Ex vivo IL-1 receptor type I expression in human CD4 + T cells identifies an early intermediate in the differentiation of Th17 from FOXP3 + naive regulatory T cells

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5196-5202

  Raffin, Caroline ^a   Raimbaud, Isabelle ^a   Valmori, Danila ^a,b   Ayyoub, Maha ^a  

^a CENTRE RENÉ GAUDUCHEAU   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 17; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EFFECTOR CELL; EX VIVO STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MEMORY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH17 CELL;

CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-17; RECEPTORS, INTERLEUKIN-1; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TIME FACTORS;

EID: 81455135858     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101742     Document Type: Article

References (26)

1. Amadi-Obi, A., C. R. Yu, X. Liu, R. M. Mahdi, G. L. Clarke, R. B. Nussenblatt, I. Gery, Y. S. Lee, and C. E. Egwuagu. 2007. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13: 711-718. (Pubitemid 46889754)
2. Kolls, J. K., and A. Lindén. 2004. Interleukin-17 family members and inflammation. Immunity 21: 467-476. (Pubitemid 39370503)
3. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133. (Pubitemid 44380299)
4. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057. (Pubitemid 351871737)
5. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 cells. Annu. Rev. Immunol. 27: 485-517.
6. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
7. Koenen, H. J., R. L. Smeets, P. M. Vink, E. van Rijssen, A. M. Boots, and I. Joosten. 2008. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112: 2340-2352.
8. Deknuydt, F., G. Bioley, D. Valmori, and M. Ayyoub. 2009. IL-1beta and IL-2 convert human Treg into T(H)17 cells. Clin. Immunol. 131: 298-307.
9. Ayyoub, M., F. Deknuydt, I. Raimbaud, C. Dousset, L. Leveque, G. Bioley, and D. Valmori. 2009. Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor ROR-gamma t. Proc. Natl. Acad. Sci. USA 106: 8635-8640.
10. Voo, K. S., Y. H. Wang, F. R. Santori, C. Boggiano, Y. H. Wang, K. Arima, L. Bover, S. Hanabuchi, J. Khalili, E. Marinova, et al. 2009. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc. Natl. Acad. Sci. USA 106: 4793-4798.
11. Valmori, D., A. Merlo, N. E. Souleimanian, C. S. Hesdorffer, and M. Ayyoub. 2005. A peripheral circulating compartment of natural naive CD4 Tregs. J. Clin. Invest. 115: 1953-1962. (Pubitemid 40979735)
12. Valmori, D., C. Raffin, I. Raimbaud, and M. Ayyoub. 2010. Human RORγt+ TH17 cells preferentially differentiate from naive FOXP3+Treg in the presence of lineage-specific polarizing factors. Proc. Natl. Acad. Sci. USA 107: 19402-19407.
13. O'Neill, L. A. 2008. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol. Rev. 226: 10-18.
14. Chung, Y., S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2009. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30: 576-587.
15. Lee, W. W., S. W. Kang, J. Choi, S. H. Lee, K. Shah, E. E. Eynon, R. A. Flavell, and I. Kang. 2010. Regulating human Th17 cells via differential expression of IL-1 receptor. Blood 115: 530-540.
16. Tran, D. Q., J. Andersson, D. Hardwick, L. Bebris, G. G. Illei, and E. M. Shevach. 2009. Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3+ regulatory T cells allows for their purification from expansion cultures. Blood 113: 5125-5133.
17. Mercer, F., L. Kozhaya, and D. Unutmaz. 2010. Expression and function of TNF and IL-1 receptors on human regulatory T cells. PLoS ONE 5: e8639.
18. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
19. Tosello, V., K. Odunsi, N. E. Souleimanian, S. Lele, P. Shrikant, L. J. Old, D. Valmori, and M. Ayyoub. 2008. Differential expression of CCR7 defines two distinct subsets of human memory CD4+CD25+ Tregs. Clin. Immunol. 126: 291-302.
20. Acosta-Rodriguez, E. V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8: 639-646. (Pubitemid 46785128)
21. Annunziato, F., L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Filì, S. Ferri, F. Frosali, et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204: 1849-1861. (Pubitemid 47240944)
22. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
23. Rivino, L., M. Messi, D. Jarrossay, A. Lanzavecchia, F. Sallusto, and J. Geginat. 2004. Chemokine receptor expression identifies Pre-T helper (Th)1, Pre-Th2, and nonpolarized cells among human CD4+ central memory T cells. J. Exp. Med. 200: 725-735. (Pubitemid 39299459)
24. Kryczek, I., K. Wu, E. Zhao, S. Wei, L. Vatan, W. Szeliga, E. Huang, J. Greenson, A. Chang, J. Roliński, et al. 2011. IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer. J. Immunol. 186: 4388-4395.
25. Hoffmann, P., R. Eder, T. J. Boeld, K. Doser, B. Piseshka, R. Andreesen, and M. Edinger. 2006. Only the CD45RA+ subpopulation of CD4+CD25high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion. Blood 108: 4260-4267. (Pubitemid 44913302)
26. Safinia, N., P. Sagoo, R. Lechler, and G. Lombardi. 2010. Adoptive regulatory T cell therapy: challenges in clinical transplantation. Curr. Opin. Organ Transplant. 15: 427-434.