Aire Inhibits the Generation of a Perinatal Population of Interleukin-17A-Producing γδ T Cells to Promote Immunologic Tolerance

Immunity

Volumn 45, Issue 5, 2016, Pages 999-1012

  Fujikado, Noriyuki ^a   Mann, Alexander O ^a   Bansal, Kushagra ^a   Romito, Kimberly R ^b   Ferre, Elise M N ^c   Rosenzweig, Sergio D ^b   Lionakis, Michail S ^c   Benoist, Christophe ^a   Mathis, Diane ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNE REGULATOR PROTEIN; INTERLEUKIN 17; LYMPHOCYTE ANTIGEN RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE POLYENDOCRINOPATHY CANDIDIASIS ECTODERMAL DYSTROPHY; AUTOIMMUNITY; CELL COMPARTMENTALIZATION; CELL INFILTRATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE SUBPOPULATION; MALE; MOUSE; NONHUMAN; PARALLEL DESIGN; PERINATAL PERIOD; PRIORITY JOURNAL; RETINA CELL; THYMOCYTE; WILD TYPE; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; GENE EXPRESSION PROFILING; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; POLYENDOCRINOPATHY; POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; CHILD; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-17; MALE; MICE; MICE, KNOCKOUT; POLYENDOCRINOPATHIES, AUTOIMMUNE; POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; YOUNG ADULT;

EID: 84999652058     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.10.023     Document Type: Article

References (67)

1. Anderson, M.S., Venanzi, E.S., Klein, L., Chen, Z., Berzins, S.P., Turley, S.J., von Boehmer, H., Bronson, R., Dierich, A., Benoist, C., Mathis, D., Projection of an immunological self shadow within the thymus by the aire protein. Science 298 (2002), 1395–1401.
2. Anderson, M.S., Venanzi, E.S., Chen, Z., Berzins, S.P., Benoist, C., Mathis, D., The cellular mechanism of Aire control of T cell tolerance. Immunity 23 (2005), 227–239.
3. Barbee, S.D., Woodward, M.J., Turchinovich, G., Mention, J.J., Lewis, J.M., Boyden, L.M., Lifton, R.P., Tigelaar, R., Hayday, A.C., Skint-1 is a highly specific, unique selecting component for epidermal T cells. Proc. Natl. Acad. Sci. USA 108 (2011), 3330–3335.
4. Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J.L., Cerletti, M., Jang, Y., Sefik, E., Tan, T.G., Wagers, A.J., Benoist, C., Mathis, D., A special population of regulatory T cells potentiates muscle repair. Cell 155 (2013), 1282–1295.
5. 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 118 (2011), 129–138.
6. Cai, Y., Shen, X., Ding, C., Qi, C., Li, K., Li, X., Jala, V.R., Zhang, H.G., Wang, T., Zheng, J., Yan, J., Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35 (2011), 596–610.
7. Chien, Y.H., Meyer, C., Bonneville, M., γδ T cells: first line of defense and beyond. Annu. Rev. Immunol. 32 (2014), 121–155.
8. 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. 120 (2010), 1762–1773.
9. Cua, D.J., Tato, C.M., Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10 (2010), 479–489.
10. + uveitogenic T cells. J. Immunol. 183 (2009), 560–567.
11. 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. 127 (2009), 8–12.
12. Dimova, T., Brouwer, M., Gosselin, F., Tassignon, J., Leo, O., Donner, C., Marchant, A., Vermijlen, D., Effector Vγ9Vδ2 T cells dominate the human fetal γδ T-cell repertoire. Proc. Natl. Acad. Sci. USA 112 (2015), E556–E565.
13. Gardner, J.M., Devoss, J.J., Friedman, R.S., Wong, D.J., Tan, Y.X., Zhou, X., Johannes, K.P., Su, M.A., Chang, H.Y., Krummel, M.F., Anderson, M.S., Deletional tolerance mediated by extrathymic Aire-expressing cells. Science 321 (2008), 843–847.
14. Giraud, M., Yoshida, H., Abramson, J., Rahl, P.B., Young, R.A., Mathis, D., Benoist, C., Aire unleashes stalled RNA polymerase to induce ectopic gene expression in thymic epithelial cells. Proc. Natl. Acad. Sci. USA 109 (2012), 535–540.
15. Guerau-de-Arellano, M., Martinic, M., Benoist, C., Mathis, D., Neonatal tolerance revisited: a perinatal window for Aire control of autoimmunity. J. Exp. Med. 206 (2009), 1245–1252.
16. Hayes, S.M., Li, L., Love, P.E., TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity 22 (2005), 583–593.
17. Heilig, J.S., Tonegawa, S., Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 322 (1986), 836–840.
18. 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 γ. Immunity 29 (2008), 90–100.
19. Jiang, W., Anderson, M.S., Bronson, R., Mathis, D., Benoist, C., Modifier loci condition autoimmunity provoked by Aire deficiency. J. Exp. Med. 202 (2005), 805–815.
20. Jin, Y., Xia, M., Sun, A., Saylor, C.M., Xiong, N., CCR10 is important for the development of skin-specific gammadeltaT cells by regulating their migration and location. J. Immunol. 185 (2010), 5723–5731.
21. Johnnidis, J.B., Venanzi, E.S., Taxman, D.J., Ting, J.P., Benoist, C.O., Mathis, D.J., Chromosomal clustering of genes controlled by the aire transcription factor. Proc. Natl. Acad. Sci. USA 102 (2005), 7233–7238.
22. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, 2013, R36.
23. Kisand, K., Peterson, P., Autoimmune polyendocrinopathy candidiasis ectodermal dystrophy. J. Clin. Immunol. 35 (2015), 463–478.
24. Kisand, K., Bøe Wolff, A.S., Podkrajsek, K.T., Tserel, L., Link, M., Kisand, K.V., Ersvaer, E., Perheentupa, J., Erichsen, M.M., Bratanic, N., et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J. Exp. Med. 207 (2010), 299–308.
25. Koh, A.S., Kingston, R.E., Benoist, C., Mathis, D., Global relevance of Aire binding to hypomethylated lysine-4 of histone-3. Proc. Natl. Acad. Sci. USA 107 (2010), 13016–13021.
26. + T cell homeostasis in the monogenic human disease autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy. J. Immunol. 187 (2011), 2023–2030.
27. Lei, Y., Ripen, A.M., Ishimaru, N., Ohigashi, I., Nagasawa, T., Jeker, L.T., Bösl, M.R., Holländer, G.A., Hayashi, Y., Malefyt, Rde.W., et al. Aire-dependent production of XCL1 mediates medullary accumulation of thymic dendritic cells and contributes to regulatory T cell development. J. Exp. Med. 208 (2011), 383–394.
28. Liston, A., Lesage, S., Wilson, J., Peltonen, L., Goodnow, C.C., Aire regulates negative selection of organ-specific T cells. Nat. Immunol. 4 (2003), 350–354.
29. 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. 177 (2006), 4662–4669.
30. Malchow, S., Leventhal, D.S., Nishi, S., Fischer, B.I., Shen, L., Paner, G.P., Amit, A.S., Kang, C., Geddes, J.E., Allison, J.P., et al. Aire-dependent thymic development of tumor-associated regulatory T cells. Science 339 (2013), 1219–1224.
31. Meeks, K.D., Sieve, A.N., Kolls, J.K., Ghilardi, N., Berg, R.E., IL-23 is required for protection against systemic infection with Listeria monocytogenes. J. Immunol. 183 (2009), 8026–8034.
32. Meredith, M., Zemmour, D., Mathis, D., Benoist, C., Aire controls gene expression in the thymic epithelium with ordered stochasticity. Nat. Immunol. 16 (2015), 942–949.
33. Michel, M.L., Pang, D.J., Haque, S.F., Potocnik, A.J., Pennington, D.J., Hayday, A.C., Interleukin 7 (IL-7) selectively promotes mouse and human IL-17-producing γδ cells. Proc. Natl. Acad. Sci. USA 109 (2012), 17549–17554.
34. 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., Immunological Genome Project Consortium. Intrathymic programming of effector fates in three molecularly distinct γδ T cell subtypes. Nat. Immunol. 13 (2012), 511–518.
35. Nitta, T., Muro, R., Shimizu, Y., Nitta, S., Oda, H., Ohte, Y., Goto, M., Yanobu-Takanashi, R., Narita, T., Takayanagi, H., et al. The thymic cortical epithelium determines the TCR repertoire of IL-17-producing γδT cells. EMBO Rep. 16 (2015), 638–653.
36. O'Brien, R.L., Born, W.K., Dermal γδ T cells-What have we learned?. Cell. Immunol. 296 (2015), 62–69.
37. Oven, I., Brdicková, N., Kohoutek, J., Vaupotic, T., Narat, M., Peterlin, B.M., AIRE recruits P-TEFb for transcriptional elongation of target genes in medullary thymic epithelial cells. Mol. Cell. Biol. 27 (2007), 8815–8823.
38. Paget, C., Chow, M.T., Gherardin, N.A., Beavis, P.A., Uldrich, A.P., Duret, H., Hassane, M., Souza-Fonseca-Guimaraes, F., Mogilenko, D.A., Staumont-Sallé, D., et al. CD3bright signals on γδ T cells identify IL-17A-producing Vγ6Vδ1+ T cells. Immunol. Cell Biol. 93 (2015), 198–212.
39. Pennington, D.J., Silva-Santos, B., Silberzahn, T., Escórcio-Correia, M., Woodward, M.J., Roberts, S.J., Smith, A.L., Dyson, P.J., Hayday, A.C., Early events in the thymus affect the balance of effector and regulatory T cells. Nature 444 (2006), 1073–1077.
40. Pereira, P., Boucontet, L., Rates of recombination and chain pair biases greatly influence the primary gammadelta TCR repertoire in the thymus of adult mice. J. Immunol. 173 (2004), 3261–3270.
41. Perry, J.S., Lio, C.W., Kau, A.L., Nutsch, K., Yang, Z., Gordon, J.I., Murphy, K.M., Hsieh, C.S., Distinct contributions of Aire and antigen-presenting-cell subsets to the generation of self-tolerance in the thymus. Immunity 41 (2014), 414–426.
42. 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 33 (2010), 351–363.
43. Picelli, S., Björklund, A.K., Faridani, O.R., Sagasser, S., Winberg, G., Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 10 (2013), 1096–1098.
44. Picelli, S., Faridani, O.R., Björklund, A.K., Winberg, G., Sagasser, S., Sandberg, R., Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9 (2014), 171–181.
45. Pitt, L.A., Hubert, F.X., Scott, H.S., Godfrey, D.I., Berzins, S.P., NKT cell development in the absence of the autoimmune regulator gene (Aire). Eur. J. Immunol. 38 (2008), 2689–2696.
46. Puel, A., Döffinger, R., Natividad, A., Chrabieh, M., Barcenas-Morales, G., Picard, C., Cobat, A., Ouachée-Chardin, M., Toulon, A., Bustamante, J., et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J. Exp. Med. 207 (2010), 291–297.
47. Rei, M., Gonçalves-Sousa, N., Lança, T., Thompson, R.G., Mensurado, S., Balkwill, F.R., Kulbe, H., Pennington, D.J., Silva-Santos, B., Murine CD27(-) Vγ6(+) γδ T cells producing IL-17A promote ovarian cancer growth via mobilization of protumor small peritoneal macrophages. Proc. Natl. Acad. Sci. USA 111 (2014), E3562–E3570.
48. Ribeiro, A.R., Rodrigues, P.M., Meireles, C., Di Santo, J.P., Alves, N.L., Thymocyte selection regulates the homeostasis of IL-7-expressing thymic cortical epithelial cells in vivo. J. Immunol. 191 (2013), 1200–1209.
49. Ribot, J.C., Chaves-Ferreira, M., d'Orey, F., Wencker, M., Gonçalves-Sousa, N., Decalf, J., Simas, J.P., Hayday, A.C., Silva-Santos, B., Cutting edge: adaptive versus innate receptor signals selectively control the pool sizes of murine IFN-γ- or IL-17-producing γδ T cells upon infection. J. Immunol. 185 (2010), 6421–6425.
50. Riol-Blanco, L., Lazarevic, V., Awasthi, A., Mitsdoerffer, M., Wilson, B.S., Croxford, A., Waisman, A., Kuchroo, V.K., Glimcher, L.H., Oukka, M., IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J. Immunol. 184 (2010), 1710–1720.
51. Roark, C.L., French, J.D., Taylor, M.A., Bendele, A.M., Born, W.K., O'Brien, R.L., Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing γ δ T cells. J. Immunol. 179 (2007), 5576–5583.
52. +) medullary epithelium. Immunity 36 (2012), 427–437.
53. Sansom, S.N., Shikama-Dorn, N., Zhanybekova, S., Nusspaumer, G., Macaulay, I.C., Deadman, M.E., Heger, A., Ponting, C.P., Holländer, G.A., Population and single-cell genomics reveal the Aire dependency, relief from Polycomb silencing, and distribution of self-antigen expression in thymic epithelia. Genome Res. 24 (2014), 1918–1931.
54. Sato, K., Sato, U., Tateishi, S., Kubo, K., Horikawa, R., Mimura, T., Yamamoto, K., Kanda, H., Aire downregulates multiple molecules that have contradicting immune-enhancing and immune-suppressive functions. Biochem. Biophys. Res. Commun. 318 (2004), 935–940.
55. + regulatory T cells. Science 349 (2015), 993–997.
56. 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. 178 (2007), 4466–4472.
57. Sim, G.K., Olsson, C., Augustin, A., Commitment and maintenance of the alpha beta and gamma delta T cell lineages. J. Immunol. 154 (1995), 5821–5831.
58. 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 31 (2009), 331–341.
59. Taniguchi, R.T., DeVoss, J.J., Moon, J.J., Sidney, J., Sette, A., Jenkins, M.K., Anderson, M.S., Detection of an autoreactive T-cell population within the polyclonal repertoire that undergoes distinct autoimmune regulator (Aire)-mediated selection. Proc. Natl. Acad. Sci. USA 109 (2012), 7847–7852.
60. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7 (2012), 562–578.
61. Trombetta, J.J., Gennert, D., Lu, D., Satija, R., Shalek, A.K., Regev, A., Preparation of single-cell RNA-seq libraries for next generation sequencing. Curr. Protoc. Mol. Biol. 107 (2014), 1–17.
62. Tuovinen, H., Pöntynen, N., Gylling, M., Kekäläinen, E., Perheentupa, J., Miettinen, A., Arstila, T.P., gammadelta T cells develop independently of Aire. Cell. Immunol. 257 (2009), 5–12.
63. 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 35 (2011), 59–68.
64. Vantourout, P., Hayday, A., Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol. 13 (2013), 88–100.
65. Wu, P., Wu, D., Ni, C., Ye, J., Chen, W., Hu, G., Wang, Z., Wang, C., Zhang, Z., Xia, W., et al. γδT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40 (2014), 785–800.
66. Yang, S., Fujikado, N., Kolodin, D., Benoist, C., Mathis, D., Immune tolerance. Regulatory T cells generated early in life play a distinct role in maintaining self-tolerance. Science 348 (2015), 589–594.
67. Zeng, X., Wei, Y.L., Huang, J., Newell, E.W., Yu, H., Kidd, B.A., Kuhns, M.S., Waters, R.W., Davis, M.M., Weaver, C.T., Chien, Y.H., γδ T cells recognize a microbial encoded B cell antigen to initiate a rapid antigen-specific interleukin-17 response. Immunity 37 (2012), 524–534.