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Helmut Jonuleit¹, Edgar Schmitt², Hacer Kakirman¹, Michael Stassen², Jürgen Knop¹ and Alexander H. Enk¹

¹ Department of Dermatology, University of Mainz, 55101 Mainz, Germany
² Institute of Immunology, University of Mainz, 55101 Mainz, Germany

Address correspondence to H. Jonuleit, Dept. of Dermatology, University of Mainz, D-55101 Mainz, Germany. Phone: 49-6131-173541; Fax: 49-6131-175505 or 17-473541; E-mail: jonuleit{at}hautklinik.klinik.uni-mainz.de

Regulatory CD4⁺CD25⁺ T cells (Treg) are mandatory for maintaining immunologic self-tolerance. We demonstrate that the cell-cell contact–mediated suppression of conventional CD4⁺ T cells by human CD25⁺ Treg cells is fixation resistant, independent from membrane-bound TGF-ß but requires activation and protein synthesis of CD25⁺ Treg cells. Coactivation of CD25⁺ Treg cells with Treg cell–depleted CD4⁺ T cells results in anergized CD4⁺ T cells that in turn inhibit the activation of conventional, freshly isolated CD4⁺ T helper (Th) cells. This infectious suppressive activity, transferred from CD25⁺ Treg cells via cell contact, is cell contact–independent and partially mediated by soluble transforming growth factor (TGF)-ß. The induction of suppressive properties in conventional CD4⁺ Th cells represents a mechanism underlying the phenomenon of infectious tolerance. This explains previously published conflicting data on the role of TGF-ß in CD25⁺ Treg cell–induced immunosuppression.

Key Words: human regulatory T cells • CD4⁺CD25⁺ T cells • infectious tolerance • T cell inhibition • TGF-ß

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• Zheng, S. G., Wang, J. H., Koss, M. N., Quismorio, F. Jr., Gray, J. D., Horwitz, D. A. (2004). CD4+ and CD8+ Regulatory T Cells Generated Ex Vivo with IL-2 and TGF-{beta} Suppress a Stimulatory Graft-versus-Host Disease with a Lupus-Like Syndrome. J. Immunol. 172: 1531-1539 [Abstract] [Full Text]  
• Chen, W., Jin, W., Hardegen, N., Lei, K.-j., Li, L., Marinos, N., McGrady, G., Wahl, S. M. (2003). 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. 198: 1875-1886 [Abstract] [Full Text]  
• Jonuleit, H., Schmitt, E. (2003). The Regulatory T Cell Family: Distinct Subsets and their Interrelations. J. Immunol. 171: 6323-6327 [Full Text]  
• Koenen, H. J. P. M., Fasse, E., Joosten, I. (2003). IL-15 and Cognate Antigen Successfully Expand De Novo-Induced Human Antigen-Specific Regulatory CD4+ T Cells That Require Antigen-Specific Activation for Suppression. J. Immunol. 171: 6431-6441 [Abstract] [Full Text]  
• Liu, H., Hu, B., Xu, D., Liew, F. Y. (2003). CD4+CD25+ Regulatory T Cells Cure Murine Colitis: The Role of IL-10, TGF-{beta}, and CTLA4. J. Immunol. 171: 5012-5017 [Abstract] [Full Text]  
• Foussat, A., Cottrez, F., Brun, V., Fournier, N., Breittmayer, J.-P., Groux, H. (2003). A Comparative Study between T Regulatory Type 1 and CD4+CD25+ T Cells in the Control of Inflammation. J. Immunol. 171: 5018-5026 [Abstract] [Full Text]  
• Unger, W. W. J., Hauet-Broere, F., Jansen, W., van Berkel, L. A., Kraal, G., Samsom, J. N. (2003). Early Events in Peripheral Regulatory T Cell Induction via the Nasal Mucosa. J. Immunol. 171: 4592-4603 [Abstract] [Full Text]  
• Horwitz, D. A., Zheng, S. G., Gray, J. D. (2003). 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. 74: 471-478 [Abstract] [Full Text]  
• Feunou, P., Poulin, L., Habran, C., Le Moine, A., Goldman, M., Braun, M. Y. (2003). CD4+CD25+ and CD4+CD25- T Cells Act Respectively as Inducer and Effector T Suppressor Cells in Superantigen-Induced Tolerance. J. Immunol. 171: 3475-3484 [Abstract] [Full Text]  
• Green, E. A., Gorelik, L., McGregor, C. M., Tran, E. H., Flavell, R. A. (2003). CD4+CD25+ T regulatory cells control anti-islet CD8+ T cells through TGF-{beta}-TGF-{beta} receptor interactions in type 1 diabetes. Proc. Natl. Acad. Sci. USA 100: 10878-10883 [Abstract] [Full Text]  
• Roelofs-Haarhuis, K., Wu, X., Nowak, M., Fang, M., Artik, S., Gleichmann, E. (2003). Infectious Nickel Tolerance: A Reciprocal Interplay of Tolerogenic APCs and T Suppressor Cells That Is Driven by Immunization. J. Immunol. 171: 2863-2872 [Abstract] [Full Text]  
• Yamazaki, S., Iyoda, T., Tarbell, K., Olson, K., Velinzon, K., Inaba, K., Steinman, R. M. (2003). Direct Expansion of Functional CD25+ CD4+ Regulatory T Cells by Antigen-processing Dendritic Cells. J. Exp. Med. 198: 235-247 [Abstract] [Full Text]  
• Unger, W. W. J., Jansen, W., Wolvers, D. A. W., van Halteren, A. G. S., Kraal, G., Samsom, J. N. (2003). Nasal tolerance induces antigen-specific CD4+CD25- regulatory T cells that can transfer their regulatory capacity to naive CD4+ T cells. Int Immunol 15: 731-739 [Abstract] [Full Text]  

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