A dynamic dual role of IL-2 signaling in the two-step differentiation process of adaptive regulatory T cells

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3153-3162

  Guo, Zhiyong ^a,b   Khattar, Mithun ^a   Schroder, Paul M ^a   Miyahara, Yoshihiro ^a   Wang, Guohua ^a   He, Xiaoshung ^b   Chen, Wenhao ^a,c   Stepkowski, Stanislaw M ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; JANUS KINASE 3; STAT5 PROTEIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ CD25- FOXP3- T LYMPHOCYTE; COLITIS; CONTROLLED STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPLEEN CELL;

ANIMALS; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; COLITIS; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PRECURSOR CELLS, T-LYMPHOID; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84875455009     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200751     Document Type: Article

References (30)

1. Sakaguchi, S. 2005. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6: 345-352.
2. Zheng, Y., and A. Y. Rudensky. 2007. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8: 457-462.
3. Malek, T. R. 2008. The biology of interleukin-2. Annu. Rev. Immunol. 26: 453-479.
4. Sadlack, B., H. Merz, H. Schorle, A. Schimpl, A. C. Feller, and I. Horak. 1993. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell 75: 253-261.
5. Suzuki, H., T. M. Kündig, C. Furlonger, A. Wakeham, E. Timms, T. Matsuyama, R. Schmits, J. J. Simard, P. S. Ohashi, H. Griesser, et al. 1995. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor beta. Science 268: 1472-1476.
6. Malek, T. R., A. Yu, V. Vincek, P. Scibelli, and L. Kong. 2002. CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rbeta-deficient mice. Implications for the nonredundant function of IL-2. Immunity 17: 167-178.
7. Boyman, O., and J. Sprent. 2012. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12: 180-190.
8. Wang, G., M. Khattar, Z. Guo, Y. Miyahara, S. P. Linkes, Z. Sun, X. He, S. M. Stepkowski, and W. Chen. 2010. IL-2-deprivation and TGF-beta are two non-redundant suppressor mechanisms of CD4+CD25+ regulatory T cell which jointly restrain CD4+CD25- cell activation. Immunol. Lett. 132: 61-68.
9. Pandiyan, P., L. Zheng, S. Ishihara, J. Reed, and M. J. Lenardo. 2007. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat. Immunol. 8: 1353-1362.
10. Josefowicz, S. Z., L. F. Lu, and A. Y. Rudensky. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30: 531-564.
11. Burchill, M. A., J. Yang, C. Vogtenhuber, B. R. Blazar, and M. A. Farrar. 2007. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J. Immunol. 178: 280-290.
12. Lio, C. W., and C. S. Hsieh. 2008. A two-step process for thymic regulatory T cell development. Immunity 28: 100-111.
13. Burchill, M. A., J. Yang, K. B. Vang, J. J. Moon, H. H. Chu, C. W. Lio, A. L. Vegoe, C. S. Hsieh, M. K. Jenkins, and M. A. Farrar. 2008. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 28: 112-121.
14. Vang, K. B., J. Yang, S. A. Mahmud, M. A. Burchill, A. L. Vegoe, and M. A. Farrar. 2008. IL-2, -7, and -15, but not thymic stromal lymphopoietin, redundantly govern CD4+Foxp3+ regulatory T cell development. J. Immunol. 181: 3285-3290.
15. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4+CD252 naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
16. Zheng, S. G., J. Wang, P. Wang, J. D. Gray, and D. A. Horwitz. 2007. IL-2 is essential for TGF-beta to convert naive CD4+CD25- cells to CD25+Foxp3+ regulatory T cells and for expansion of these cells. J. Immunol. 178: 2018-2027.
17. Davidson, T. S., R. J. DiPaolo, J. Andersson, and E. M. Shevach. 2007. Cutting edge: IL-2 is essential for TGF-beta-mediated induction of Foxp3+ T regulatory cells. J. Immunol. 178: 4022-4026.
18. Wang, G., Y. Miyahara, Z. Guo, M. Khattar, S. M. Stepkowski, and W. Chen. 2010. "Default" generation of neonatal regulatory T cells. J. Immunol. 185: 71-78.
19. Izcue, A., S. Hue, S. Buonocore, C. V. Arancibia-Cárcamo, P. P. Ahern, Y. Iwakura, K. J. Maloy, and F. Powrie. 2008. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28: 559-570.
20. Schallenberg, S., P. Y. Tsai, J. Riewaldt, and K. Kretschmer. 2010. Identification of an immediate Foxp3(-) precursor to Foxp3(+) regulatory T cells in peripheral lymphoid organs of nonmanipulated mice. J. Exp. Med. 207: 1393-1407.
21. Polansky, J. K., K. Kretschmer, J. Freyer, S. Floess, A. Garbe, U. Baron, S. Olek, A. Hamann, H. von Boehmer, and J. Huehn. 2008. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 38: 1654-1663.
22. Williams, M. A., A. J. Tyznik, and M. J. Bevan. 2006. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441: 890-893.
23. Webster, K. E., S. Walters, R. E. Kohler, T. Mrkvan, O. Boyman, C. D. Surh, S. T. Grey, and J. Sprent. 2009. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J. Exp. Med. 206: 751-760.
24. Boyman, O., M. Kovar, M. P. Rubinstein, C. D. Surh, and J. Sprent. 2006. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 311: 1924-1927.
25. Grinberg-Bleyer, Y., A. Baeyens, S. You, R. Elhage, G. Fourcade, S. Gregoire, N. Cagnard, W. Carpentier, Q. Tang, J. Bluestone, et al. 2010. IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J. Exp. Med. 207: 1871-1878.
26. Selvaraj, R. K., and T. L. Geiger. 2007. A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-beta. J. Immunol. 178: 7667-7677.
27. Yao, Z., Y. Kanno, M. Kerenyi, G. Stephens, L. Durant, W. T. Watford, A. Laurence, G. W. Robinson, E. M. Shevach, R. Moriggl, et al. 2007. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 109: 4368-4375.
28. Josefowicz, S. Z., and A. Rudensky. 2009. Control of regulatory T cell lineage commitment and maintenance. Immunity 30: 616-625.
29. Curotto de Lafaille, M. A., and J. J. Lafaille. 2009. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30: 626-635.
30. Kretschmer, K., I. Apostolou, D. Hawiger, K. Khazaie, M. C. Nussenzweig, and H. von Boehmer. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6: 1219-1227.