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*
Institut National de la Santé et de la Recherche Médical, Unité 520, Institut Curie, Paris, France;
Commissariat à l’Energie Atomique, Laboratoire de Chimie des Protéines, Grenoble, France;
Department of Biotechnology and Biological Sciences, Second University of Milan, Milan, Italy; and
Centre National de la Recherche Scientifique, Unité Mixte de Recherche 144, Institut Curie, Paris, France
Dendritic cells constitutively secrete a population of small
(50–90 nm diameter) Ag-presenting vesicles called exosomes. When
sensitized with tumor antigenic peptides, dendritic cells produce
exosomes, which stimulate anti-tumor immune responses and the
rejection of established tumors in mice. Using a systematic proteomic
approach, we establish the first extensive protein map of a particular
exosome population; 21 new exosomal proteins were thus identified. Most
proteins present in exosomes are related to endocytic compartments. New
exosomal residents include cytosolic proteins most likely involved in
exosome biogenesis and function, mainly cytoskeleton-related (cofilin,
profilin I, and elongation factor 1
) and intracellular membrane
transport and signaling factors (such as several annexins, rab 7 and
11, rap1B, and syntenin). Importantly, we also identified a novel
category of exosomal proteins related to apoptosis: thioredoxin
peroxidase II, Alix, 14-3-3, and galectin-3. These findings led us to
analyze possible structural relationships between exosomes and
microvesicles released by apoptotic cells. We show that although they
both represent secreted populations of membrane vesicles relevant to
immune responses, exosomes and apoptotic vesicles are biochemically and
morphologically distinct. Therefore, in addition to cytokines,
dendritic cells produce a specific population of membrane vesicles,
exosomes, with unique molecular composition and strong
immunostimulating properties.
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I. Potolicchio, G. J. Carven, X. Xu, C. Stipp, R. J. Riese, L. J. Stern, and L. Santambrogio Proteomic Analysis of Microglia-Derived Exosomes: Metabolic Role of the Aminopeptidase CD13 in Neuropeptide Catabolism J. Immunol., August 15, 2005; 175(4): 2237 - 2243. [Abstract] [Full Text] [PDF]
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A. Clayton, A. Turkes, H. Navabi, M. D. Mason, and Z. Tabi Induction of heat shock proteins in B-cell exosomes J. Cell Sci., August 15, 2005; 118(16): 3631 - 3638. [Abstract] [Full Text] [PDF]
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K. M. Hardy, E. A. Hoffman, P. Gonzalez, B. S. McKay, and W. D. Stamer Extracellular Trafficking of Myocilin in Human Trabecular Meshwork Cells J. Biol. Chem., August 12, 2005; 280(32): 28917 - 28926. [Abstract] [Full Text] [PDF]
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T. Sakaguchi, A. Kato, F. Sugahara, Y. Shimazu, M. Inoue, K. Kiyotani, Y. Nagai, and T. Yoshida AIP1/Alix Is a Binding Partner of Sendai Virus C Protein and Facilitates Virus Budding J. Virol., July 15, 2005; 79(14): 8933 - 8941. [Abstract] [Full Text] [PDF]
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 M.-P. Caby, D. Lankar, C. Vincendeau-Scherrer, G. Raposo, and C. Bonnerot Exosomal-like vesicles are present in human blood plasma Int. Immunol., July 1, 2005; 17(7): 879 - 887. [Abstract] [Full Text] [PDF]
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E. Segura, C. Nicco, B. Lombard, P. Veron, G. Raposo, F. Batteux, S. Amigorena, and C. Thery ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming Blood, July 1, 2005; 106(1): 216 - 223. [Abstract] [Full Text] [PDF]
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S.-H. Kim, E. R. Lechman, N. Bianco, R. Menon, A. Keravala, J. Nash, Z. Mi, S. C. Watkins, A. Gambotto, and P. D. Robbins Exosomes Derived from IL-10-Treated Dendritic Cells Can Suppress Inflammation and Collagen-Induced Arthritis J. Immunol., May 15, 2005; 174(10): 6440 - 6448. [Abstract] [Full Text] [PDF]
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J. Roy, G. Martin, J.-F. Giguere, D. Belanger, M. Petrin, and M. J. Tremblay HIV Type 1 Can Act as an APC upon Acquisition from the Host Cell of Peptide-Loaded HLA-DR and CD86 Molecules J. Immunol., April 15, 2005; 174(8): 4779 - 4788. [Abstract] [Full Text] [PDF]
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J. Sun, M. Walsh, A. V. Villarino, L. Cervi, C. A. Hunter, Y. Choi, and E. J. Pearce TLR Ligands Can Activate Dendritic Cells to Provide a MyD88-Dependent Negative Signal for Th2 Cell Development J. Immunol., January 15, 2005; 174(2): 742 - 751. [Abstract] [Full Text] [PDF]
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A. E. Morelli, A. T. Larregina, W. J. Shufesky, M. L. G. Sullivan, D. B. Stolz, G. D. Papworth, A. F. Zahorchak, A. J. Logar, Z. Wang, S. C. Watkins, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells Blood, November 15, 2004; 104(10): 3257 - 3266. [Abstract] [Full Text] [PDF]
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N. Amzallag, B. J. Passer, D. Allanic, E. Segura, C. Thery, B. Goud, R. Amson, and A. Telerman TSAP6 Facilitates the Secretion of Translationally Controlled Tumor Protein/Histamine-releasing Factor via a Nonclassical Pathway J. Biol. Chem., October 29, 2004; 279(44): 46104 - 46112. [Abstract] [Full Text] [PDF]
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T. Pisitkun, R.-F. Shen, and M. A. Knepper Identification and proteomic profiling of exosomes in human urine PNAS, September 7, 2004; 101(36): 13368 - 13373. [Abstract] [Full Text] [PDF]
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M. D. Stuchell, J. E. Garrus, B. Muller, K. M. Stray, S. Ghaffarian, R. McKinnon, H.-G. Krausslich, S. G. Morham, and W. I. Sundquist The Human Endosomal Sorting Complex Required for Transport (ESCRT-I) and Its Role in HIV-1 Budding J. Biol. Chem., August 20, 2004; 279(34): 36059 - 36071. [Abstract] [Full Text] [PDF]
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A. R. Mantegazza, M. M. Barrio, S. Moutel, L. Bover, M. Weck, P. Brossart, J.-L. Teillaud, and J. Mordoh CD63 tetraspanin slows down cell migration and translocates to the endosomal-lysosomal-MIICs route after extracellular stimuli in human immature dendritic cells Blood, August 15, 2004; 104(4): 1183 - 1190. [Abstract] [Full Text] [PDF]
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F. Aline, D. Bout, S. Amigorena, P. Roingeard, and I. Dimier-Poisson Toxoplasma gondii Antigen-Pulsed-Dendritic Cell-Derived Exosomes Induce a Protective Immune Response against T. gondii Infection Infect. Immun., July 1, 2004; 72(7): 4127 - 4137. [Abstract] [Full Text] [PDF]
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 V M Diaz, M Hurtado, T M Thomson, J Reventos, and R Paciucci Specific interaction of tissue-type plasminogen activator (t-PA) with annexin II on the membrane of pancreatic cancer cells activates plasminogen and promotes invasion in vitro Gut, July 1, 2004; 53(7): 993 - 1000. [Abstract] [Full Text] [PDF]
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 M. P. Bard, J. P. Hegmans, A. Hemmes, T. M. Luider, R. Willemsen, L.-A. A. Severijnen, J. P. van Meerbeeck, S. A. Burgers, H. C. Hoogsteden, and B. N. Lambrecht Proteomic Analysis of Exosomes Isolated from Human Malignant Pleural Effusions Am. J. Respir. Cell Mol. Biol., July 1, 2004; 31(1): 114 - 121. [Abstract] [Full Text] [PDF]
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B. Fevrier, D. Vilette, F. Archer, D. Loew, W. Faigle, M. Vidal, H. Laude, and G. Raposo Cells release prions in association with exosomes PNAS, June 29, 2004; 101(26): 9683 - 9688. [Abstract] [Full Text] [PDF]
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M. Sachse, G. J. Strous, and J. Klumperman ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles J. Cell Sci., May 1, 2004; 117(9): 1699 - 1708. [Abstract] [Full Text] [PDF]
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J. P.J.J. Hegmans, M. P.L. Bard, A. Hemmes, T. M. Luider, M. J. Kleijmeer, J.-B. Prins, L. Zitvogel, S. A. Burgers, H. C. Hoogsteden, and B. N. Lambrecht Proteomic Analysis of Exosomes Secreted by Human Mesothelioma Cells Am. J. Pathol., May 1, 2004; 164(5): 1807 - 1815. [Abstract] [Full Text] [PDF]
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J. A. Coppinger, G. Cagney, S. Toomey, T. Kislinger, O. Belton, J. P. McRedmond, D. J. Cahill, A. Emili, D. J. Fitzgerald, and P. B. Maguire Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions Blood, March 15, 2004; 103(6): 2096 - 2104. [Abstract] [Full Text] [PDF]
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A. W. Purcell and J. J. Gorman Immunoproteomics: Mass Spectrometry-based Methods to Study the Targets of the Immune Response Mol. Cell. Proteomics, March 1, 2004; 3(3): 193 - 208. [Abstract] [Full Text] [PDF]
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F. Andre, N. Chaput, N. E. C. Schartz, C. Flament, N. Aubert, J. Bernard, F. Lemonnier, G. Raposo, B. Escudier, D.-H. Hsu, et al. Exosomes as Potent Cell-Free Peptide-Based Vaccine. I. Dendritic Cell-Derived Exosomes Transfer Functional MHC Class I/Peptide Complexes to Dendritic Cells J. Immunol., February 15, 2004; 172(4): 2126 - 2136. [Abstract] [Full Text] [PDF]
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G. Greicius, L. Westerberg, E. J. Davey, E. Buentke, A. Scheynius, J. Thyberg, and E. Severinson Microvilli structures on B lymphocytes: inducible functional domains? Int. Immunol., February 1, 2004; 16(2): 353 - 364. [Abstract] [Full Text] [PDF]
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 H. Matsuo, J. Chevallier, N. Mayran, I. Le Blanc, C. Ferguson, J. Faure, N. S. Blanc, S. Matile, J. Dubochet, R. Sadoul, et al. Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization Science, January 23, 2004; 303(5657): 531 - 534. [Abstract] [Full Text] [PDF]
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Y. Trioulier, S. Torch, B. Blot, N. Cristina, C. Chatellard-Causse, J.-M. Verna, and R. Sadoul Alix, a Protein Regulating Endosomal Trafficking, Is Involved in Neuronal Death J. Biol. Chem., January 16, 2004; 279(3): 2046 - 2052. [Abstract] [Full Text] [PDF]
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Y. Yan, L. Phan, F. Yang, M. Talpaz, Y. Yang, Z. Xiong, B. Ng, N. A. Timchenko, C. J. Wu, J. Ritz, et al. A Novel Mechanism of Alternative Promoter and Splicing Regulates the Epitope Generation of Tumor Antigen CML66-L J. Immunol., January 1, 2004; 172(1): 651 - 660. [Abstract] [Full Text] [PDF]
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S. Taverna, G. Ghersi, A. Ginestra, S. Rigogliuso, S. Pecorella, G. Alaimo, F. Saladino, V. Dolo, P. Dell'Era, A. Pavan, et al. Shedding of Membrane Vesicles Mediates Fibroblast Growth Factor-2 Release from Cells J. Biol. Chem., December 19, 2003; 278(51): 51911 - 51919. [Abstract] [Full Text] [PDF]
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A. de Gassart, C. Geminard, B. Fevrier, G. Raposo, and M. Vidal Lipid raft-associated protein sorting in exosomes Blood, December 15, 2003; 102(13): 4336 - 4344. [Abstract] [Full Text] [PDF]
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E. Nikko, A.-M. Marini, and B. Andre Permease Recycling and Ubiquitination Status Reveal a Particular Role for Bro1 in the Multivesicular Body Pathway J. Biol. Chem., December 12, 2003; 278(50): 50732 - 50743. [Abstract] [Full Text] [PDF]
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K. Katoh, H. Shibata, H. Suzuki, A. Nara, K. Ishidoh, E. Kominami, T. Yoshimori, and M. Maki The ALG-2-interacting Protein Alix Associates with CHMP4b, a Human Homologue of Yeast Snf7 That Is Involved in Multivesicular Body Sorting J. Biol. Chem., October 3, 2003; 278(40): 39104 - 39113. [Abstract] [Full Text] [PDF]
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S. J. Gould, A. M. Booth, and J. E. K. Hildreth The Trojan exosome hypothesis PNAS, September 16, 2003; 100(19): 10592 - 10597. [Abstract] [Full Text] [PDF]
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 N. M. McKechnie, D. Copland, and G. Braun Hr44 Secreted with Exosomes: Loss from Ciliary Epithelium in Response to Inflammation Invest. Ophthalmol. Vis. Sci., June 1, 2003; 44(6): 2650 - 2656. [Abstract] [Full Text] [PDF]
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R. Wubbolts, R. S. Leckie, P. T. M. Veenhuizen, G. Schwarzmann, W. Mobius, J. Hoernschemeyer, J.-W. Slot, H. J. Geuze, and W. Stoorvogel Proteomic and Biochemical Analyses of Human B Cell-derived Exosomes. POTENTIAL IMPLICATIONS FOR THEIR FUNCTION AND MULTIVESICULAR BODY FORMATION J. Biol. Chem., March 21, 2003; 278(13): 10963 - 10972. [Abstract] [Full Text] [PDF]
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I. D. Davis, M. Jefford, P. Parente, and J. Cebon Rational approaches to human cancer immunotherapy J. Leukoc. Biol., January 1, 2003; 73(1): 3 - 29. [Abstract] [Full Text] [PDF]
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A. R. Bateman, K. J. Harrington, T. Kottke, A. Ahmed, A. A. Melcher, M. J. Gough, E. Linardakis, D. Riddle, A. Dietz, C. M. Lohse, et al. Viral Fusogenic Membrane Glycoproteins Kill Solid Tumor Cells by Nonapoptotic Mechanisms That Promote Cross Presentation of Tumor Antigens by Dendritic Cells Cancer Res., November 15, 2002; 62(22): 6566 - 6578. [Abstract] [Full Text] [PDF]
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B. Fritzsching, B. Schwer, J. Kartenbeck, A. Pedal, V. Horejsi, and M. Ott Release and Intercellular Transfer of Cell Surface CD81 Via Microparticles J. Immunol., November 15, 2002; 169(10): 5531 - 5537. [Abstract] [Full Text] [PDF]
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C. Chatellard-Causse, B. Blot, N. Cristina, S. Torch, M. Missotten, and R. Sadoul Alix (ALG-2-interacting Protein X), a Protein Involved in Apoptosis, Binds to Endophilins and Induces Cytoplasmic Vacuolization J. Biol. Chem., August 2, 2002; 277(32): 29108 - 29115. [Abstract] [Full Text] [PDF]
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H. Vincent-Schneider, P. Stumptner-Cuvelette, D. Lankar, S. Pain, G. Raposo, P. Benaroch, and C. Bonnerot Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells Int. Immunol., July 1, 2002; 14(7): 713 - 722. [Abstract] [Full Text] [PDF]
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K. E. Pace, T. Lebestky, T. Hummel, P. Arnoux, K. Kwan, and L. G. Baum Characterization of a Novel Drosophila melanogaster Galectin. EXPRESSION IN DEVELOPING IMMUNE, NEURAL, AND MUSCLE TISSUES J. Biol. Chem., April 5, 2002; 277(15): 13091 - 13098. [Abstract] [Full Text] [PDF]
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