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The Journal of Immunology, 2001, 166: 3008-3018.
Copyright © 2001 by The American Association of Immunologists

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

Oliver Annacker2, Ricardo Pimenta-Araujo, Odile Burlen-Defranoux, Theolis C. Barbosa3, Ana Cumano and Antonio Bandeira

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 (CD45RBlow) CD4 T cells, but not CD25- CD45RBlow CD4 T cells, inhibits the accumulation of cotransferred CD45RBhigh CD4 T cells in lymphocyte-deficient mice. However, both CD25+ and CD25- CD45RBlow 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+ CD45RBlow 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 CD45RBhigh CD4 T cells upon transfer compared with their wild-type counterparts. Although CD25+ CD45RBlow CD4 T cells are capable of expanding when transferred in vivo, they reach a homeostatic equilibrium at lower cell numbers than CD25- CD45RBlow or CD45RBhigh CD4 T cells. We conclude that CD25+ CD45RBlow 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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M. A. Curotto de Lafaille, A. C. Lino, N. Kutchukhidze, and J. J. Lafaille
CD25- T Cells Generate CD25+Foxp3+ Regulatory T Cells by Peripheral Expansion
J. Immunol., December 15, 2004; 173(12): 7259 - 7268.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
O. R. Millington, A. McI. Mowat, and P. Garside
Induction of Bystander Suppression by Feeding Antigen Occurs despite Normal Clonal Expansion of the Bystander T Cell Population
J. Immunol., November 15, 2004; 173(10): 6059 - 6064.
[Abstract] [Full Text] [PDF]


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BloodHome page
E. Xystrakis, A. S. Dejean, I. Bernard, P. Druet, R. Liblau, D. Gonzalez-Dunia, and A. Saoudi
Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation
Blood, November 15, 2004; 104(10): 3294 - 3301.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
H. C. Dujardin, O. Burlen-Defranoux, L. Boucontet, P. Vieira, A. Cumano, and A. Bandeira
Regulatory potential and control of Foxp3 expression in newborn CD4+ T cells
PNAS, October 5, 2004; 101(40): 14473 - 14478.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
J. Machen, J. Harnaha, R. Lakomy, A. Styche, M. Trucco, and N. Giannoukakis
Antisense Oligonucleotides Down-Regulating Costimulation Confer Diabetes-Preventive Properties to Nonobese Diabetic Mouse Dendritic Cells
J. Immunol., October 1, 2004; 173(7): 4331 - 4341.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. Makita, T. Kanai, S. Oshima, K. Uraushihara, T. Totsuka, T. Sawada, T. Nakamura, K. Koganei, T. Fukushima, and M. Watanabe
CD4+CD25bright T Cells in Human Intestinal Lamina Propria as Regulatory Cells
J. Immunol., September 1, 2004; 173(5): 3119 - 3130.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
U. Wagner, M. Pierer, M. Wahle, F. Moritz, S. Kaltenhauser, and H. Hantzschel
Ex Vivo Homeostatic Proliferation of CD4+ T Cells in Rheumatoid Arthritis Is Dysregulated and Driven by Membrane-Anchored TNF{alpha}
J. Immunol., August 15, 2004; 173(4): 2825 - 2833.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
E. Nishimura, T. Sakihama, R. Setoguchi, K. Tanaka, and S. Sakaguchi
Induction of antigen-specific immunologic tolerance by in vivo and in vitro antigen-specific expansion of naturally arising Foxp3+CD25+CD4+ regulatory T cells
Int. Immunol., August 1, 2004; 16(8): 1189 - 1201.
[Abstract] [Full Text] [PDF]


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BloodHome page
P. Hoffmann, R. Eder, L. A. Kunz-Schughart, R. Andreesen, and M. Edinger
Large-scale in vitro expansion of polyclonal human CD4+CD25high regulatory T cells
Blood, August 1, 2004; 104(3): 895 - 903.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Inagaki-Ohara, T. Chinen, G. Matsuzaki, A. Sasaki, Y. Sakamoto, K. Hiromatsu, F. Nakamura-Uchiyama, Y. Nawa, and A. Yoshimura
Mucosal T Cells Bearing TCR{gamma}{delta} Play a Protective Role in Intestinal Inflammation
J. Immunol., July 15, 2004; 173(2): 1390 - 1398.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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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J. Immunol.Home page
M. K. Lee IV, D. J. Moore, B. P. Jarrett, M. M. Lian, S. Deng, X. Huang, J. W. Markmann, M. Chiaccio, C. F. Barker, A. J. Caton, et al.
Promotion of Allograft Survival by CD4+CD25+ Regulatory T Cells: Evidence for In Vivo Inhibition of Effector Cell Proliferation
J. Immunol., June 1, 2004; 172(11): 6539 - 6544.
[Abstract] [Full Text] [PDF]


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BloodHome page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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Int ImmunolHome page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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JEMHome page
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]


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Int ImmunolHome page
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]


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Int ImmunolHome page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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J. Leukoc. Biol.Home page
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]


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J. Immunol.Home page
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]


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J. Immunol.Home page
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]


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JEMHome page
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]


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J. Immunol.Home page
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]


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Proc. Natl. Acad. Sci. USAHome page
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]


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JEMHome page
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]


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JEMHome page
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]


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J. Immunol.Home page
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]




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