γ δ T cell effector functions: A blend of innate programming and acquired plasticity

Nature Reviews Immunology

Volumn 10, Issue 7, 2010, Pages 467-478

  Bonneville, Marc ^a   O'Brien, Rebecca L ^b   Born, Willi K ^b  

^a INSERM   (France)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; LYMPHOCYTE ANTIGEN RECEPTOR; T LYMPHOCYTE RECEPTOR;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; B LYMPHOCYTE; CELL STRESS; CYTOKINE PRODUCTION; EFFECTOR CELL; GAMMA DELTA T LYMPHOCYTE; HOMEOSTASIS; HUMAN; INFECTION; INFLAMMATION; INNATE IMMUNITY; KINETICS; LYMPHOCYTE FUNCTION; NONHUMAN; PATHOPHYSIOLOGY; PLASTICITY; POLARIZATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; THYMUS; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; PHYSIOLOGICAL STRESS; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; INFECTION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COOPERATION; MICE; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTE SUBSETS;

EID: 77954143558     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2781     Document Type: Review

References (142)

1. Janeway, C. A. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
2. Gallucci, S., Lolkema, M. & Matzinger, P. Natural adjuvants: endogenous activators of dendritic cells. Nature Med. 5, 1249-1255 (1999).
3. Medzhitov, R. Origin and physiological roles of inflammation. Nature 454, 428-435 (2008).
4. Banchereau, J. & Steinman, R. M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
5. Bendelac, A., Bonneville, M. & Kearney, J. F. Autore activity by design: innate B and T lymphocytes. Nature Rev. Immunol. 1, 177-186 (2001).
6. Treiner, E. et al. Selection of evolutionary conserved mucosal-associated invariant T cells by MR 1. Nature 422, 164-169 (2003).
7. Hayday, A. C. yd T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196 (2009).
8. Chien, Y. H. & Konigshofer, Y. Antigen recognition by yS T cells. Immunol. Rev. 215, 46-58 (2007).
9. Sciammas, R. et al. Unique antigen recognition by a herpesvirus-specific TCR yS cell. J. Immunol. 152, 5392-5397 (1994).
10. Scotet, E. et al. Tumor recognition following Vy9VS2 T cell receptor interations with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity 22, 71-80 (2005).
11. Adams, E. J., Chien, Y. H. & Garcia, K. C. Structure of a yS T cell receptor in complex with the nonclassical MHC T22. Science 308, 227-231 (2005).
12. Aydintug, M. K., Roark, C. L, Chain, J. L, Born, W. K. & O'Brien, R. L. Macrophages express multiple ligands for yS TCRs. Mol. Immunol. 45, 3253-3263 (2008).
13. Constant, P. et al. Stimulation of human yS T cells by nonpeptidic mycobacterial antigens. Science 264, 267-270 (1994).
14. Tanaka, Y. et al. Natural and synthetic non-peptide antigens recognized by human yS T cells. Nature 375, 155-158 (1995).
15. Hintz, M. et al. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human yS T cells in Escherichia coli. FEBS Lett. 509, 317-322 (2001).
16. Halary, F et al. Shared reactivity of VS2-yS T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J. Exp. Med. 201, 1567-1578 (2005).
17. Thedrez, A. et al. Self/non-self discrimination by human yS T cells: simple solutions for a complex issue? Immunol. Rev. 215, 123-135 (2007).
18. Raulet, D. H. & Guerra, N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nature Rev. Immunol. 9, 568-578 (2009).
19. Viey, E. et al. Phosphostim-activated yS T cells kill autologous metastatic renal cell carcinoma. J. Immunol. 174, 1338-1347 (2005).
20. Corvaisier, M. et al. Vy9VS2 T cell response to colon carcinoma cells. J. Immunol. 175, 5481-5488 (2005).
21. Girardi, M. et al. Regulation of cutaneous malignancy by yS T cells. Science 294, 605-609 (2001).
22. Qin, G. et al. Phosphoantigen-expanded human y5 T cells display potent cytotoxicity against monocyte-derived macrophages infected with human and avian influenza viruses. J. Infect. Dis. 200, 858-865 (2009).
23. Strid, J. et al. Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nature Immunol. 9, 146-154 (2008).
24. + yS T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178, 4466-4472 (2007).
25. Martin, B., Hirota, K., Cua, D. J., Stockinger, B. & Veldhoen, M. Interleukin-17 producing yS T cells selectively expand in response to pathogen products and environmental signals. Immunity 31, 321-330 (2009).
26. Raulet, D. H. Interplay of natural killer cells and their receptors with the adaptive immune response. Nature Immunol. 5, 996-1002 (2004).
27. Zitvogel, L, Terme, M., Borg, C. & Trinchieri, G. Dendritic cell-NK cross-talk: regulation and physiopathology. Curr. Top. Microbiol. Immunol. 298, 157-174 (2006).
28. Brigl, M. & Brenner, M. B. CD 1: antigen presentation and T cell function. Annu. Rev. Immunol. 22, 817-890 (2004).
29. Devilder, M.-C. et al. Potentiation of antigen-stimulated Vy9V62 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J. Immunol. 176, 1386-1393 (2006).
30. Conti, L. et al. Reciprocal activating interactions between dendritic cells and pamidronate-stimulated yS T cells: role of CD86 and inflammatory cytokines. J. Immunol. 174, 252-260 (2005).
31. Devilder, M. C, Allain, S., Dousset, C, Bonneville, M. & Scotet, E. Early triggering of exclusive IFN-y responses of human Vy9V62 T cells by TLR-activated myeloid and plasmacytoid dendritic cells. J. Immunol. 183, 3625-3633 (2009).
32. Parker, C. M. et al. Evidence for extrathymic changes in the T cell receptor yS repertoire. J. Exp. Med. 171, 1597-1612 (1990).
33. Adams, E. J., Strop, P., Shin, S., Chien, Y H. & Garcia, K. C. An autonomous CDR36 is sufficient for recognition of the nonclassical MHC class I molecules T10 and T22 by yS T cells. Nature Immunol. 9, 777-784 (2008).
34. Dieli, F et al. Granulysin-dependent killing of intracellular and extracellular Mycobacterium tuberculosis by Vy9/V62 T lymphocytes. J. Infect. Dis. 184, 1082-1085 (2001).
35. Dudal, S. et al. Release of LL-37 by activated human Vy9V62 T cells: a microbicidal weapon against Brucella suis. J. Immunol. 177, 5533-5539 (2006).
36. Hamada, S. et al. IL-17A produced by yS T cells plays a critical role in innate immunity against Listeria monocytogenes infection in the liver. J. Immunol. 181, 3456-3463 (2008).
37. Jameson, J. & Havran, W. L. Skin yS T-cell functions in homeostasis and wound healing. Immunol. Rev. 215, 114-122 (2007).
38. O'Brien, R. L. et al. yS T cell receptors: functional correlations. Immunol. Rev. 215, 77-88 (2007).
39. Simonian, P. L. et al. IL-17A-expressing T cells are essential for bacterial clearance in a murine model of hypersensitivity pneumonitis. J. Immunol. 182, 6540-6549 (2009).
40. Gerber, D. J. et al. IL-4-producing yS T cells that express a very restricted TCR repertoire are preferentially localized in liver and spleen. J. Immunol. 163, 3076-3082 (1999).
41. Huber, S., Shi, C. & Budd, R. C. yS T cells promote a Th 1 response during coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J. Virol. 76, 6487-6494 (2002).
42. + pulmonary T cells regulate a(3 T cell-independent airway responsiveness. Proc. Natl Acad. Sci. USA 99, 8850-8855 (2002).
43. Roark, C. L. et al. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing yS T cells. J. Immunol. 179, 5576-5583 (2007).
44. Morita, C. T et al. Functionally distinct subsets of human yS T cells. Eur. J. Immunol. 21, 2999-3007 (1991).
45. Fenoglio, D. et al. yS T lymphocytes producing IFN-y and IL-17 are expanded in HIV-1-infected patients and respond to Candida albicans. Blood 113, 6611-6618 (2009).
46. Chen, L. et al. Epigenetic and transcriptional programs lead to default IFN-y production by yS T cells. J. Immunol. 178, 2730-2736 (2007).
47. + yS T cells in the absence of Itk results in elevated IgE production. Blood 114, 564-571 (2009).
48. O'Brien, R. L, Roark, C. L. & Born, W. K. IL-17-producing yS T cells. Eur. J. Immunol. 39, 662-666 (2009).
49. Kabelitz, D. & Wesch, D. Features and functions of yS T lymphocytes: focus on chemokines and their receptors. Crit. Rev. Immunol. 23, 339-370 (2003).
50. Haas, J. D. et al. CCR6 and NK1.1 distinguish between IL-17A and IFN-y-producing yS effector T cells. Eur. J. Immunol. 39, 3488-3497 (2009).
51. + yS regulatory T cells in the presence of antigen stimulation. J. Immunol. 183, 3574-3577 (2009).
52. Vermijlen, D. et al. Distinct cy to kin e-driven responses of activated blood yS T cells: insights into unconventional T cell pleiotropy. J. Immunol. 178, 4304-4314 (2007).
53. Havran, W. & Allison, J. P. Developmentally ordered appearance of thymocytes expressing different T cell antigen receptors. Nature 335, 443-445 (1988).
54. Lewis, J. et al. Selection of the cutaneous intraepithelial yS T cell repertoire by a thymic stromal element. Nature Immunol. 7, 843-850 (2006).
55. Xiong, N., Kang, C. & Raulet, D. H. Positive selection of dendritic epidermal yd T cell precursors in the fetal thymus determines expression of skin-homing receptors. Immunity 21, 121-131 (2004).
56. Boyden, L. M. et al. Skint 1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal yS T cells. Nature Genet. 40, 656-662 (2008).
57. Kreslavsky, T. et al. TCR-inducible PLZF transcription factor required for innate phenotype of a subset of yS T cells with restricted TCR diversity. Proc. Natl Acad. Sci. USA 106, 12453-12458 (2009).
58. Kovalovsky, D. et al. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nature Immunol. 9, 1055-1064 (2008).
59. Felices, M., Yin, C. C, Kosaka, Y., Kang, J. & Berg, L. J. Tec kinase Itk in yS T cells is pivotal for controlling IgE production in vivo. Proc. Natl Acad. Sci. USA 106, 8308-8313 (2009).
60. Nunez-Cruz, S. et al. LAT regulates yS T cell homeostasis and differentiation. Nature Immunol. 4, 999-1008 (2003).
61. -/- a(3 and yS T cells independently contribute to autoimmunity in Itchy mice. Blood 111, 4273-4282 (2008).
62. Jensen, K. D. C. et al. Thymic selection determines yS T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon y. Immunity 29, 90-100 (2008).
63. Ribot, J. C. et al. CD27 is a thymic determinant of the balance between interferon-y-and interleukin-17-producing yS T cell subsets. Nature Immunol. 10, 427-436 (2009).
64. Do, J.-S. et al. Cutting edge: spontaneous development of IL-17-producing yS T cells in the thymus occurs via a TGF-(31-dependent mechanism. J. Immunol. 184, 1675-1679 (2010).
65. Romani, L. et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451, 211-215 (2008).
66. Wesch, D., Glatzel, A. & Kabelitz, D. Differentiation of resting human peripheral blood yS T cells toward Th 1-or Th2-phenotype. Cell. Immunol. 212, 110-117 (2001).
67. Thedrez, A. et al. IL-21-mediated potentiation of antitumor cytolytic and proinflammatory responses of human Vy9VS2 T cells for adoptive immunotherapy. J. Immunol. 182, 3423-3431 (2009).
68. Dobmeyer, T. S. et al. Reciprocal alterations of Th1/Th2 function in yS T-cell subsets of human immunodeficiency virus-1-infected patients. Br. J. Haematol. 118, 282-288 (2002).
69. Li, B. et al. Disease-specific changes in yS T cell repertoire and function in patients with pulmonary tuberculosis. J. Immunol. 157, 4222-4229 (1996).
70. Rincon-Orozco, B. et al. Activation of Vy9V62 T cells by NKG2D. J. Immunol. 175, 2144-2151 (2005).
71. Jin, N. et al. Mismatched antigen prepares yS T cells for suppression of airway hyperresponsiveness. J. Immunol. 174, 2671-2679 (2005).
72. + dendritic cells enable the development of yS T cells that modulate airway hyperresponsiveness. J. Immunol. 181, 309-319 (2008).
73. Huang, Y et al. The influence of IgE-enhancing and IgE-suppressive yS T cell changes with exposure to inhaled ovalbumin. J. Immunol. 183, 849-855 (2009).
74. Duan, J., Chung, H., Troy, E. & Kasper, D. L. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing yS T cells. Cell Host Microbe 7, 140-150 (2010).
75. Peng, M. Y et al. Interleukin 17-producing yd T cells increased in patients with active pulmonary tuberculosis. Cell. Mol. Immunol. 5, 203-208 (2008).
76. Stark, M. A. et al. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294 (2005).
77. Braun, R. K. et al. IL-17 producing yS T cells are required for a controlled inflammatory response after bleomycin-induced lung injury. Inflammation 31, 167-179 (2008).
78. Carding, S. R. et al. Late dominance of the inflammatory process in murine influenza by yS T cells. J. Exp. Med. 172, 1225-1231 (1990).
79. Mombaerts, P., Arnoldi, J., Russ, F., Tonegawa, S. & Kaufmann, S. H. E. Different roles of a(3 and yS T cells in immunity against an intracellular bacterial pathogen. Nature 365, 53-56 (1993).
80. Fu, Y.-X. et al. Immune protection and control of inflammatory tissue necrosis by yS T cells. J. Immunol. 153, 3101-3115 (1994).
81. Dalton, J. E., Howell, G., Pearson, J., Scott, P. & Carding, S. R. Fas-Fas ligand interactions are essential for the binding to and killing of activated macrophages by yS T cells. J. Immunol. 173, 3660-3667 (2004).
82. Ito, Y. et al. yS T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum. 60, 2294-2303 (2009).
83. Shichita, T. et al. Pivotal role of cerebral interleukin-17-producing yS T cells in the delayed phase of ischemic brain injury. Nature Med. 15, 946-950 (2009).
84. Eberl, M. et al. A rapid crosstalk of human yS T cells and monocytes drives the acute inflammation in bacterial infections. PLoS Pathog. 5, e1000308 (2009).
85. + uveitogenic T cells. J. Immunol. 183, 560-567 (2009).
86. Brandes, M., Williman, K. & Moser, B. Professional antigen-presenting function by human yS T cells. Science 309, 264-268 (2005).
87. + a(3 T cell responses. Proc. Natl Acad. Sci. USA 106, 2307-2312 (2009).
88. Wu, Y et al. Human yS T cells: a lymphoid lineage capable of professional phagocytosis. J. Immunol. 183, 5622-5629 (2009).
89. Cheng, L. et al. Mouse yS T cells are capable of expressing MHC class II molecules, and of functioning as antigen-presenting cells. J. Neuroimmunol. 203, 3-11 (2008).
90. Koizumi, H. et al. Expression of perforin and serine esterases by human yS T cells. J. Exp. Med. 173, 499-502 (1991).
91. Mukasa, A., Lahn, M., Pflum, E. K., Born, W. & O' Brien, R. L. Evidence that the same yS T cells respond during infection-induced and autoimmune inflammation. J. Immunol. 159, 5787-5794 (1997).
92. high yS T cells in Lyme arthritis. J. Exp. Med. 184, 2109-2117 (1996).
93. + intraepithelial lymphocytes have attributes of regulatory cells in patients with celiac disease. J. Clin. Invest. 118, 281-293 (2008).
94. Ashour, H. M. & Niederkorn, J. Y yS T cells promote anterior chamber-associated immune deviation and immune priviledge through their production of IL-10. J. Immunol. 177, 8331-8337 (2006).
95. Peng, G. et al. Tumor-infiltrating yS T cells suppress T and dendritic cell function via mechanisms controlled by a unique Toll-like receptor signalling pathway. Immunity 27, 334-348 (2007).
96. + T cells in the lung of ovalbumin-sensitized and challenged mice. Immunol. Lett. 121, 87-92 (2008).
97. Wen, L. et al. Germinal center formation, immunoglobulin class switching, and autoantibody production driven by "non a(3" T cells. J. Exp. Med. 183, 2271-2282 (1996).
98. Pao, W. et al. yS T cell help of B cells is induced by repeated parasitic infection, in the absence of other T cells. Curr. Biol. 6, 1317-1325 (1996).
99. Zuany-Amorim, C. et al. Requirement for yS T cells in allergic airway inflammation. Science 280, 1265-1267 (1998).
100. McMenamin, C, Pimm, C, McKersey, M. & Holt, P. G. Regulation of IgE responses to inhaled antigen in mice by antigen-specific yS T cells. Science 265, 1869-1871 (1994).
101. Mizoguchi, A. et al. Role of the CD5 molecule on TCR yS T cell-mediated immune functions: development of germinal centers and chronic intestinal inflammation. Int. Immunol. 15, 97-108 (2003).
102. Brandes, M. et al. Flexible migration program regulates yS T-cell involvement in humoral immunity. Blood 102, 3693-3701 (2003).
103. Komano, H. et al. Homeostatic regulation of intestinal epithelia by intraepithelial yS T cells. Proc. Natl Acad. Sci. USA 92, 6147-6151 (1995).
104. Yang, H., Antony, P. A., Wildhaber, B. E. & Teitelbaum, D. H. Intestinal intraepithelial lymphocyte yS-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J. Immunol. 172, 4151-4158 (2004).
105. Chen, Y., Chou, K., Fuchs, E., Havran, W. L. & Boismenu, R. Protection of the intestinal mucosa by intraepithelial yS T cells. Proc. Natl Acad. Sci. USA 99, 14338-14343 (2002).
106. Inagaki-Ohara, K. et al. Mucosal T cells bearing TCR yS play a protective role in intestinal inflammation. J. Immunol. 173, 1390-1398 (2004).
107. Tsuchiya, T et al. Role of yS T cells in the inflammatory response of experimental colitis mice. J. Immunol. 171, 5507-5513 (2003).
108. Inagaki-Ohara, K., Sawaguchi, A., Suganuma, T, Matsusaki, G. & Nawa, Y. Intraepithelial lymphocytes express junctional molecules in murine small intestine. Biochem. Biophys. Res. Comm. 331, 977-983 (2005).
109. Roberts, S. J. et al. T-cell a(3 and yS deficient mice display abnormal but distinct phenotypes toward a natural, widespread infection of the intestinal epithelium. Proc. Natl Acad. Sci. USA 93, 11774-11779 (1996).
110. Jameson, J. M., Cauvi, G., Witherden, D. A. & Havran, W. L. A keratinocyte-responsive yS TCR is necessary for dendritic epidermal T cell activation by damaged keratinocytes and maintenance in the epidermis. J. Immunol. 172, 3573-3579 (2004).
111. Jameson, J. M., Cauvi, G., Sharp, L. L, Witherden, D. A. & Havran, W L. yS T cell-induced hyaluronan production by epithelial cells regulates inflammation. J. Exp. Med. 201, 1269-1279 (2005).
112. Toulon, A. et al. A role for human skin-resident T cells in wound healing. J. Exp. Med. 206, 743-750 (2009).
113. Li, Z., Burns, A. R., Rumbaut, R. E. & Smith, C. W. yS T cells are necessary for platelet and neutrophil accumulation in limbal vessels and efficient epithelial repair after corneal abrasion. Am. J. Pathol. 171, 838-845 (2007).
114. King, D. P. et al. Cutting edge: protective response to pulmonary injury requires yS T lymphocytes. J. Immunol. 162, 5033-5036 (1999).
115. Heyborne, K. D., Cranfill, R. L., Carding, S. R., Born, W K. & O'Brien, R. L. Characterization of yS T lymphocytes at the maternal-fetal interface. J. Immunol. 149, 2872-2878 (1992).
116. Reardon, C. et al. Expression of yS T cell receptors on lymphocytes from the lactating mammary gland. J. Exp. Med. 172, 1263-1266 (1990).
117. Miyazaki, K. et al. Gene expression profiling of peripheral T cell lymphoma including yS T cell lymphoma. Blood 113, 1071-1074 (2008).
118. Bonneville, M. & Scotet, E. Human Vy9V52 T cells: promising new leads for immunotherapy of infections and tumors. Curr. Opin. Immunol. 18, 539-546 (2007).
119. Sicard, H. et al. In vivo immunomanipulation of Vy9V52 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. J. Immunol. 175, 5471-5480 (2005).
120. Huang, D. et al. Antigen-specific Vy2V52 T effector cells confer homeostatic protection against pneumonic plaque lesions. Proc. Natl Acad. Sci. USA 106, 7553-7558 (2009).
121. Wilhelm, M. et al. yS T cells for immune therapy of patients with lymphoid malignancies. Blood 102, 200-206 (2003).
122. Dieli, F et al. Targeting human yS T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67, 7450-7457 (2008).
123. Zarski, J. P. et al. Repeated administration of IPH1101 in monotherapy or combined with low dose IL-2 in patients chronically infected with hepatitis C virus: efficacy, safety and immuno-biology results from a phase 2 study. Hepatology Abstr. 50, 1031A (2009).
124. Gertner-Dardenne, J. et al. Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood 113, 4875-4884 (2009).
125. Laurent, G. et al. Phase I/II study of IPH1101 (BrHPP), a Vy9V52 T cell agonist, combined with Rituximab in low grade follicular lymphoma patients\interim data. Blood Abstr. 114, 658A (2009).
126. + CD4-CD8-T lymphocytes in AIDS patients with disseminated Mycobacterium avium-intracellulare complex infection. J. Infect. Dis. 174, 969-976 (1996).
127. Dechanet, J. et al. Implication of yS T cells in the human immune response to cytomegalovirus. J. Clin. Invest. 103, 1437-1449 (1999).
128. Tonegawa, S. et al. Diversity, development, ligands, and probable functions of yS T cells. Cold Spring Harb. Symp. Quant. Biol. 54, 31-44 (1989).
129. Raulet, D. H. The structure, function and molecular genetics of the human yS T cell receptor. Annu. Rev Immunol. 7, 175-207 (1989).
130. Heilig, J. S. & Tonegawa, S. Diversity of murine y genes and expression in fetal and adult T lymphocytes. Nature 322, 836-840 (1986).
131. Lefranc, M. P. & Rabbitts, T. H. A nomenclature to fit the organization of the human T-cell receptor y and 6 genes. Res. Immunol. 141, 615-618 (1990).
132. Mossmann, T R. & Coffman, R. L. Th 1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7, 145-173 (1989).
133. Dong, C. Th 17 cells in development: an updated view of their molecular identity and genetic programming. Nature Rev. Immunol. 8, 337-348 (2008).
134. King, C. New insights into the differentiation and function of T follicular helper cells. Nature Rev Immunol. 9, 757-766 (2009).
135. + T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J. Immunol. 165, 4174-4181 (2000).
136. H2 cytokines, and airway inflammation. J. Immunol. 172, 2894-2902 (2004).
137. Matsubara, S. et al. Vy 1 + T cells and tumor necrosis factor-a in ozone-induced airway hyperresponsiveness. Am. J. Respir. Cell. Mol. Biol. 40, 454-463 (2009).
138. Jin, N. et al. Airway hyperresponsiveness through synergy of yS T cells and NKT cells. J. Immunol. 179, 2961-2968 (2007).
139. + yS T cells have proinflammatory and antiviral effects in viral lung disease. J. Immunol. 182, 1174-1181 (2009).
140. Welte, T. et al. Role of two distinct yS T cell subsets during West Nile virus infection. FEMS Immunol. Med. Microbiol. 53, 275-283 (2008).
141. Shiohara, T., Moriya, N., Hayakawa, J., Itohara, S. & Ishikawa, H. Resistance to cutaneous graft-vs-host disease is not induced in T cell receptor 8 gene-mutant mice. J. Exp. Med. 183, 1483-1489 (1996).
142. Wu, H. et al. Depletion of yS T cells exacerbates murine adriamycin nephropathy. J. Am. Soc. Nephrol. 18, 1180-1189 (2007).