Development of Interleukin-17-Producing γδ T Cells Is Restricted to a Functional Embryonic Wave

Immunity

Volumn 37, Issue 1, 2012, Pages 48-59

  Haas, Jan D ^a   Ravens, Sarina ^a,d   Düber, Sandra ^b   Sandrock, Inga ^a   Oberdörfer, Linda ^a   Kashani, Elham ^a   Chennupati, Vijaykumar ^a,e   Föhse, Lisa ^a   Naumann, Ronald ^c   Weiss, Siegfried ^b   Krueger, Andreas ^a   Förster, Reinhold ^a   Prinz, Immo ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; T LYMPHOCYTE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO DEVELOPMENT; GAMMA DELTA T LYMPHOCYTE; LYMPHOID CELL; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; THYMUS;

ANIMALS; ANTIGENS, CD27; BONE MARROW; CHIMERISM; HOMEOSTASIS; IMMUNITY, INNATE; INTERLEUKIN-17; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, CCR6; T-LYMPHOCYTE SUBSETS; THYMOCYTES; THYMUS GLAND;

EID: 84864325431     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.06.003     Document Type: Article

References (69)

1. Asarnow D.M., Kuziel W.A., Bonyhadi M., Tigelaar R.E., Tucker P.W., Allison J.P. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell 1988, 55:837-847.
2. Asarnow D.M., Goodman T., LeFrancois L., Allison J.P. Distinct antigen receptor repertoires of two classes of murine epithelium-associated T cells. Nature 1989, 341:60-62.
3. Benlagha K., Wei D.G., Veiga J., Teyton L., Bendelac A. Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 2005, 202:485-492.
4. Bonneville M., O'Brien R.L., Born W.K. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 2010, 10:467-478.
5. Buonocore S., Ahern P.P., Uhlig H.H., Ivanov I.I., Littman D.R., Maloy K.J., Powrie F. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010, 464:1371-1375.
6. Caccamo N., La Mendola C., Orlando V., Meraviglia S., Todaro M., Stassi G., Sireci G., Fournié J.J., Dieli F. Differentiation, phenotype, and function of interleukin-17-producing human Vγ9Vδ2 T cells. Blood 2011, 118:129-138.
7. Carding S.R., Egan P.J. Gammadelta T cells: functional plasticity and heterogeneity. Nat. Rev. Immunol. 2002, 2:336-345.
8. Chennupati V., Worbs T., Liu X., Malinarich F.H., Schmitz S., Haas J.D., Malissen B., Förster R., Prinz I. Intra- and intercompartmental movement of gammadelta T cells: intestinal intraepithelial and peripheral gammadelta T cells represent exclusive nonoverlapping populations with distinct migration characteristics. J. Immunol. 2010, 185:5160-5168.
9. Cho J.S., Pietras E.M., Garcia N.C., Ramos R.I., Farzam D.M., Monroe H.R., Magorien J.E., Blauvelt A., Kolls J.K., Cheung A.L., et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 2010, 120:1762-1773.
10. Cua D.J., Tato C.M. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 2010, 10:479-489.
11. Cui Y., Shao H., Lan C., Nian H., O'Brien R.L., Born W.K., Kaplan H.J., Sun D. Major role of gamma delta T cells in the generation of IL-17+ uveitogenic T cells. J. Immunol. 2009, 183:560-567.
12. DeBarros A., Chaves-Ferreira M., d'Orey F., Ribot J.C., Silva-Santos B. CD70-CD27 interactions provide survival and proliferative signals that regulate T cell receptor-driven activation of human γδ peripheral blood lymphocytes. Eur. J. Immunol. 2011, 41:195-201.
13. Deknuydt F., Scotet E., Bonneville M. Modulation of inflammation through IL-17 production by gammadelta T cells: mandatory in the mouse, dispensable in humans?. Immunol. Lett. 2009, 127:8-12.
14. Do J.S., Fink P.J., Li L., Spolski R., Robinson J., Leonard W.J., Letterio J.J., Min B. Cutting edge: spontaneous development of IL-17-producing gamma delta T cells in the thymus occurs via a TGF-beta 1-dependent mechanism. J. Immunol. 2010, 184:1675-1679.
15. Düber S., Hafner M., Krey M., Lienenklaus S., Roy B., Hobeika E., Reth M., Buch T., Waisman A., Kretschmer K., Weiss S. Induction of B-cell development in adult mice reveals the ability of bone marrow to produce B-1a cells. Blood 2009, 114:4960-4967.
16. Dudakov J.A., Hanash A.M., Jenq R.R., Young L.F., Ghosh A., Singer N.V., West M.L., Smith O.M., Holland A.M., Tsai J.J., et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science 2012, 336:91-95.
17. Dunon D., Courtois D., Vainio O., Six A., Chen C.H., Cooper M.D., Dangy J.P., Imhof B.A. Ontogeny of the immune system: gamma/delta and alpha/beta T cells migrate from thymus to the periphery in alternating waves. J. Exp. Med. 1997, 186:977-988.
18. Gerber D.J., Azuara V., Levraud J.P., Huang S.Y., Lembezat M.P., Pereira P. IL-4-producing gamma delta T cells that express a very restricted TCR repertoire are preferentially localized in liver and spleen. J. Immunol. 1999, 163:3076-3082.
19. Gray E.E., Suzuki K., Cyster J.G. Cutting edge: Identification of a motile IL-17-producing gammadelta T cell population in the dermis. J. Immunol. 2011, 186:6091-6095.
20. Grigoriadou K., Boucontet L., Pereira P. Most IL-4-producing gamma delta thymocytes of adult mice originate from fetal precursors. J. Immunol. 2003, 171:2413-2420.
21. Haas J.D., González F.H., Schmitz S., Chennupati V., Föhse L., Kremmer E., Förster R., Prinz I. CCR6 and NK1.1 distinguish between IL-17A and IFN-gamma-producing gammadelta effector T cells. Eur. J. Immunol. 2009, 39:3488-3497.
22. Hamada S., Umemura M., Shiono T., Tanaka K., Yahagi A., Begum M.D., Oshiro K., Okamoto Y., Watanabe H., Kawakami 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.
23. Hameyer D., Loonstra A., Eshkind L., Schmitt S., Antunes C., Groen A., Bindels E., Jonkers J., Krimpenfort P., Meuwissen R., et al. Toxicity of ligand-dependent Cre recombinases and generation of a conditional Cre deleter mouse allowing mosaic recombination in peripheral tissues. Physiol. Genomics 2007, 31:32-41.
24. Havran W.L., Allison J.P. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 1988, 335:443-445.
25. Hayday A.C. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 2009, 31:184-196.
26. Hirota K., Duarte J.H., Veldhoen M., Hornsby E., Li Y., Cua D.J., Ahlfors H., Wilhelm C., Tolaini M., Menzel U., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 2011, 12:255-263.
27. Ishigame H., Kakuta S., Nagai T., Kadoki M., Nambu A., Komiyama Y., Fujikado N., Tanahashi Y., Akitsu A., Kotaki H., et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30:108-119.
28. Itohara S., Farr A.G., Lafaille J.J., Bonneville M., Takagaki Y., Haas W., Tonegawa S. Homing of a gamma delta thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature 1990, 343:754-757.
29. Iwakura Y., Ishigame H., Saijo S., Nakae S. Functional specialization of interleukin-17 family members. Immunity 2011, 34:149-162.
30. Jensen K.D., Chien Y.H. Thymic maturation determines gammadelta T cell function, but not their antigen specificities. Curr. Opin. Immunol. 2009, 21:140-145.
31. Jensen K.D., Su X., Shin S., Li L., Youssef S., Yamasaki S., Steinman L., Saito T., Locksley R.M., Davis M.M., 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.
32. Jensen K.D., Shin S., Chien Y.H. Cutting edge: Gammadelta intraepithelial lymphocytes of the small intestine are not biased toward thymic antigens. J. Immunol. 2009, 182:7348-7351.
33. Kisielow J., Kopf M., Karjalainen K. SCART scavenger receptors identify a novel subset of adult gammadelta T cells. J. Immunol. 2008, 181:1710-1716.
34. Laird R.M., Laky K., Hayes S.M. Unexpected role for the B cell-specific Src family kinase B lymphoid kinase in the development of IL-17-producing γδ T cells. J. Immunol. 2010, 185:6518-6527.
35. Lalor S.J., Dungan L.S., Sutton C.E., Basdeo S.A., Fletcher J.M., Mills K.H. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gammadelta and CD4 T cells that mediate autoimmunity. J. Immunol. 2011, 186:5738-5748.
36. Lambolez F., Arcangeli M.L., Joret A.M., Pasqualetto V., Cordier C., Di Santo J.P., Rocha B., Ezine S. The thymus exports long-lived fully committed T cell precursors that can colonize primary lymphoid organs. Nat. Immunol. 2006, 7:76-82.
37. Lewis J.M., Girardi M., Roberts S.J., Barbee S.D., Hayday A.C., Tigelaar R.E. Selection of the cutaneous intraepithelial gammadelta+ T cell repertoire by a thymic stromal determinant. Nat. Immunol. 2006, 7:843-850.
38. Lockhart E., Green A.M., 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.
39. Ma Y., Aymeric L., Locher C., Mattarollo S.R., Delahaye N.F., Pereira P., Boucontet L., Apetoh L., Ghiringhelli F., Casares N., et al. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J. Exp. Med. 2011, 208:491-503.
40. Malinarich F.H., Grabski E., Worbs T., Chennupati V., Haas J.D., Schmitz S., Candia E., Quera R., Malissen B., Förster R., et al. Constant TCR triggering suggests that the TCR expressed on intestinal intraepithelial γδ T cells is functional in vivo. Eur. J. Immunol. 2010, 40:3378-3388.
41. Marks B.R., Nowyhed H.N., Choi J.Y., Poholek A.C., Odegard J.M., Flavell R.A., Craft J. Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nat. Immunol. 2009, 10:1125-1132.
42. Mills K.H. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 2008, 38:2636-2649.
43. Moens E., Brouwer M., Dimova T., Goldman M., Willems F., Vermijlen D. IL-23R and TCR signaling drives the generation of neonatal Vgamma9Vdelta2 T cells expressing high levels of cytotoxic mediators and producing IFN-gamma and IL-17. J. Leukoc. Biol. 2011, 89:743-752.
44. Muranski P., Borman Z.A., Kerkar S.P., Klebanoff C.A., Ji Y., Sanchez-Perez L., Sukumar M., Reger R.N., Yu Z., Kern S.J., et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 2011, 35:972-985.
45. Murdoch J.R., Lloyd C.M. Resolution of allergic airway inflammation and airway hyperreactivity is mediated by IL-17-producing gammadeltaT cells. Am. J. Respir. Crit. Care Med. 2010, 182:464-476.
46. Narayan K., Sylvia K.E., Malhotra N., Yin C.C., Martens G., Vallerskog T., Kornfeld H., Xiong N., Cohen N.R., Brenner M.B., et al. Intrathymic programming of effector fates in three molecularly distinct γδ T cell subtypes. Nat. Immunol. 2012, 13:511-518. Immunological Genome Project Consortium.
47. Ness-Schwickerath K.J., Jin C., Morita C.T. Cytokine requirements for the differentiation and expansion of IL-17A- and IL-22-producing human Vgamma2Vdelta2 T cells. J. Immunol. 2010, 184:7268-7280.
48. O'Brien R.L., Roark C.L., Born W.K. IL-17-producing gammadelta T cells. Eur. J. Immunol. 2009, 39:662-666.
49. Peng M.Y., Wang Z.H., Yao C.Y., Jiang L.N., Jin Q.L., Wang J., Li B.Q. Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell. Mol. Immunol. 2008, 5:203-208.
50. Petermann F., Rothhammer V., Claussen M.C., Haas J.D., Blanco L.R., Heink S., Prinz I., Hemmer B., Kuchroo V.K., Oukka M., Korn T. γδ T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity 2010, 33:351-363.
51. Powolny-Budnicka I., Riemann M., Tänzer S., Schmid R.M., Hehlgans T., Weih F. RelA and RelB transcription factors in distinct thymocyte populations control lymphotoxin-dependent interleukin-17 production in γδ T cells. Immunity 2011, 34:364-374.
52. Prinz I., Sansoni A., Kissenpfennig A., Ardouin L., Malissen M., Malissen B. Visualization of the earliest steps of gammadelta T cell development in the adult thymus. Nat. Immunol. 2006, 7:995-1003.
53. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332:65-68.
54. Ribot J.C., deBarros A., Pang D.J., Neves J.F., Peperzak V., Roberts S.J., Girardi M., Borst J., Hayday A.C., Pennington D.J., Silva-Santos B. 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.
55. Roark C.L., Simonian P.L., Fontenot A.P., Born W.K., O'Brien R.L. gammadelta T cells: an important source of IL-17. Curr. Opin. Immunol. 2008, 20:353-357.
56. 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 2008, 451:211-215.
57. Shibata K., Yamada H., Hara H., Kishihara K., 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.
58. Shibata K., Yamada H., Nakamura R., Sun X., Itsumi M., Yoshikai Y. Identification of CD25+ gamma delta T cells as fetal thymus-derived naturally occurring IL-17 producers. J. Immunol. 2008, 181:5940-5947.
59. Shibata K., Yamada H., Sato T., Dejima T., Nakamura M., Ikawa T., Hara H., Yamasaki S., Kageyama R., Iwakura Y., et al. Notch-Hes1 pathway is required for the development of IL-17-producing γδ T cells. Blood 2011, 118:586-593.
60. Shichita T., Sugiyama Y., Ooboshi H., Sugimori H., Nakagawa R., Takada I., Iwaki T., Okada Y., Iida M., Cua D.J., et al. Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat. Med. 2009, 15:946-950.
61. Simonian P.L., Roark C.L., Wehrmann F., Lanham A.M., Born W.K., O'Brien R.L., Fontenot A.P. IL-17A-expressing T cells are essential for bacterial clearance in a murine model of hypersensitivity pneumonitis. J. Immunol. 2009, 182:6540-6549.
62. Smith E., Stark M.A., Zarbock A., Burcin T.L., Bruce A.C., Vaswani D., Foley P., Ley K. IL-17A inhibits the expansion of IL-17A-producing T cells in mice through " short-loop" inhibition via IL-17 receptor. J. Immunol. 2008, 181:1357-1364.
63. Stark M.A., Huo Y., Burcin T.L., Morris M.A., Olson T.S., Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005, 22:285-294.
64. Sumaria N., Roediger B., Ng L.G., Qin J., Pinto R., Cavanagh L.L., Shklovskaya E., Fazekas de St Groth B., Triccas J.A., Weninger W. Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J. Exp. Med. 2011, 208:505-518.
65. Sutton C.E., Lalor S.J., Sweeney C.M., Brereton C.F., Lavelle E.C., 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.
66. Takagaki Y., DeCloux A., Bonneville M., Tonegawa S. Diversity of gamma delta T-cell receptors on murine intestinal intra-epithelial lymphocytes. Nature 1989, 339:712-714.
67. Turchinovich G., Hayday A.C. Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 2011, 35:59-68.
68. van de Veerdonk F.L., Plantinga T.S., Hoischen A., Smeekens S.P., Joosten L.A., Gilissen C., Arts P., Rosentul D.C., Carmichael A.J., Smits-van der Graaf C.A., et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N. Engl. J. Med. 2011, 365:54-61.
69. Xiong N., Kang C., Raulet D.H. Positive selection of dendritic epidermal gammadelta T cell precursors in the fetal thymus determines expression of skin-homing receptors. Immunity 2004, 21:121-131.