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Claudia Winzler^*, Patrizia Rovere, Maria Rescigno^*, Francesca Granucci^*, Giuseppe Penna, Luciano Adorini, Valerie S. Zimmermann, Jean Davoust, and Paola Ricciardi-Castagnoli^*

From the ^* CNR Centre of Cellular and Molecular Pharmacology, Milan 20129, Italy; Roche Milano Ricerche, Milan 20132, Italy; Centre d'Immunologie INSERM-CNRS de Marseille Luminy, Parc Scientifique de Luminy, Case 906, Marseille 13288, France

The signals controlling the checkpoints of dendritic cells (DC) maturation and the correlation between phenotypical and functional maturational stages were investigated in a defined model system of growth factor–dependent immature mouse DC. Three sequential stages of DC maturation (immature, mature, and apoptotic) were defined and characterized. Immature DC (stage 1) had low expression of costimulatory molecules, highly organized cytoskeleton, focal adhesion plaques, and slow motility; accordingly, they were very efficient in antigen uptake and processing of soluble proteins. Further, at this stage most of major histocompatibility complex class II molecules were within cytoplasmic compartments consistent with a poor allostimulatory capacity. Bacteria or cytokines were very efficient in inducing progression from stage 1 towards stage 2 (mature). Morphological changes were observed by confocal analysis including depolymerization of F-actin and loss of vinculin containing adhesive structures which correlates with acquisition of high motility. Antigen uptake and presentation of native protein antigen was reduced. In contrast, presentation of immunogenic peptides and allostimulatory activity became very efficient and secretion of IL-12 p75 was detectable after antigen presentation. This functional DC maturation ended by apoptotic cell death, and no reversion to the immature phenotype was observed.

This work was supported by the Italian Ministry of Public Health (Istituto Superiore di Sanità: AIDS grant 9403-92 and MS grant 52), by the National Council Research (CNR), by Biotop, and by the French Association against Cancer, grant 6058 (ARC).

¹ Abbreviations used in this paper: DC, dendritic cells; LC, Langerhans cells; SN, supernatant.

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• Kalupahana, R., Emilianus, A. R., Maskell, D., Blacklaws, B. (2003). Salmonella enterica Serovar Typhimurium Expressing Mutant Lipid A with Decreased Endotoxicity Causes Maturation of Murine Dendritic Cells. Infect. Immun. 71: 6132-6140 [Abstract] [Full Text]  
• QUARANTA, M. G., MATTIOLI, B., SPADARO, F., STRAFACE, E., GIORDANI, L., RAMONI, C., MALORNI, W., VIORA, M. (2003). HIV-1 Nef triggers Vav-mediated signaling pathway leading to functional and morphological differentiation of dendritic cells. FASEB J. 17: 2025-2036 [Abstract] [Full Text]  
• Granucci, F., Petralia, F., Urbano, M., Citterio, S., Di Tota, F., Santambrogio, L., Ricciardi-Castagnoli, P. (2003). The scavenger receptor MARCO mediates cytoskeleton rearrangements in dendritic cells and microglia. Blood 102: 2940-2947 [Abstract] [Full Text]  
• Haicheur, N., Benchetrit, F., Amessou, M., Leclerc, C., Falguieres, T., Fayolle, C., Bismuth, E., Fridman, W. H., Johannes, L., Tartour, E. (2003). The B subunit of Shiga toxin coupled to full-size antigenic protein elicits humoral and cell-mediated immune responses associated with a Th1-dominant polarization. Int Immunol 15: 1161-1171 [Abstract] [Full Text]  
• Colino, J., Snapper, C. M. (2003). Opposing Signals from Pathogen-Associated Molecular Patterns and IL-10 Are Critical for Optimal Dendritic Cell Induction of In Vivo Humoral Immunity to Streptococcus pneumoniae. J. Immunol. 171: 3508-3519 [Abstract] [Full Text]  
• Wilson, N. S., El-Sukkari, D., Belz, G. T., Smith, C. M., Steptoe, R. J., Heath, W. R., Shortman, K., Villadangos, J. A. (2003). Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102: 2187-2194 [Abstract] [Full Text]  
• Bajenoff, M., Granjeaud, S., Guerder, S. (2003). The Strategy of T Cell Antigen-presenting Cell Encounter in Antigen-draining Lymph Nodes Revealed by Imaging of Initial T Cell Activation. JEM 198: 715-724 [Abstract] [Full Text]  
• Xu, S., Koski, G. K., Faries, M., Bedrosian, I., Mick, R., Maeurer, M., Cheever, M. A., Cohen, P. A., Czerniecki, B. J. (2003). Rapid High Efficiency Sensitization of CD8+ T Cells to Tumor Antigens by Dendritic Cells Leads to Enhanced Functional Avidity and Direct Tumor Recognition Through an IL-12-Dependent Mechanism. J. Immunol. 171: 2251-2261 [Abstract] [Full Text]  
• Nakahara, S., Tsunoda, T., Baba, T., Asabe, S., Tahara, H. (2003). Dendritic Cells Stimulated with a Bacterial Product, OK-432, Efficiently Induce Cytotoxic T Lymphocytes Specific to Tumor Rejection Peptide. Cancer Res. 63: 4112-4118 [Abstract] [Full Text]  
• Hafalla, J. C. R., Morrot, A., Sano, G.-i., Milon, G., Lafaille, J. J., Zavala, F. (2003). Early Self-Regulatory Mechanisms Control the Magnitude of CD8+ T Cell Responses Against Liver Stages of Murine Malaria. J. Immunol. 171: 964-970 [Abstract] [Full Text]  
• Geuze, H. J., Murk, J. L., Stroobants, A. K., Griffith, J. M., Kleijmeer, M. J., Koster, A. J., Verkleij, A. J., Distel, B., Tabak, H. F. (2003). Involvement of the Endoplasmic Reticulum in Peroxisome Formation. Mol. Biol. Cell 14: 2900-2907 [Abstract] [Full Text]  
• Yanagawa, Y., Onoe, K. (2003). CCR7 ligands induce rapid endocytosis in mature dendritic cells with concomitant up-regulation of Cdc42 and Rac activities. Blood 101: 4923-4929 [Abstract] [Full Text]  
• Granucci, F., Feau, S., Angeli, V., Trottein, F., Ricciardi-Castagnoli, P. (2003). Early IL-2 Production by Mouse Dendritic Cells Is the Result of Microbial-Induced Priming. J. Immunol. 170: 5075-5081 [Abstract] [Full Text]  
• Angeli, V., Hammad, H., Staels, B., Capron, M., Lambrecht, B. N., Trottein, F. (2003). Peroxisome Proliferator-Activated Receptor {gamma} Inhibits the Migration of Dendritic Cells: Consequences for the Immune Response. J. Immunol. 170: 5295-5301 [Abstract] [Full Text]  
• TURECI, O., BIAN, H., NESTLE, F. O., RADDRIZZANI, L., ROSINSKI, J. A., TASSIS, A., HILTON, H., WALSTEAD, M., SAHIN, U., HAMMER, J. (2003). Cascades of transcriptional induction during dendritic cell maturation revealed by genome-wide expression analysis. FASEB J. 17: 836-847 [Abstract] [Full Text]  
• Datta, S. K., Redecke, V., Prilliman, K. R., Takabayashi, K., Corr, M., Tallant, T., DiDonato, J., Dziarski, R., Akira, S., Schoenberger, S. P., Raz, E. (2003). A Subset of Toll-Like Receptor Ligands Induces Cross-presentation by Bone Marrow-Derived Dendritic Cells. J. Immunol. 170: 4102-4110 [Abstract] [Full Text]  
• Vorderstrasse, B. A., Dearstyne, E. A., Kerkvliet, N. I. (2003). Influence of 2,3,7,8-Tetrachlorodibenzo-p-dioxin on the Antigen-Presenting Activity of Dendritic Cells. Toxicol Sci 72: 103-112 [Abstract] [Full Text]  
• Mueller, S. N., Jones, C. M., Chen, W., Kawaoka, Y., Castrucci, M. R., Heath, W. R., Carbone, F. R. (2003). The Early Expression of Glycoprotein B from Herpes Simplex Virus Can Be Detected by Antigen-Specific CD8+ T Cells. J. Virol. 77: 2445-2451 [Abstract] [Full Text]  
• Ocana-Morgner, C., Mota, M. M., Rodriguez, A. (2003). Malaria Blood Stage Suppression of Liver Stage Immunity by Dendritic Cells. JEM 197: 143-151 [Abstract] [Full Text]  
• Sedlik, C., Orbach, D., Veron, P., Schweighoffer, E., Colucci, F., Gamberale, R., Ioan-Facsinay, A., Verbeek, S., Ricciardi-Castagnoli, P., Bonnerot, C., Tybulewicz, V. L. J., Di Santo, J., Amigorena, S. (2003). A Critical Role for Syk Protein Tyrosine Kinase in Fc Receptor-Mediated Antigen Presentation and Induction of Dendritic Cell Maturation. J. Immunol. 170: 846-852 [Abstract] [Full Text]  
• Tesselaar, K., Xiao, Y., Arens, R., van Schijndel, G. M. W., Schuurhuis, D. H., Mebius, R. E., Borst, J., van Lier, R. A. W. (2003). Expression of the Murine CD27 Ligand CD70 In Vitro and In Vivo. J. Immunol. 170: 33-40 [Abstract] [Full Text]  

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