J. Exp. Med.
© The Rockefeller University Press
0022-1007/97/01/317/12 $2.00
Volume 185 January 1997 317-328

Maturation Stages of Mouse Dendritic Cells in Growth Factor-dependent Long-Term Cultures

By 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.

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• 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]  
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• 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]  
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• 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]  
• Ramirez, M. C., Sigal, L. J. (2002). Macrophages and Dendritic Cells Use the Cytosolic Pathway to Rapidly Cross-Present Antigen from Live, Vaccinia-Infected Cells. J. Immunol. 169: 6733-6742 [Abstract] [Full Text]  
• Zwaveling, S., Vierboom, M. P. M., Ferreira Mota, S. C., Hendriks, J. A., Ooms, M. E., Sutmuller, R. P. M., Franken, K. L. M. C., Nijman, H. W., Ossendorp, F., van der Burg, S. H., Offringa, R., Melief, C. J. M. (2002). Antitumor Efficacy of Wild-Type p53-specific CD4+ T-Helper Cells. Cancer Res. 62: 6187-6193 [Abstract] [Full Text]  
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• Nopora, A., Brocker, T. (2002). Bcl-2 Controls Dendritic Cell Longevity In Vivo. J. Immunol. 169: 3006-3014 [Abstract] [Full Text]  
• Yanagawa, Y., Onoe, K. (2002). CCL19 induces rapid dendritic extension of murine dendritic cells. Blood 100: 1948-1956 [Abstract] [Full Text]  
• Vincent-Schneider, H., Stumptner-Cuvelette, P., Lankar, D., Pain, S., Raposo, G., Benaroch, P., Bonnerot, C. (2002). Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int Immunol 14: 713-722 [Abstract] [Full Text]  
• Cebulla, C. M., Miller, D. M., Zhang, Y., Rahill, B. M., Zimmerman, P., Robinson, J. M., Sedmak, D. D. (2002). Human Cytomegalovirus Disrupts Constitutive MHC Class II Expression. J. Immunol. 169: 167-176 [Abstract] [Full Text]  
• Zwaveling, S., Mota, S. C. F., Nouta, J., Johnson, M., Lipford, G. B., Offringa, R., van der Burg, S. H., Melief, C. J. M. (2002). Established Human Papillomavirus Type 16-Expressing Tumors Are Effectively Eradicated Following Vaccination with Long Peptides. J. Immunol. 169: 350-358 [Abstract] [Full Text]  

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