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The Journal of Immunology, 2001, 167: 4245-4253.
Copyright © 2001 by The American Association of Immunologists

Activation of CD25+CD4+ Regulatory T Cells by Oral Antigen Administration1

Xingmin Zhang, Leonid Izikson, Liming Liu and Howard L. Weiner2

Center for Neurologic Diseases, Harvard Medical School, Boston, MA 02115

CD25+CD4+ T cells are naturally occurring regulatory T cells that are anergic and have suppressive properties. Although they can be isolated from the spleens of normal mice, there are limited studies on how they can be activated or expanded in vivo. We found that oral administration of OVA to OVA TCR transgenic mice resulted in a modification of the ratio of CD25+CD4+ to CD25-CD4+ cells with an increase of CD25+CD4+ T cells accompanied by a decrease of CD25-CD4+ T cells. The relative increase in CD25+CD4+ T cells persisted for as long as 4 wk post feeding. We also found that CTLA-4 was dominantly expressed in CD25+CD4+ T cells and there was an increase in the percentage of CD25+CD4+ T cells expressing CTLA-4 in OVA-fed mice. In contrast to CD25-CD4+ cells, CD25+CD4+ cells from fed mice proliferated only minimally to OVA or anti-CD3 and secreted IL-10 and elevated levels of TGF-{beta}1 following anti-CD3 stimulation. CD25+CD4+ cells from fed mice suppressed the proliferation of CD25-CD4+ T cells in vitro more potently than CD25+CD4+ T cells isolated from unfed mice, and this suppression was partially reversible by IL-10 soluble receptor or TGF-{beta} soluble receptor and high concentration of anti-CTLA-4. With anti-CD3 stimulation, CD25+CD4+ cells from unfed mice secreted IFN-{gamma}, whereas CD25+CD4+ cells from fed mice did not. Adoptive transfer of CD25+CD4+ T cells from fed mice suppressed in vivo delayed-type hypersensitivity responses in BALB/c mice. These results demonstrate an Ag-specific in vivo method to activate CD25+CD4+ regulatory T cells and suggest that they may be involved in oral tolerance.




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J. Immunol.Home page
P. Zhou, R. Borojevic, C. Streutker, D. Snider, H. Liang, and K. Croitoru
Expression of Dual TCR on DO11.10 T Cells Allows for Ovalbumin-Induced Oral Tolerance to Prevent T Cell-Mediated Colitis Directed against Unrelated Enteric Bacterial Antigens
J. Immunol., February 1, 2004; 172(3): 1515 - 1523.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Nakamura, A. Kitani, I. Fuss, A. Pedersen, N. Harada, H. Nawata, and W. Strober
TGF-{beta}1 Plays an Important Role in the Mechanism of CD4+CD25+ Regulatory T Cell Activity in Both Humans and Mice
J. Immunol., January 15, 2004; 172(2): 834 - 842.
[Abstract] [Full Text] [PDF]


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JEMHome page
W. Chen, W. Jin, N. Hardegen, K.-j. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl
Conversion of Peripheral CD4+CD25- Naive T Cells to CD4+CD25+ Regulatory T Cells by TGF-{beta} Induction of Transcription Factor Foxp3
J. Exp. Med., December 15, 2003; 198(12): 1875 - 1886.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. Cavani, F. Nasorri, C. Ottaviani, S. Sebastiani, O. De Pita, and G. Girolomoni
Human CD25+ Regulatory T Cells Maintain Immune Tolerance to Nickel in Healthy, Nonallergic Individuals
J. Immunol., December 1, 2003; 171(11): 5760 - 5768.
[Abstract] [Full Text] [PDF]


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BloodHome page
B. Dubois, L. Chapat, A. Goubier, M. Papiernik, J.-F. Nicolas, and D. Kaiserlian
Innate CD4+CD25+ regulatory T cells are required for oral tolerance and inhibition of CD8+ T cells mediating skin inflammation
Blood, November 1, 2003; 102(9): 3295 - 3301.
[Abstract] [Full Text] [PDF]


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JEMHome page
A. Kitani, I. Fuss, K. Nakamura, F. Kumaki, T. Usui, and W. Strober
Transforming Growth Factor (TGF)-{beta}1-producing Regulatory T Cells Induce Smad-mediated Interleukin 10 Secretion That Facilitates Coordinated Immunoregulatory Activity and Amelioration of TGF-{beta}1-mediated Fibrosis
J. Exp. Med., October 20, 2003; 198(8): 1179 - 1188.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
D. A. Horwitz, S. G. Zheng, and J. D. Gray
The role of the combination of IL-2 and TGF-{beta} or IL-10 in the generation and function of CD4+ CD25+ and CD8+regulatory T cell subsets
J. Leukoc. Biol., October 1, 2003; 74(4): 471 - 478.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. Kaji, S. Hachimura, W. Ise, and S. Kaminogawa
Proteome Analysis Reveals Caspase Activation in Hyporesponsive CD4 T Lymphocytes Induced in Vivo by the Oral Administration of Antigen
J. Biol. Chem., July 18, 2003; 278(30): 27836 - 27843.
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Int ImmunolHome page
W. W. J. Unger, W. Jansen, D. A. W. Wolvers, A. G. S. van Halteren, G. Kraal, and J. N. Samsom
Nasal tolerance induces antigen-specific CD4+CD25- regulatory T cells that can transfer their regulatory capacity to naive CD4+ T cells
Int. Immunol., June 1, 2003; 15(6): 731 - 739.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
C. Vasu, R.-N. E. Dogan, M. J. Holterman, and B. S. Prabhakar
Selective Induction of Dendritic Cells Using Granulocyte Macrophage-Colony Stimulating Factor, But Not fms-Like Tyrosine Kinase Receptor 3-Ligand, Activates Thyroglobulin-Specific CD4+/CD25+ T Cells and Suppresses Experimental Autoimmune Thyroiditis
J. Immunol., June 1, 2003; 170(11): 5511 - 5522.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
M. Paas-Rozner, M. Sela, and E. Mozes
A dual altered peptide ligand down-regulates myasthenogenic T cell responses by up-regulating CD25- and CTLA-4-expressing CD4+ T cells
PNAS, May 27, 2003; 100(11): 6676 - 6681.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. Grundstrom, L. Cederbom, A. Sundstedt, P. Scheipers, and F. Ivars
Superantigen-Induced Regulatory T Cells Display Different Suppressive Functions in the Presence or Absence of Natural CD4+CD25+ Regulatory T Cells In Vivo
J. Immunol., May 15, 2003; 170(10): 5008 - 5017.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
C. Vasu, S. R. Gorla, B. S. Prabhakar, and M. J. Holterman
Targeted engagement of CTLA-4 prevents autoimmune thyroiditis
Int. Immunol., May 1, 2003; 15(5): 641 - 654.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
A. Lundgren, E. Suri-Payer, K. Enarsson, A.-M. Svennerholm, and B. S. Lundin
Helicobacterpylori-Specific CD4+ CD25high Regulatory T Cells Suppress Memory T-Cell Responses to H. pylori in Infected Individuals
Infect. Immun., April 1, 2003; 71(4): 1755 - 1762.
[Abstract] [Full Text]


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Int ImmunolHome page
N. M. Tsuji, K. Mizumachi, and J.-i. Kurisaki
Antigen-specific, CD4+CD25+ regulatory T cell clones induced in Peyer's patches
Int. Immunol., April 1, 2003; 15(4): 525 - 534.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. Oida, X. Zhang, M. Goto, S. Hachimura, M. Totsuka, S. Kaminogawa, and H. L. Weiner
CD4+CD25- T Cells That Express Latency-Associated Peptide on the Surface Suppress CD4+CD45RBhigh-Induced Colitis by a TGF-{beta}-Dependent Mechanism
J. Immunol., March 1, 2003; 170(5): 2516 - 2522.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
C. Montagnoli, A. Bacci, S. Bozza, R. Gaziano, P. Mosci, A. H. Sharpe, and L. Romani
B7/CD28-Dependent CD4+CD25+ Regulatory T Cells Are Essential Components of the Memory-Protective Immunity to Candida albicans
J. Immunol., December 1, 2002; 169(11): 6298 - 6308.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J. Lehmann, J. Huehn, M. de la Rosa, F. Maszyna, U. Kretschmer, V. Krenn, M. Brunner, A. Scheffold, and A. Hamann
Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells
PNAS, October 1, 2002; 99(20): 13031 - 13036.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Y. Wu, F. J. Ward, and N. A. Staines
Histone Peptide-Induced Nasal Tolerance: Suppression of Murine Lupus
J. Immunol., July 15, 2002; 169(2): 1126 - 1134.
[Abstract] [Full Text] [PDF]


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Rheumatology (Oxford)Home page
P. M. Cobelens, A. Kavelaars, R. van der Zee, W. van Eden, and C. J. Heijnen
Dynamics of mycobacterial HSP65-induced T-cell cytokine expression during oral tolerance induction in adjuvant arthritis
Rheumatology, July 1, 2002; 41(7): 775 - 779.
[Abstract] [Full Text] [PDF]




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