Original Article

Induction of Interleukin 10–producing, Nonproliferating CD4⁺ T Cells with Regulatory Properties by Repetitive Stimulation with Allogeneic Immature Human Dendritic Cells

Correspondence to: Helmut Jonuleit, Dept. of Dermatology, University of Mainz, D-55101 Mainz, Germany. Tel:49-6131-173541 Fax:49-6131-17473541

The functional properties of dendritic cells (DCs) are strictly dependent on their maturational state. To analyze the influence of the maturational state of DCs on priming and differentiation of T cells, immature CD83^- and mature CD83⁺ human DCs were used for stimulation of naive, allogeneic CD4⁺ T cells. Repetitive stimulation with mature DCs resulted in a strong expansion of alloreactive T cells and the exclusive development of T helper type 1 (Th1) cells. In contrast, after repetitive stimulation with immature DCs the alloreactive T cells showed an irreversibly inhibited proliferation that could not be restored by restimulation with mature DCs or peripheral blood mononuclear cells, or by the addition of interleukin (IL)-2. Only stimulation of T cells with mature DCs resulted in an upregulation of CD154, CD69, and CD70, whereas T cells activated with immature DCs showed an early upregulation of the negative regulator cytotoxic T lymphocyte–associated molecule 4 (CTLA-4). These T cells lost their ability to produce interferon , IL-2, or IL-4 after several stimulations with immature DCs and differentiated into nonproliferating, IL-10–producing T cells. Furthermore, in coculture experiments these T cells inhibited the antigen-driven proliferation of Th1 cells in a contact- and dose-dependent, but antigen-nonspecific manner. These data show that immature and mature DCs induce different types of T cell responses: inflammatory Th1 cells are induced by mature DCs, and IL-10–producing T cell regulatory 1–like cells by immature DCs.

Key Words: dendritic cells, regulatory T cells, T helper type 1 cells, interleukin 10, T cell differentiation

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• Bruder, D., Westendorf, A. M., Hansen, W., Prettin, S., Gruber, A. D., Qian, Y., von Boehmer, H., Mahnke, K., Buer, J. (2005). On the Edge of Autoimmunity: T-Cell Stimulation by Steady-State Dendritic Cells Prevents Autoimmune Diabetes. Diabetes 54: 3395-3401 [Abstract] [Full Text]  
• Rubio, M. T., Means, T. K., Chakraverty, R., Shaffer, J., Fudaba, Y., Chittenden, M., Luster, A. D., Sykes, M. (2005). Maturation of human monocyte-derived dendritic cells (MoDCs) in the presence of prostaglandin E2 optimizes CD4 and CD8 T cell-mediated responses to protein antigens: role of PGE2 in chemokine and cytokine expression by MoDCs. Int Immunol 17: 1561-1572 [Abstract] [Full Text]  
• Thum, T., Bauersachs, J., Poole-Wilson, P. A., Volk, H.-D., Anker, S. D. (2005). The Dying Stem Cell Hypothesis: Immune Modulation as a Novel Mechanism for Progenitor Cell Therapy in Cardiac Muscle. J Am Coll Cardiol 46: 1799-1802 [Abstract] [Full Text]  
• Skapenko, A., Kalden, J. R., Lipsky, P. E., Schulze-Koops, H. (2005). The IL-4 Receptor {alpha}-Chain-Binding Cytokines, IL-4 and IL-13, Induce Forkhead Box P3-Expressing CD25+CD4+ Regulatory T Cells from CD25-CD4+ Precursors. J. Immunol. 175: 6107-6116 [Abstract] [Full Text]  
• Schimmelpfennig, C. H., Schulz, S., Arber, C., Baker, J., Tarner, I., McBride, J., Contag, C. H., Negrin, R. S. (2005). Ex Vivo Expanded Dendritic Cells Home to T-Cell Zones of Lymphoid Organs and Survive in Vivo after Allogeneic Bone Marrow Transplantation. Am. J. Pathol. 167: 1321-1331 [Abstract] [Full Text]  
• Sen, Y., Yongyi, B., Yuling, H., Luokun, X., Li, H., Jie, X., Tao, D., Gang, Z., Junyan, L., Chunsong, H., Zhang, X., Youxin, J., Feili, G., Boquan, J., Jinquan, T. (2005). V{alpha}24-Invariant NKT Cells from Patients with Allergic Asthma Express CCR9 at High Frequency and Induce Th2 Bias of CD3+ T Cells upon CD226 Engagement. J. Immunol. 175: 4914-4926 [Abstract] [Full Text]  
• Breckpot, K., Corthals, J., Bonehill, A., Michiels, A., Tuyaerts, S., Aerts, C., Heirman, C., Thielemans, K. (2005). Dendritic cells differentiated in the presence of IFN-{beta} and IL-3 are potent inducers of an antigen-specific CD8+ T cell response. J. Leukoc. Biol. 78: 898-908 [Abstract] [Full Text]  
• Chorny, A., Gonzalez-Rey, E., Fernandez-Martin, A., Pozo, D., Ganea, D., Delgado, M. (2005). Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc. Natl. Acad. Sci. USA 102: 13562-13567 [Abstract] [Full Text]  
• Beyer, M., Kochanek, M., Darabi, K., Popov, A., Jensen, M., Endl, E., Knolle, P. A., Thomas, R. K., von Bergwelt-Baildon, M., Debey, S., Hallek, M., Schultze, J. L. (2005). Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 106: 2018-2025 [Abstract] [Full Text]  
• Zhang, X., Huang, H., Yuan, J., Sun, D., Hou, W.-S., Gordon, J., Xiang, J. (2005). CD4-8- Dendritic Cells Prime CD4+ T Regulatory 1 Cells to Suppress Antitumor Immunity. J. Immunol. 175: 2931-2937 [Abstract] [Full Text]  
• Tan, J. K. H., O'Neill, H. C. (2005). Maturation requirements for dendritic cells in T cell stimulation leading to tolerance versus immunity. J. Leukoc. Biol. 78: 319-324 [Abstract] [Full Text]  
• Rossi, M., Young, J. W. (2005). Human Dendritic Cells: Potent Antigen-Presenting Cells at the Crossroads of Innate and Adaptive Immunity. J. Immunol. 175: 1373-1381 [Abstract] [Full Text]  
• Baratelli, F., Lin, Y., Zhu, L., Yang, S.-C., Heuze-Vourc'h, N., Zeng, G., Reckamp, K., Dohadwala, M., Sharma, S., Dubinett, S. M. (2005). Prostaglandin E2 Induces FOXP3 Gene Expression and T Regulatory Cell Function in Human CD4+ T Cells. J. Immunol. 175: 1483-1490 [Abstract] [Full Text]  
• Herter, S., Osterloh, P., Hilf, N., Rechtsteiner, G., Hohfeld, J., Rammensee, H.-G., Schild, H. (2005). Dendritic Cell Aggresome-Like-Induced Structure Formation and Delayed Antigen Presentation Coincide in Influenza Virus-Infected Dendritic Cells. J. Immunol. 175: 891-898 [Abstract] [Full Text]  
• Schutyser, E., Richmond, A., Van Damme, J. (2005). Involvement of CC chemokine ligand 18 (CCL18) in normal and pathological processes. J. Leukoc. Biol. 78: 14-26 [Abstract] [Full Text]  

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