestone J.A., Matis L., Draper R.K., and Chien Y.H. The nature of major histocompatibility complex recognition by gamma delta T cells. Cell 76 (1994) 29-37
39. Schweighoffer E., and Fowlkes B.J. Positive selection is not required for thymic maturation of transgenic gamma delta T cells. J. Exp. Med. 183 (1996) 2033-2041
40. Sciammas R., and Bluestone J.A. HSV-1 glycoprotein I-reactive TCR gamma delta cells directly recognize the peptide backbone in a conformationally dependent manner. J. Immunol. 161 (1998) 5187-5192
41. Serwold T., Hochedlinger K., Inlay M.A., Jaenisch R., and Weissman I.L. Early TCR expression and aberrant T cell development in mice with endogenous prerearranged T cell receptor genes. J. Immunol. 179 (2007) 928-938
42. 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. 178 (2007) 4466-4472
43. Shin S., El-Diwany R., Schaffert S., Adams E.J., Garcia K.C., Pereira P., and Chien Y.H. Antigen recognition determinants of gammadelta T cell receptors. Science 308 (2005) 252-255
44. Shires J., Theodoridis E., and Hayday A.C. Biological insights into TCRgammadelta+ and TCRalphabeta+ intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity 15 (2001) 419-434
45. 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. 29 (1999) 4060-4071
46. 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 22 (2005) 285-294
47. Stetson D.B., Mohrs M., Reinhardt R.L., Baron J.L., Wang Z.E., Gapin L., Kronenberg M., and Locksley R.M. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198 (2003) 1069-1076
48. Tarakhovsky A., Kanner S.B., Hombach J., Ledbetter J.A., Muller W., Killeen N., and Rajewsky K. A role for CD5 in TCR-mediated signal transduction and thymocyte selection. Science 269 (1995) 535-537
49. Toth B., Alexander M., Daniel T., Chaudry I.H., Hubbard W.J., and Schwacha M.G. The role of gammadelta T cells in the regulation of neutrophil-mediated tissue damage after thermal injury. J. Leukoc. Biol. 76 (2004) 545-552
50. Tough D.F., and Sprent J. Lifespan of gamma/delta T cells. J. Exp. Med. 187 (1998) 357-365
51. Umemura M., Yahagi A., Hamada S., Begum M.D., Watanabe H., Kawakami K., Suda T., Sudo K., Nakae S., Iwakura Y., and Matsuzaki G. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178 (2007) 3786-3796
52. Van Laethem F., Sarafova S.D., Park J.H., Tai X., Pobezinsky L., Guinter T.I., Adoro S., Adams A., Sharrow S.O., Feigenbaum L., and Singer A. Deletion of CD4 and CD8 coreceptors permits generation of alphabeta T cells that recognize antigens independently of the MHC. Immunity 27 (2007) 735-750
53. 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 24 (2006) 677-688
54. Weintraub B.C., Jackson M.R., and Hedrick S.M. Gamma delta T cells can recognize nonclassical MHC in the absence of conventional antigenic peptides. J. Immunol. 153 (1994) 3051-3058
55. Wells F.B., Gahm S.J., Hedrick S.M., Bluestone J.A., Dent A., and Matis L.A. Requirement for positive selection of gamma delta receptor-bearing T cells. Science 253 (1991) 903-905
56. Wucherpfennig K.W., Newcombe J., Li H., Keddy C., Cuzner M.L., and Hafler D.A. Gamma delta T-cell receptor repertoire in acute multiple sclerosis lesions. Proc. Natl. Acad. Sci. USA 89 (1992) 4588-4592
57. Xiong N., Kang C., and Raulet D.H. Positive selection of dendritic epidermal gammadelta T cell precursors in the fetal thymus determines expression of skin-homing receptors. Immunity 21 (2004) 121-131
58. Yamasaki S., Ishikawa E., Sakuma M., Ogata K., Sakata-Sogawa K., Hiroshima M., Wiest D.L., Tokunaga M., and Saito T. Mechanistic basis of pre-T cell receptor-mediated autonomous signaling critical for thymocyte development. Nat. Immunol. 7 (2006) 67-75
59. Yoshimura A., Longmore G., and Lodish H.F. Point mutation in the exoplasmic domain of the erythropoietin receptor resulting in hormone-independent activation and tumorigenicity. Nature 348 (1990) 647-649
60. Zuany-Amorim C., Ruffie C., Haile S., Vargaftig B.B., Pereira P., and Pretolani M. Requirement for gammadelta T cells in allergic airway inflammation. Science 280 (1998) 1265-1267