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CD8⁺ and CD8^– Subclasses of Dendritic Cells Direct the Development of Distinct T Helper Cells In Vivo

Roberto Maldonado-López^*, Thibaut De Smedt^*, Patrick Michel, Jacques Godfroid, Bernard Pajak^*, Carlo Heirman, Kris Thielemans, Oberdan Leo^*, Jacques Urbain^*, and Muriel Moser^*

From the ^* Département de Biologie Moléculaire, Université Libre de Bruxelles, B-1640 Rhode-Saint-Genèse, Belgium; Veterinary and Agrochemical Research Center, B-1180 Brussels, Belgium; and Laboratorium of Hematologie-Immunologie, Vrije Universiteit Brussel, B-1090 Brussels, Belgium

Cells of the dendritic family display some unique properties that confer to them the capacity to sensitize naive T cells in vitro and in vivo. In the mouse, two subclasses of dendritic cells (DCs) have been described that differ by their CD8 expression and their localization in lymphoid organs. The physiologic function of both cell populations remains obscure. Studies conducted in vitro have suggested that CD8⁺ DCs could play a role in the regulation of immune responses, whereas conventional CD8^– DCs would be more stimulatory. We report here that both subclasses of DCs efficiently prime antigen-specific T cells in vivo, and direct the development of distinct T helper (Th) populations. Antigen-pulsed CD8⁺ and CD8^– DCs are separated after overnight culture in recombinant granulocyte/macrophage colony-stimulating factor and injected into the footpads of syngeneic mice. Administration of CD8^– DCs induces a Th2-type response, whereas injection of CD8⁺ DCs leads to Th1 differentiation. We further show that interleukin 12 plays a critical role in Th1 development by CD8⁺ DCs. These findings suggest that the nature of the DC that presents the antigen to naive T cells may dictate the class selection of the adaptative immune response.

Key Words: primary response • T helper cell type 1/type 2 balance • interleukin 12 • tolerance • memory

The Laboratory of Animal Physiology was supported by grants of the Fonds National de la Recherche Scientifique/Télévie, by the Fonds de la Recherche Fondamentale Collective, by the European Commission (CEC TMR Network Contract FMRX-CT96-0053), and by the Belgian Programme on Interuniversity Poles of Attraction initiated by the Belgian State, Prime Minister's Office, Science Policy Programming. R. Maldonado, T. De Smedt, and M. Moser are supported by the Fonds National de la Recherche Scientifique.

¹ Abbreviation used in this paper: DC, dendritic cell.

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• Curtsinger, J. M., Valenzuela, J. O., Agarwal, P., Lins, D., Mescher, M. F. (2005). Cutting Edge: Type I IFNs Provide a Third Signal to CD8 T Cells to Stimulate Clonal Expansion and Differentiation. J. Immunol. 174: 4465-4469 [Abstract] [Full Text]  
• Hanada, T., Tanaka, K., Matsumura, Y., Yamauchi, M., Nishinakamura, H., Aburatani, H., Mashima, R., Kubo, M., Kobayashi, T., Yoshimura, A. (2005). Induction of Hyper Th1 Cell-Type Immune Responses by Dendritic Cells Lacking the Suppressor of Cytokine Signaling-1 Gene. J. Immunol. 174: 4325-4332 [Abstract] [Full Text]  
• Pulendran, B. (2005). Variegation of the Immune Response with Dendritic Cells and Pathogen Recognition Receptors. J. Immunol. 174: 2457-2465 [Abstract] [Full Text]  
• Wirtz, S., Becker, C., Fantini, M. C., Nieuwenhuis, E. E., Tubbe, I., Galle, P. R., Schild, H.-J., Birkenbach, M., Blumberg, R. S., Neurath, M. F. (2005). EBV-Induced Gene 3 Transcription Is Induced by TLR Signaling in Primary Dendritic Cells via NF-{kappa}B Activation. J. Immunol. 174: 2814-2824 [Abstract] [Full Text]  
• Montoya, M., Edwards, M. J., Reid, D. M., Borrow, P. (2005). Rapid Activation of Spleen Dendritic Cell Subsets following Lymphocytic Choriomeningitis Virus Infection of Mice: Analysis of the Involvement of Type 1 IFN. J. Immunol. 174: 1851-1861 [Abstract] [Full Text]  
• Yasumi, T., Katamura, K., Okafuji, I., Yoshioka, T., Meguro, T.-a., Nishikomori, R., Kusunoki, T., Heike, T., Nakahata, T. (2005). Limited Ability of Antigen-Specific Th1 Responses to Inhibit Th2 Cell Development In Vivo. J. Immunol. 174: 1325-1331 [Abstract] [Full Text]  
• Oriss, T. B., Ostroukhova, M., Seguin-Devaux, C., Dixon-McCarthy, B., Stolz, D. B., Watkins, S. C., Pillemer, B., Ray, P., Ray, A. (2005). Dynamics of Dendritic Cell Phenotype and Interactions with CD4+ T Cells in Airway Inflammation and Tolerance. J. Immunol. 174: 854-863 [Abstract] [Full Text]  
• Andris, F., Denanglaire, S., de Mattia, F., Urbain, J., Leo, O. (2004). Naive T Cells Are Resistant to Anergy Induction by Anti-CD3 Antibodies. J. Immunol. 173: 3201-3208 [Abstract] [Full Text]  
• Rivas-Carvalho, A., Meraz-Rios, M. A., Santos-Argumedo, L., Bajana, S., Soldevila, G., Moreno-Garcia, M. E., Sanchez-Torres, C. (2004). CD16+ human monocyte-derived dendritic cells matured with different and unrelated stimuli promote similar allogeneic Th2 responses: regulation by pro- and anti-inflammatory cytokines. Int Immunol 16: 1251-1263 [Abstract] [Full Text]  
• Chang, W. L. W., Baumgarth, N., Yu, D., Barry, P. A. (2004). Human Cytomegalovirus-Encoded Interleukin-10 Homolog Inhibits Maturation of Dendritic Cells and Alters Their Functionality. J. Virol. 78: 8720-8731 [Abstract] [Full Text]  
• Jankovic, D., Kullberg, M. C., Caspar, P., Sher, A. (2004). Parasite-Induced Th2 Polarization Is Associated with Down-Regulated Dendritic Cell Responsiveness to Th1 Stimuli and a Transient Delay in T Lymphocyte Cycling. J. Immunol. 173: 2419-2427 [Abstract] [Full Text]  
• Yang, R., Murillo, F. M., Lin, K.-Y., Yutzy, W. H. IV, Uematsu, S., Takeda, K., Akira, S., Viscidi, R. P., Roden, R. B. S. (2004). Human Papillomavirus Type-16 Virus-Like Particles Activate Complementary Defense Responses in Key Dendritic Cell Subpopulations. J. Immunol. 173: 2624-2631 [Abstract] [Full Text]  
• Teleshova, N., Kenney, J., Jones, J., Marshall, J., Van Nest, G., Dufour, J., Bohm, R., Lifson, J. D., Gettie, A., Pope, M. (2004). CpG-C Immunostimulatory Oligodeoxyribonucleotide Activation of Plasmacytoid Dendritic Cells in Rhesus Macaques to Augment the Activation of IFN-{gamma}-Secreting Simian Immunodeficiency Virus-Specific T Cells. J. Immunol. 173: 1647-1657 [Abstract] [Full Text]  
• Marino, S., Pawar, S., Fuller, C. L., Reinhart, T. A., Flynn, J. L., Kirschner, D. E. (2004). Dendritic Cell Trafficking and Antigen Presentation in the Human Immune Response to Mycobacterium tuberculosis. J. Immunol. 173: 494-506 [Abstract] [Full Text]  

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