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CD25⁺ CD4⁺ T Cells Regulate the Expansion of Peripheral CD4 T Cells Through the Production of IL-10¹

Unité du Développement des Lymphocytes, Centre National de la Recherche Scientifique, Unité de Recherche Associée 1961, Institut Pasteur, Paris, France

The mechanisms by which the immune system achieves constant T cell numbers throughout life, thereby controlling autoaggressive cell expansions, are to date not completely understood. Here, we show that the CD25⁺ subpopulation of naturally activated (CD45RB^low) CD4 T cells, but not CD25^- CD45RB^low CD4 T cells, inhibits the accumulation of cotransferred CD45RB^high CD4 T cells in lymphocyte-deficient mice. However, both CD25⁺ and CD25^- CD45RB^low CD4 T cell subpopulations contain regulatory cells, since they can prevent naive CD4 T cell-induced wasting disease. In the absence of a correlation between disease and the number of recovered CD4⁺ cells, we conclude that expansion control and disease prevention are largely independent processes. CD25⁺ CD45RB^low CD4 T cells from IL-10-deficient mice do not protect from disease. They accumulate to a higher cell number and cannot prevent the expansion of CD45RB^high CD4 T cells upon transfer compared with their wild-type counterparts. Although CD25⁺ CD45RB^low CD4 T cells are capable of expanding when transferred in vivo, they reach a homeostatic equilibrium at lower cell numbers than CD25^- CD45RB^low or CD45RB^high CD4 T cells. We conclude that CD25⁺ CD45RB^low CD4 T cells from nonmanipulated mice control the number of peripheral CD4 T cells through a mechanism involving the production of IL-10 by regulatory T cells.

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				L. Graca, A. Le Moine, C.-Y. Lin, P. J. Fairchild, S. P. Cobbold, and H. Waldmann Donor-specific transplantation tolerance: The paradoxical behavior of CD4+CD25+ T cells PNAS, July 6, 2004; 101(27): 10122 - 10126. [Abstract] [Full Text] [PDF]

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				O. Joffre, N. Gorsse, P. Romagnoli, D. Hudrisier, and J. P. M. van Meerwijk Induction of antigen-specific tolerance to bone marrow allografts with CD4+CD25+ T lymphocytes Blood, June 1, 2004; 103(11): 4216 - 4221. [Abstract] [Full Text] [PDF]

				P. L. Vieira, J. R. Christensen, S. Minaee, E. J. O'Neill, F. J. Barrat, A. Boonstra, T. Barthlott, B. Stockinger, D. C. Wraith, and A. O'Garra IL-10-Secreting Regulatory T Cells Do Not Express Foxp3 but Have Comparable Regulatory Function to Naturally Occurring CD4+CD25+ Regulatory T Cells J. Immunol., May 15, 2004; 172(10): 5986 - 5993. [Abstract] [Full Text] [PDF]

				S. P. Cobbold, R. Castejon, E. Adams, D. Zelenika, L. Graca, S. Humm, and H. Waldmann Induction of foxP3+ Regulatory T Cells in the Periphery of T Cell Receptor Transgenic Mice Tolerized to Transplants J. Immunol., May 15, 2004; 172(10): 6003 - 6010. [Abstract] [Full Text] [PDF]

				I. M. de Kleer, L. R. Wedderburn, L. S. Taams, A. Patel, H. Varsani, M. Klein, W. de Jager, G. Pugayung, F. Giannoni, G. Rijkers, et al. CD4+CD25bright Regulatory T Cells Actively Regulate Inflammation in the Joints of Patients with the Remitting Form of Juvenile Idiopathic Arthritis J. Immunol., May 15, 2004; 172(10): 6435 - 6443. [Abstract] [Full Text] [PDF]

				T. W. Vahlenkamp, M. B. Tompkins, and W. A. F. Tompkins Feline Immunodeficiency Virus Infection Phenotypically and Functionally Activates Immunosuppressive CD4+CD25+ T Regulatory Cells J. Immunol., April 15, 2004; 172(8): 4752 - 4761. [Abstract] [Full Text] [PDF]

				L. A. Yi, S. Hajialiasgar, and E. Chuang Tyrosine-mediated inhibitory signals contribute to CTLA-4 function in vivo Int. Immunol., April 1, 2004; 16(4): 539 - 547. [Abstract] [Full Text] [PDF]

				B. Martin, A. Banz, B. Bienvenu, C. Cordier, N. Dautigny, C. Becourt, and B. Lucas Suppression of CD4+ T Lymphocyte Effector Functions by CD4+CD25+ Cells In Vivo J. Immunol., March 15, 2004; 172(6): 3391 - 3398. [Abstract] [Full Text] [PDF]

				M. Hesse, C. A. Piccirillo, Y. Belkaid, J. Prufer, M. Mentink-Kane, M. Leusink, A. W. Cheever, E. M. Shevach, and T. A. Wynn The Pathogenesis of Schistosomiasis Is Controlled by Cooperating IL-10-Producing Innate Effector and Regulatory T Cells J. Immunol., March 1, 2004; 172(5): 3157 - 3166. [Abstract] [Full Text] [PDF]

				J. Huehn, K. Siegmund, J. C.U. Lehmann, C. Siewert, U. Haubold, M. Feuerer, G. F. Debes, J. Lauber, O. Frey, G. K. Przybylski, et al. Developmental Stage, Phenotype, and Migration Distinguish Naive- and Effector/Memory-like CD4+ Regulatory T Cells J. Exp. Med., February 2, 2004; 199(3): 303 - 313. [Abstract] [Full Text] [PDF]

				X. Zhang, D. N. Koldzic, L. Izikson, J. Reddy, R. F. Nazareno, S. Sakaguchi, V. K. Kuchroo, and H. L. Weiner IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+CD4+ regulatory T cells Int. Immunol., February 1, 2004; 16(2): 249 - 256. [Abstract] [Full Text] [PDF]

				L. A. Stephens, A. N. Barclay, and D. Mason Phenotypic characterization of regulatory CD4+CD25+ T cells in rats Int. Immunol., February 1, 2004; 16(2): 365 - 375. [Abstract] [Full Text] [PDF]

				L. E. Marra, Z. X. Zhang, B. Joe, J. Campbell, G. A. Levy, J. Penninger, and L. Zhang IL-10 Induces Regulatory T Cell Apoptosis by Up-Regulation of the Membrane Form of TNF-{alpha} J. Immunol., January 15, 2004; 172(2): 1028 - 1035. [Abstract] [Full Text] [PDF]

				H. Jonuleit and E. Schmitt The Regulatory T Cell Family: Distinct Subsets and their Interrelations J. Immunol., December 15, 2003; 171(12): 6323 - 6327. [Full Text] [PDF]

				T. R. Malek The main function of IL-2 is to promote the development of T regulatory cells J. Leukoc. Biol., December 1, 2003; 74(6): 961 - 965. [Abstract] [Full Text]

				C. Cozzo, J. Larkin III, and A. J. Caton Cutting Edge: Self-Peptides Drive the Peripheral Expansion of CD4+CD25+ Regulatory T Cells J. Immunol., December 1, 2003; 171(11): 5678 - 5682. [Abstract] [Full Text] [PDF]

				A. Foussat, F. Cottrez, V. Brun, N. Fournier, J.-P. Breittmayer, and H. Groux A Comparative Study between T Regulatory Type 1 and CD4+CD25+ T Cells in the Control of Inflammation J. Immunol., November 15, 2003; 171(10): 5018 - 5026. [Abstract] [Full Text] [PDF]

				S. Fisson, G. Darrasse-Jeze, E. Litvinova, F. Septier, D. Klatzmann, R. Liblau, and B. L. Salomon Continuous Activation of Autoreactive CD4+ CD25+ Regulatory T Cells in the Steady State J. Exp. Med., September 2, 2003; 198(5): 737 - 746. [Abstract] [Full Text] [PDF]

				T. L. Denning, H. Qi, R. Konig, K. G. Scott, M. Naganuma, and P. B. Ernst CD4+ Th Cells Resembling Regulatory T Cells That Inhibit Chronic Colitis Differentiate in the Absence of Interactions Between CD4 and Class II MHC J. Immunol., September 1, 2003; 171(5): 2279 - 2286. [Abstract] [Full Text] [PDF]

				L. Klein, K. Khazaie, and H. von Boehmer In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro PNAS, July 22, 2003; 100(15): 8886 - 8891. [Abstract] [Full Text] [PDF]

				S. Yamazaki, T. Iyoda, K. Tarbell, K. Olson, K. Velinzon, K. Inaba, and R. M. Steinman Direct Expansion of Functional CD25+ CD4+ Regulatory T Cells by Antigen-processing Dendritic Cells J. Exp. Med., July 21, 2003; 198(2): 235 - 247. [Abstract] [Full Text] [PDF]

				L. S.K. Walker, A. Chodos, M. Eggena, H. Dooms, and A. K. Abbas Antigen-dependent Proliferation of CD4+ CD25+ Regulatory T Cells In Vivo J. Exp. Med., July 21, 2003; 198(2): 249 - 258. [Abstract] [Full Text] [PDF]

				K. Uraushihara, T. Kanai, K. Ko, T. Totsuka, S. Makita, R. Iiyama, T. Nakamura, and M. Watanabe Regulation of Murine Inflammatory Bowel Disease by CD25+ and CD25- CD4+ Glucocorticoid-Induced TNF Receptor Family-Related Gene+ Regulatory T Cells J. Immunol., July 15, 2003; 171(2): 708 - 716. [Abstract] [Full Text] [PDF]