Original Article

Molecular Characterization of Dendritic Cell-derived Exosomes: Selective Accumulation of the Heat Shock Protein hsc73

Correspondence to: Sebastian Amigorena, INSERM, U520, Institut Curie, 12 rue Lhomond, 75005 Paris, France. Tel:33-1-42-34-63-89 Fax:33-1-42-34-63-82 E-mail: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

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• 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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