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Original Article

^a Laboratory of Virology, Istituto Superiore di Sanità, 00161 Rome, Italy
Laboratory of Virology, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy.39-06-4990-209739-06-4990-3290

belard{at}iss.it

Type I interferons (IFNs) are cytokines exhibiting antiviral and antitumor effects, including multiple activities on immune cells. However, the importance of these cytokines in the early events leading to the generation of an immune response is still unclear. Here, we have investigated the effects of type I IFNs on freshly isolated granulocyte/macrophage colony-stimulating factor (GM-CSF)–treated human monocytes in terms of dendritic cell (DC) differentiation and activity in vitro and in severe combined immunodeficiency mice reconstituted with human peripheral blood leukocytes (hu-PBL-SCID) mice. Type I IFNs induced a surprisingly rapid maturation of monocytes into short-lived tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)–expressing DCs endowed with potent functional activities, superior with respect to the interleukin (IL)-4/GM-CSF treatment, as shown by FACS^® analyses, mixed leukocyte reaction assays with allogeneic PBLs, and lymphocyte proliferation responses to HIV-1–pulsed autologous DCs. Type I IFN induced IL-15 production and strongly promoted a T helper cell type 1 response. Notably, injection of IFN-treated HIV-1–pulsed DCs in SCID mice reconstituted with autologous PBLs resulted in the generation of a potent primary immune response, as evaluated by the detection of human antibodies to various HIV-1 antigens. These results provide a rationale for using type I IFNs as vaccine adjuvants and support the concept that a natural alliance between these cytokines and monocytes/DCs represents an important early mechanism for connecting innate and adaptive immunity.

Key Words: interferon • dendritic cell maturation and activation • monocytes • SCID mice • immunity

Abbreviations used in this paper: AT, aldrithiol; CIFN, consensus IFN; DC, dendritic cell; ELISPOT, enzyme-linked immunospot; GFP, green fluorescent protein; hu, human; RT, reverse transcription; s, soluble; TRAIL, TNF-related apoptosis-inducing ligand.

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• Yoshida, A., Tanaka, R., Murakami, T., Takahashi, Y., Koyanagi, Y., Nakamura, M., Ito, M., Yamamoto, N., Tanaka, Y. (2003). Induction of Protective Immune Responses against R5 Human Immunodeficiency Virus Type 1 (HIV-1) Infection in hu-PBL-SCID Mice by Intrasplenic Immunization with HIV-1-Pulsed Dendritic Cells: Possible Involvement of a Novel Factor of Human CD4+ T-Cell Origin. J. Virol. 77: 8719-8728 [Abstract] [Full Text]  
• Lapenta, C., Santini, S. M., Logozzi, M., Spada, M., Andreotti, M., Di Pucchio, T., Parlato, S., Belardelli, F. (2003). Potent Immune Response against HIV-1 and Protection from Virus Challenge in hu-PBL-SCID Mice Immunized with Inactivated Virus-pulsed Dendritic Cells Generated in the Presence of IFN-{alpha}. JEM 198: 361-367 [Abstract] [Full Text]  
• Moschella, F., Bisikirska, B., Maffei, A., Papadopoulos, K. P., Skerrett, D., Liu, Z., Hesdorffer, C. S., Harris, P. E. (2003). Gene Expression Profiling and Functional Activity of Human Dendritic Cells Induced with IFN-{alpha}-2b: Implications for Cancer Immunotherapy. Clin. Cancer Res. 9: 2022-2031 [Abstract] [Full Text]  
• Santodonato, L., D'Agostino, G., Nisini, R., Mariotti, S., Monque, D. M., Spada, M., Lattanzi, L., Paola Perrone, M., Andreotti, M., Belardelli, F., Ferrantini, M. (2003). Monocyte-Derived Dendritic Cells Generated After a Short-Term Culture with IFN-{alpha} and Granulocyte-Macrophage Colony-Stimulating Factor Stimulate a Potent Epstein-Barr Virus-Specific CD8+ T Cell Response. J. Immunol. 170: 5195-5202 [Abstract] [Full Text]  
• Fonteneau, J.-F., Gilliet, M., Larsson, M., Dasilva, I., Munz, C., Liu, Y.-J., Bhardwaj, N. (2003). Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood 101: 3520-3526 [Abstract] [Full Text]  
• Dauer, M., Obermaier, B., Herten, J., Haerle, C., Pohl, K., Rothenfusser, S., Schnurr, M., Endres, S., Eigler, A. (2003). Mature Dendritic Cells Derived from Human Monocytes Within 48 Hours: A Novel Strategy for Dendritic Cell Differentiation from Blood Precursors. J. Immunol. 170: 4069-4076 [Abstract] [Full Text]  
• Krug, A., Rothenfusser, S., Selinger, S., Bock, C., Kerkmann, M., Battiany, J., Sarris, A., Giese, T., Speiser, D., Endres, S., Hartmann, G. (2003). CpG-A Oligonucleotides Induce a Monocyte-Derived Dendritic Cell-Like Phenotype That Preferentially Activates CD8 T Cells. J. Immunol. 170: 3468-3477 [Abstract] [Full Text]  
• Yonezawa, A., Morita, R., Takaori-Kondo, A., Kadowaki, N., Kitawaki, T., Hori, T., Uchiyama, T. (2003). Natural Alpha Interferon-Producing Cells Respond to Human Immunodeficiency Virus Type 1 with Alpha Interferon Production and Maturation into Dendritic Cells. J. Virol. 77: 3777-3784 [Abstract] [Full Text]  
• Lande, R., Giacomini, E., Grassi, T., Remoli, M. E., Iona, E., Miettinen, M., Julkunen, I., Coccia, E. M. (2003). IFN-{alpha}{beta} Released by Mycobacterium tuberculosis-Infected Human Dendritic Cells Induces the Expression of CXCL10: Selective Recruitment of NK and Activated T Cells. J. Immunol. 170: 1174-1182 [Abstract] [Full Text]  
• Qu, C., Moran, T. M., Randolph, G. J. (2003). Autocrine Type I IFN and Contact with Endothelium Promote the Presentation of Influenza A Virus by Monocyte-Derived APC. J. Immunol. 170: 1010-1018 [Abstract] [Full Text]  
• Schiavoni, G., Mattei, F., Sestili, P., Borghi, P., Venditti, M., Morse, H. C. III, Belardelli, F., Gabriele, L. (2002). ICSBP Is Essential for the Development of Mouse Type I Interferon-producing Cells and for the Generation and Activation of CD8{alpha}+ Dendritic Cells. JEM 196: 1415-1425 [Abstract] [Full Text]  
• Robertson, N. M., Zangrilli, J. G., Steplewski, A., Hastie, A., Lindemeyer, R. G., Planeta, M. A., Smith, M. K., Innocent, N., Musani, A., Pascual, R., Peters, S., Litwack, G. (2002). Differential Expression of TRAIL and TRAIL Receptors in Allergic Asthmatics Following Segmental Antigen Challenge: Evidence for a Role of TRAIL in Eosinophil Survival. J. Immunol. 169: 5986-5996 [Abstract] [Full Text]  
• Holtl, L., Zelle-Rieser, C., Gander, H., Papesh, C., Ramoner, R., Bartsch, G., Rogatsch, H., Barsoum, A. L., Coggin, J. H. Jr., Thurnher, M. (2002). Immunotherapy of Metastatic Renal Cell Carcinoma with Tumor Lysate-pulsed Autologous Dendritic Cells. Clin. Cancer Res. 8: 3369-3376 [Abstract] [Full Text]  
• Gauzzi, M. C., Canini, I., Eid, P., Belardelli, F., Gessani, S. (2002). Loss of Type I IFN Receptors and Impaired IFN Responsiveness During Terminal Maturation of Monocyte-Derived Human Dendritic Cells. J. Immunol. 169: 3038-3045 [Abstract] [Full Text]  
• Randolph, G. J., Sanchez-Schmitz, G., Liebman, R. M., Schakel, K. (2002). The CD16+ (Fc{gamma}RIII+) Subset of Human Monocytes Preferentially Becomes Migratory Dendritic Cells in a Model Tissue Setting. JEM 196: 517-527 [Abstract] [Full Text]  
• Abel, K., Alegria-Hartman, M. J., Rothaeusler, K., Marthas, M., Miller, C. J. (2002). The Relationship between Simian Immunodeficiency Virus RNA Levels and the mRNA Levels of Alpha/Beta Interferons (IFN-{alpha}/{beta}) and IFN-{alpha}/{beta}-Inducible Mx in Lymphoid Tissues of Rhesus Macaques during Acute and Chronic Infection. J. Virol. 76: 8433-8445 [Abstract] [Full Text]  
• Remoli, M. E., Giacomini, E., Lutfalla, G., Dondi, E., Orefici, G., Battistini, A., Uze, G., Pellegrini, S., Coccia, E. M. (2002). Selective Expression of Type I IFN Genes in Human Dendritic Cells Infected with Mycobacterium tuberculosis. J. Immunol. 169: 366-374 [Abstract] [Full Text]  
• Proietti, E., Bracci, L., Puzelli, S., Di Pucchio, T., Sestili, P., De Vincenzi, E., Venditti, M., Capone, I., Seif, I., De Maeyer, E., Tough, D., Donatelli, I., Belardelli, F. (2002). Type I IFN as a Natural Adjuvant for a Protective Immune Response: Lessons from the Influenza Vaccine Model. J. Immunol. 169: 375-383 [Abstract] [Full Text]  
• Montoya, M., Schiavoni, G., Mattei, F., Gresser, I., Belardelli, F., Borrow, P., Tough, D. F. (2002). Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99: 3263-3271 [Abstract] [Full Text]  
• Poluektova, L. Y., Munn, D. H., Persidsky, Y., Gendelman, H. E. (2002). Generation of Cytotoxic T Cells Against Virus-Infected Human Brain Macrophages in a Murine Model of HIV-1 Encephalitis. J. Immunol. 168: 3941-3949 [Abstract] [Full Text]  
• Padovan, E., Spagnoli, G. C., Ferrantini, M., Heberer, M. (2002). IFN-{alpha}2a induces IP-10/CXCL10 and MIG/CXCL9 production in monocyte-derived dendritic cells and enhances their capacity to attract and stimulate CD8+ effector T cells. J. Leukoc. Biol. 71: 669-676 [Abstract] [Full Text]  
• Luft, T., Luetjens, P., Hochrein, H., Toy, T., Masterman, K.-A., Rizkalla, M., Maliszewski, C., Shortman, K., Cebon, J., Maraskovsky, E. (2002). IFN-{alpha} enhances CD40 ligand-mediated activation of immature monocyte-derived dendritic cells. Int Immunol 14: 367-380 [Abstract] [Full Text]  
• Buelens, C., Bartholome, E. J., Amraoui, Z., Boutriaux, M., Salmon, I., Thielemans, K., Willems, F., Goldman, M. (2002). Interleukin-3 and interferon beta cooperate to induce differentiation of monocytes into dendritic cells with potent helper T-cell stimulatory properties. Blood 99: 993-998 [Abstract] [Full Text]  

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