J. Exp. Med., Volume 189, Number 2, January 18, 1999 371-380

Fc Receptor-mediated Induction of Dendritic Cell Maturation and Major Histocompatibility Complex Class I-restricted Antigen Presentation after Immune Complex Internalization

By Armelle Regnault,^* Danielle Lankar,^* Valérie Lacabanne,^* Ana Rodriguez,^* Clotilde Théry,^* Maria Rescigno, Takashi Saito, Sjef Verbeek,^§ Christian Bonnerot,^* Paola Ricciardi-Castagnoli, and Sebastian Amigorena^*

From ^* Institut National de la Santé et de la Recherche Médicale CJF 95-01, Institut Curie, Section Recherche, 75005 Paris, France; the  Second University of Milan, Department of Biotechnology and Biological Sciences, 20126 Milan, Italy; the ^§ Department of Immunology, University Hospital, G04.614, 3584 CX, Utrecht, The Netherlands; and the  Division of Molecular Genetics, Graduate School of Medicine, Chiba University, Chuo-ku, Chiba 260-8670, Japan

Dendritic cells (DCs) express several receptors for the Fc portion of immunoglobulin (Ig)G (FcR), which mediate internalization of antigen-IgG complexes (immune complexes, ICs) and promote efficient major histocompatibility complex (MHC) class II-restricted antigen presentation. We now show that FcRs have two additional specific attributes in murine DCs: the induction of DC maturation and the promotion of efficient MHC class I-restricted presentation of peptides from exogenous, IgG-complexed antigens. Both FcR functions require the FcR-associated  chain. FcR-mediated MHC class I-restricted antigen presentation is extremely sensitive and specific to immature DCs. It requires proteasomal degradation and is dependent on functional peptide transporter associated with antigen processing, TAP1-TAP2. By promoting DC maturation and presentation on both MHC class I and II molecules, ICs should efficiently sensitize DCs for priming of both CD4⁺ helper and CD8⁺ cytotoxic T lymphocytes in vivo.

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• Ramakrishna, V., Treml, J. F., Vitale, L., Connolly, J. E., O'Neill, T., Smith, P. A., Jones, C. L., He, L.-Z., Goldstein, J., Wallace, P. K., Keler, T., Endres, M. J. (2004). Mannose Receptor Targeting of Tumor Antigen pmel17 to Human Dendritic Cells Directs Anti-Melanoma T Cell Responses via Multiple HLA Molecules. J. Immunol. 172: 2845-2852 [Abstract] [Full Text]  
• Vermeulen, M., Giordano, M., Trevani, A. S., Sedlik, C., Gamberale, R., Fernandez-Calotti, P., Salamone, G., Raiden, S., Sanjurjo, J., Geffner, J. R. (2004). Acidosis Improves Uptake of Antigens and MHC Class I-Restricted Presentation by Dendritic Cells. J. Immunol. 172: 3196-3204 [Abstract] [Full Text]  
• Heit, A., Huster, K. M., Schmitz, F., Schiemann, M., Busch, D. H., Wagner, H. (2004). CpG-DNA Aided Cross-Priming by Cross-Presenting B Cells. J. Immunol. 172: 1501-1507 [Abstract] [Full Text]  
• Maillard, P., Lavergne, J.-P., Siberil, S., Faure, G., Roohvand, F., Petres, S., Teillaud, J. L., Budkowska, A. (2004). Fc{gamma} Receptor-like Activity of Hepatitis C Virus Core Protein. J. Biol. Chem. 279: 2430-2437 [Abstract] [Full Text]  
• Lambert, S. L., Okada, C. Y., Levy, R. (2004). TCR Vaccines against a Murine T Cell Lymphoma: A Primary Role for Antibodies of the IgG2c Class in Tumor Protection. J. Immunol. 172: 929-936 [Abstract] [Full Text]  
• Prina, E., Abdi, S. Z., Lebastard, M., Perret, E., Winter, N., Antoine, J.-C. (2004). Dendritic cells as host cells for the promastigote and amastigote stages of Leishmania amazonensis: the role of opsonins in parasite uptake and dendritic cell maturation. J. Cell Sci. 117: 315-325 [Abstract] [Full Text]  
• Stebbing, J., Savage, P., Patterson, S., Gazzard, B. (2004). All for CD91 and CD91 for all. J Antimicrob Chemother 53: 1-3 [Abstract] [Full Text]  
• Romani, L., Montagnoli, C., Bozza, S., Perruccio, K., Spreca, A., Allavena, P., Verbeek, S., Calderone, R. A., Bistoni, F., Puccetti, P. (2004). The exploitation of distinct recognition receptors in dendritic cells determines the full range of host immune relationships with Candida albicans. Int Immunol 16: 149-161 [Abstract] [Full Text]  
• Benvenuti, F., Lagaudriere-Gesbert, C., Grandjean, I., Jancic, C., Hivroz, C., Trautmann, A., Lantz, O., Amigorena, S. (2004). Dendritic Cell Maturation Controls Adhesion, Synapse Formation, and the Duration of the Interactions with Naive T Lymphocytes. J. Immunol. 172: 292-301 [Abstract] [Full Text]  
• Fernandez, N., Renedo, M., Alonso, S., Crespo, M. S. (2003). Release of Arachidonic Acid by Stimulation of Opsonic Receptors in Human Monocytes: THE Fc{gamma}R AND THE COMPLEMENT RECEPTOR 3 PATHWAYS. J. Biol. Chem. 278: 52179-52187 [Abstract] [Full Text]  
• Buatois, V., Baillet, M., Becart, S., Mooney, N., Leserman, L., Machy, P. (2003). MHC Class II-Peptide Complexes in Dendritic Cell Lipid Microdomains Initiate the CD4 Th1 Phenotype. J. Immunol. 171: 5812-5819 [Abstract] [Full Text]  
• Weng, W.-K., Levy, R. (2003). Two Immunoglobulin G Fragment C Receptor Polymorphisms Independently Predict Response to Rituximab in Patients With Follicular Lymphoma. JCO 21: 3940-3947 [Abstract] [Full Text]  
• Cao, W., Bobryshev, Y. V, Lord, R. S.A, Oakley, R. E.I, Lee, S. H, Lu, J. (2003). Dendritic cells in the arterial wall express C1q: potential significance in atherogenesis. Cardiovasc Res 60: 175-186 [Abstract] [Full Text]  
• Moron, V. G., Rueda, P., Sedlik, C., Leclerc, C. (2003). In Vivo, Dendritic Cells Can Cross-Present Virus-Like Particles Using an Endosome-to-Cytosol Pathway. J. Immunol. 171: 2242-2250 [Abstract] [Full Text]  
• Wolpoe, M. E., Lutz, E. R., Ercolini, A. M., Murata, S., Ivie, S. E., Garrett, E. S., Emens, L. A., Jaffee, E. M., Reilly, R. T. (2003). HER-2/neu-Specific Monoclonal Antibodies Collaborate with HER-2/neu-Targeted Granulocyte Macrophage Colony-Stimulating Factor Secreting Whole Cell Vaccination to Augment CD8+ T Cell Effector Function and Tumor-Free Survival in Her-2/neu-Transgenic Mice. J. Immunol. 171: 2161-2169 [Abstract] [Full Text]  
• Delamarre, L., Holcombe, H., Mellman, I. (2003). Presentation of Exogenous Antigens on Major Histocompatibility Complex (MHC) Class I and MHC Class II Molecules Is Differentially Regulated during Dendritic Cell Maturation. J. Exp. Med. 198: 111-122 [Abstract] [Full Text]  
• Fausch, S. C., Da Silva, D. M., Kast, W. M. (2003). Differential Uptake and Cross-Presentation of Human Papillomavirus Virus-like Particles by Dendritic Cells and Langerhans Cells. Cancer Res. 63: 3478-3482 [Abstract] [Full Text]  
• Bell, J., Gray, D. (2003). Antigen-capturing Cells Can Masquerade as Memory B Cells. J. Exp. Med. 197: 1233-1244 [Abstract] [Full Text]  

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