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© The Rockefeller University Press, 0021-9525/1999//599 $5.00
The Journal of Cell Biology, Volume 147, Number 3, , 1999 599-610

Molecular Characterization of Dendritic Cell-Derived Exosomes

Clotilde Théry^a, Armelle Regnault^a, Jérôme Garin^b, Joseph Wolfers^c, Laurence Zitvogel^c, Paola Ricciardi-Castagnoli^d, Graça Raposo^e, and Sebastian Amigorena^a

^a Institut National de la Santé et de la Recherche Médicale, U520, Institut Curie, 75005 Paris, France
^b Commissariat à L'Energie Atomique, Laboratoire de Chimie des Protéines, 38054 Grenoble Cedex, France
^c Centre National de la Recherche Scientifique URA 1301, Laboratoire d'Immunologie Cellulaire, Département de Biologie Clinique, Institut Gustave-Roussy, 94805 Villejuif Cedex, France
^d Second University of Milan, Department of Biotechnology and Biological Sciences, 20126 Milan, Italy
^e Centre National de la Recherche Scientifique UMR 144, Institut Curie, 75005 Paris, France
INSERM, U520, Institut Curie, 12 rue Lhomond, 75005 Paris, France.33-1-42-34-63-8233-1-42-34-63-89

sebastian.amigorena{at}curie.fr

Exosomes are membrane vesicles secreted by hematopoietic cells upon fusion of late multivesicular endosomes with the plasma membrane. Dendritic cell (DC)-derived exosomes induce potent antitumor immune responses in mice, resulting in the regression of established tumors (Zitvogel, L., A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena. 1998. Nat. Med. 4:594–600). To unravel the molecular basis of exosome-induced immune stimulation, we now analyze the regulation of their production during DC maturation and characterize extensively their protein composition by peptide mass mapping. Exosomes contain several cytosolic proteins (including annexin II, heat shock cognate protein hsc73, and heteromeric G protein Gi2), as well as different integral or peripherally associated membrane proteins (major histocompatiblity complex class II, Mac-1 integrin, CD9, milk fat globule-EGF-factor VIII [MFG-E8]). MFG-E8, the major exosomal component, binds integrins expressed by DCs and macrophages, suggesting that it may be involved in exosome targeting to these professional antigen-presenting cells. Another exosome component is hsc73, a cytosolic heat shock protein (hsp) also present in DC endocytic compartments. hsc73 was shown to induce antitumor immune responses in vivo, and therefore could be involved in the exosome's potent antitumor effects. Finally, exosome production is downregulated upon DC maturation, indicating that in vivo, exosomes are produced by immature DCs in peripheral tissues. Thus, DC-derived exosomes accumulate a defined subset of cellular proteins reflecting their endosomal biogenesis and accounting for their biological function.

Key Words: endosomes • antigen presentation • dendritic cells • exosomes • heat shock protein

© 1999 The Rockefeller University Press

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• Monleon, I., Martinez-Lorenzo, M. J., Monteagudo, L., Lasierra, P., Taules, M., Iturralde, M., Pineiro, A., Larrad, L., Alava, M. A., Naval, J., Anel, A. (2001). Differential Secretion of Fas Ligand- or APO2 Ligand/TNF-Related Apoptosis-Inducing Ligand-Carrying Microvesicles During Activation-Induced Death of Human T Cells. J. Immunol. 167: 6736-6744 [Abstract] [Full Text]  
• Fortin, A., Lagace, J., Therien, H.-M. (2001). Trafficking of Surface-linked and Encapsulated Liposomal Antigens in Macrophages: an Immunocytochemical Study. J. Histochem. Cytochem. 49: 1407-1420 [Abstract] [Full Text]  
• Kleijmeer, M., Ramm, G., Schuurhuis, D., Griffith, J., Rescigno, M., Ricciardi-Castagnoli, P., Rudensky, A. Y., Ossendorp, F., Melief, C. J.M., Stoorvogel, W., Geuze, H. J. (2001). Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. JCB 155: 53-64 [Abstract] [Full Text]  
• Thery, C., Boussac, M., Veron, P., Ricciardi-Castagnoli, P., Raposo, G., Garin, J., Amigorena, S. (2001). Proteomic Analysis of Dendritic Cell-Derived Exosomes: A Secreted Subcellular Compartment Distinct from Apoptotic Vesicles. J. Immunol. 166: 7309-7318 [Abstract] [Full Text]  
• Wong, P., Pamer, E. G. (2001). Cutting Edge: Antigen-Independent CD8 T Cell Proliferation. J. Immunol. 166: 5864-5868 [Abstract] [Full Text]  
• Harshyne, L. A., Watkins, S. C., Gambotto, A., Barratt-Boyes, S. M. (2001). Dendritic Cells Acquire Antigens from Live Cells for Cross-Presentation to CTL. J. Immunol. 166: 3717-3723 [Abstract] [Full Text]  
• Engering, A., Pieters, J. (2001). Association of distinct tetraspanins with MHC class II molecules at different subcellular locations in human immature dendritic cells. Int Immunol 13: 127-134 [Abstract] [Full Text]  
• Skokos, D., Le Panse, S., Villa, I., Rousselle, J.-C., Peronet, R., David, B., Namane, A., Mecheri, S. (2001). Mast Cell-Dependent B and T Lymphocyte Activation Is Mediated by the Secretion of Immunologically Active Exosomes. J. Immunol. 166: 868-876 [Abstract] [Full Text]  
• Miwako, I, Yamamoto, A, Kitamura, T, Nagayama, K, Ohashi, M (2001). Cholesterol requirement for cation-independent mannose 6-phosphate receptor exit from multivesicular late endosomes to the Golgi. J. Cell Sci. 114: 1765-1776 [Abstract]  
• Denzer, K., van Eijk, M., Kleijmeer, M. J., Jakobson, E., de Groot, C., J. Geuze, H. (2000). Follicular Dendritic Cells Carry MHC Class II-Expressing Microvesicles at Their Surface. J. Immunol. 165: 1259-1265 [Abstract] [Full Text]  
• Shakhov, A. N., Lyakhov, I. G., Tumanov, A. V., Rubtsov, A. V., Drutskaya, L. N., Marino, M. W., Nedospasov, S. A. (2000). Gene profiling approach in the analysis of lymphotoxin and TNF deficiencies. J. Leukoc. Biol. 68: 151-157 [Abstract] [Full Text]  
• Denzer, K, Kleijmeer, M., Heijnen, H., Stoorvogel, W, Geuze, H. (2000). Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 113: 3365-3374 [Abstract]  
• Ohashi, M, Miwako, I, Yamamoto, A, Nagayama, K (2000). Arrested maturing multivesicular endosomes observed in a Chinese hamster ovary cell mutant, LEX2, isolated by repeated flow-cytometric cell sorting. J. Cell Sci. 113: 2187-2205 [Abstract]  
• Geminard, C., Nault, F., Johnstone, R. M., Vidal, M. (2001). Characteristics of the Interaction between Hsc70 and the Transferrin Receptor in Exosomes Released during Reticulocyte Maturation. J. Biol. Chem. 276: 9910-9916 [Abstract] [Full Text]  
• Le Naour, F., Hohenkirk, L., Grolleau, A., Misek, D. E., Lescure, P., Geiger, J. D., Hanash, S., Beretta, L. (2001). Profiling Changes in Gene Expression during Differentiation and Maturation of Monocyte-derived Dendritic Cells Using Both Oligonucleotide Microarrays and Proteomics. J. Biol. Chem. 276: 17920-17931 [Abstract] [Full Text]  

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