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

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-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- soluble receptor and high concentration of anti-CTLA-4. With anti-CD3 stimulation, CD25⁺CD4⁺ cells from unfed mice secreted IFN-, 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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				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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				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]