Exosomes: From biogenesis and secretion to biological function

Exosomes: composition, biogenesis and function

Théry, C., Zitvogel, L., & Amigorena, S. (2002) · Nature Reviews Immunology · doi:10.1038/nri855 · Cited by 5,346

B lymphocytes secrete antigen-presenting vesicles.

Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., & Geuze, H. J. (1996) · The Journal of experimental medicine · doi:10.1084/jem.183.3.1161 · Cited by 3,546

Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes

Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G., & Amigorena, S. (1998) · Nature Medicine · doi:10.1038/nm0598-594 · Cited by 2,266

Identification and proteomic profiling of exosomes in human urine

Pisitkun, T., Shen, R.-F., & Knepper, M. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403453101 · Cited by 2,174

Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming

Wolfers, J., Lozier, A., Raposo, G., Regnault, A., Théry, C., Masurier, C., Flament, C., Pouzieux, S., Faure, F., Tursz, T., et al. (2001) · Nature Medicine · doi:10.1038/85438 · Cited by 1,640

Proteomic Analysis of Dendritic Cell-Derived Exosomes: A Secreted Subcellular Compartment Distinct from Apoptotic Vesicles

Théry, C., Boussac, M., Véron, P., Ricciardi-Castagnoli, P., Raposo, G., Garin, J., & Amigorena, S. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.12.7309 · Cited by 1,563

ENDOCYTOSIS AND MOLECULAR SORTING

Mellman, I. (1996) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.12.1.575 · Cited by 1,533

Activated Platelets Release Two Types of Membrane Vesicles: Microvesicles by Surface Shedding and Exosomes Derived From Exocytosis of Multivesicular Bodies and -Granules

Heijnen, H. F. G., Schiel, A. E., Fijnheer, R., Geuze, H. J., & Sixma, J. J. (1999) · Blood · doi:10.1182/blood.v94.11.3791 · Cited by 1,487

Alzheimer’s disease β-amyloid peptides are released in association with exosomes

Rajendran, L., Honsho, M., Zahn, T. R., Keller, P., Geiger, K. D., Verkade, P., & Simons, K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603838103 · Cited by 1,343

Selective Enrichment of Tetraspan Proteins on the Internal Vesicles of Multivesicular Endosomes and on Exosomes Secreted by Human B-lymphocytes

Escola, J.-M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., & Geuze, H. J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.32.20121 · Cited by 1,228

Cells release prions in association with exosomes

Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., & Raposo, G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308413101 · Cited by 997

Exosomes are released by cultured cortical neurones

Fauré, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., Boyer, V., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.12.003 · Cited by 896

Proteomic and Biochemical Analyses of Human B Cell-derived Exosomes

Wubbolts, R., Leckie, R. S., Veenhuizen, P. T. M., Schwarzmann, G., Möbius, W., Hoernschemeyer, J., Slot, J.-W., Geuze, H. J., & Stoorvogel, W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m207550200 · Cited by 884

The Protein Network of HIV Budding

von Schwedler, U. K., Stuchell, M., Müller, B., Ward, D. M., Chung, H.-Y., Morita, E., Wang, H. E., Davis, T., He, G.-P., Cimbora, D. M., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00714-1 · Cited by 815

Induction of Lymphocyte Apoptosis by Tumor Cell Secretion of FasL-bearing Microvesicles

Andreola, G., Rivoltini, L., Castelli, C., Huber, V., Perego, P., Deho, P., Squarcina, P., Accornero, P., Lozupone, F., Lugini, L., et al. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011624 · Cited by 774

Intestinal epithelial cells secrete exosome–like vesicles

Van Niel, G., Raposo, G., Candalh, C., Boussac, M., Hershberg, R., Cerf–Bensussan, N., & Heyman, M. (2001) · Gastroenterology · doi:10.1053/gast.2001.26263 · Cited by 698

The Regulation of Exosome Secretion: a Novel Function of the p53 Protein

Yu, X., Harris, S. L., & Levine, A. J. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4579 · Cited by 688

Lipid raft-associated protein sorting in exosomes

de Gassart, A., Géminard, C., Février, B., Raposo, G., & Vidal, M. (2003) · Blood · doi:10.1182/blood-2003-03-0871 · Cited by 672

TCR Activation of Human T Cells Induces the Production of Exosomes Bearing the TCR/CD3/ζ Complex

Blanchard, N., Lankar, D., Faure, F., Regnault, A., Dumont, C., Raposo, G., & Hivroz, C. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.7.3235 · Cited by 660

Fab1p PtdIns(3)P 5-Kinase Function Essential for Protein Sorting in the Multivesicular Body

Odorizzi, G., Babst, M., & Emr, S. D. (1998) · Cell · doi:10.1016/s0092-8674(00)81707-9 · Cited by 656

Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells

Safaei, R., Larson, B. J., Cheng, T. C., Gibson, M. A., Otani, S., Naerdemann, W., & Howell, S. B. (2005) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-05-0102 · Cited by 564

Morphogens, Compartments, and Pattern: Lessons from Drosophila?

Lawrence, P. A., & Struhl, G. (1996) · Cell · doi:10.1016/s0092-8674(00)81297-0 · Cited by 555

Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes.

Futter, C. E., Pearse, A., Hewlett, L. J., & Hopkins, C. R. (1996) · The Journal of cell biology · doi:10.1083/jcb.132.6.1011 · Cited by 530

Murine Mammary Carcinoma Exosomes Promote Tumor Growth by Suppression of NK Cell Function

Liu, C., Yu, S., Zinn, K., Wang, J., Zhang, L., Jia, Y., Kappes, J. C., Barnes, S., Kimberly, R. P., Grizzle, W. E., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.3.1375 · Cited by 500

Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis

Abusamra, A. J., Zhong, Z., Zheng, X., Li, M., Ichim, T. E., Chin, J. L., & Min, W.-P. (2005) · Blood Cells, Molecules, and Diseases · doi:10.1016/j.bcmd.2005.07.001 · Cited by 456

Induction of heat shock proteins in B-cell exosomes

Clayton, A., Turkes, A., Navabi, H., Mason, M. D., & Tabi, Z. (2005) · Journal of Cell Science · doi:10.1242/jcs.02494 · Cited by 454

Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body

Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J., & Hopkins, C. R. (1990) · Cell · doi:10.1016/0092-8674(90)90474-s · Cited by 445

Argosomes

Greco, V., Hannus, M., & Eaton, S. (2001) · Cell · doi:10.1016/s0092-8674(01)00484-6 · Cited by 428

Proteomic Analysis of Exosomes Isolated from Human Malignant Pleural Effusions

Bard, M. P., Hegmans, J. P., Hemmes, A., Luider, T. M., Willemsen, R., Severijnen, L.-A. A., van Meerbeeck, J. P., Burgers, S. A., Hoogsteden, H. C., & Lambrecht, B. N. (2004) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2003-0238oc · Cited by 416

Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles.

Shedden, K., Xie, X. T., Chandaroy, P., Chang, Y., & Rosania, G. R. (2003) · PubMed · Cited by 385

GOLGI APPARATUS AND LYSOSOMES.

Novikoff, A. B., Essner, E. S., & Quintana, N. (1996) · PubMed · Cited by 370

Exosomes biological significance: A concise review

Johnstone, R. M. (2006) · Blood Cells, Molecules, and Diseases · doi:10.1016/j.bcmd.2005.12.001 · Cited by 339

Proteomic analysis of melanoma‐derived exosomes by two‐dimensional polyacrylamide gel electrophoresis and mass spectrometry

Mears, R., Craven, R. A., Hanrahan, S., Totty, N., Upton, C., Young, S. L., Patel, P., Selby, P. J., & Banks, R. E. (2004) · PROTEOMICS · doi:10.1002/pmic.200400876 · Cited by 335

Mast Cell-Dependent B and T Lymphocyte Activation Is Mediated by the Secretion of Immunologically Active Exosomes

Skokos, D., Le Panse, S., Villa, I., Rousselle, J.-C., Peronet, R., David, B., Namane, A., & Mécheri, S. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.868 · Cited by 333

Late endosomes derive from early endosomes by maturation

Stoorvogel, W., Strous, G. J., Geuze, H. J., Oorschot, V., & Schwartzt, A. L. (1991) · Cell · doi:10.1016/0092-8674(91)90459-c · Cited by 331

Regulation of signal transduction by endocytosis

Ceresa, B. P., & Schmid, S. L. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)00077-0 · Cited by 294

Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions.

Johnstone, R., Bianchini, A., & Teng, K. (1989) · Blood · doi:10.1182/blood.v74.5.1844.1844 · Cited by 289

Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells

Kleijmeer, M., Ramm, G., Schuurhuis, D., Griffith, J., Rescigno, M., Ricciardi-Castagnoli, P., Rudensky, A. Y., Ossendorp, F., Melief, C. J. M., Stoorvogel, W., et al. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200103071 · Cited by 288

Heparin-binding EGF-like growth factor, which acts as the diphtheria toxin receptor, forms a complex with membrane protein DRAP27/CD9, which up-regulates functional receptors and diphtheria toxin sensitivity.

Iwamoto, R., Higashiyama, S., Mitamura, T., Taniguchi, N., Klagsbrun, M., & Mekada, E. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06516.x · Cited by 265

A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44

Stoeck, A., Keller, S., Riedle, S., Sanderson, M. P., Runz, S., Le Naour, F., Gutwein, P., Ludwig, A., Rubinstein, E., & Altevogt, P. (2006) · Biochemical Journal · doi:10.1042/bj20051013 · Cited by 246

Purification, characterization and biological significance of tumor-derived exosomes.

Koga, K., Matsumoto, K., Akiyoshi, T., Kubo, M., Yamanaka, N., Tasaki, A., Nakashima, H., Nakamura, M., Kuroki, S., Tanaka, M., et al. (2005) · PubMed · Cited by 240

ADAM10‐mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles

Gutwein, P., Mechtersheimer, S., Riedle, S., Stoeck, A., Gast, D., Joumaa, S., Zentgraf, H., Fogel, M., & Altevogt, P. (2003) · The FASEB Journal · doi:10.1096/fj.02-0430fje · Cited by 225

Fusion of Lysosomes with Late Endosomes Produces a Hybrid Organelle of Intermediate Density and Is NSF Dependent

Mullock, B. M., Bright, N. A., Fearon, C. W., Gray, S. R., & Luzio, J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.3.591 · Cited by 218

Release of full-length 55-kDa TNF receptor 1 in exosome-like vesicles: A mechanism for generation of soluble cytokine receptors

Hawari, F. I., Rouhani, F. N., Cui, X., Yu, Z.-X., Buckley, C., Kaler, M., & Levine, S. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307981100 · Cited by 214

Cleavage of L1 in Exosomes and Apoptotic Membrane Vesicles Released from Ovarian Carcinoma Cells

Gutwein, P., Stoeck, A., Riedle, S., Gast, D., Runz, S., Condon, T. P., Marmé, A., Phong, M.-C., Linderkamp, O., Skorokhod, A., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-1688 · Cited by 198

Structure and Ubiquitin Binding of the Ubiquitin-interacting Motif

Fisher, R. D., Wang, B., Alam, S. L., Higginson, D. S., Robinson, H., Sundquist, W. I., & Hill, C. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302596200 · Cited by 188

Prospects for exosomes in immunotherapy of cancer

Mignot, G., Roux, S., Thery, C., Ségura, E., & Zitvogel, L. (2006) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2006.tb00406.x · Cited by 185

Problems and paradigms: Morphogens and pattern formation

Neumann, C., & Cohen, S. (1997) · BioEssays · doi:10.1002/bies.950190813 · Cited by 184

Role of exosomes in immune regulation

Li, X.-B., Zhang, Z.-R., Schluesener, H. J., & Xu, S.-Q. (2006) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2006.tb00405.x · Cited by 160

Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors

Sanderson, M. P., Dempsey, P. J., & Dunbar, A. J. (2006) · Growth Factors · doi:10.1080/08977190600634373 · Cited by 156

Endocytosis and mitogenic signaling

Fiore, P. P. D., & Gillt, G. N. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80069-6 · Cited by 128

Antigen Loading of MHC Class I Molecules in the Endocytic Tract

Kleijmeer, M. J., Escola, J.-M., UytdeHaag, F. G. C. M., Jakobson, E., Griffith, J. M., Osterhaus, A. D. M. E., Stoorvogel, W., Melief, C. J. M., Rabouille, C., & Geuze, H. J. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.020207.x · Cited by 108

Prions and exosomes: From PrPc trafficking to PrPsc propagation

Porto-Carreiro, I., Février, B., Paquet, S., Vilette, D., & Raposo, G. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.06.013 · Cited by 101

Regulating morphogen gradients in the Drosophila wing

Cadigan, K. M. (2002) · Seminars in Cell and Developmental Biology · doi:10.1016/s1084-9521(02)00014-9 · Cited by 98

Complement inhibitor membrane cofactor protein (MCP; CD46) is constitutively shed from cancer cell membranes in vesicles and converted by a metalloproteinase to a functionally active soluble form

Hakulinen, J., Junnikkala, S., Sorsa, T. A., & Meri, S. (2004) · European Journal of Immunology · doi:10.1002/eji.200424969 · Cited by 95

Transmodulation of Cell Surface Regulatory Molecules via Ectodomain Shedding

Sbarba, P. D., & Rovida, E. (2002) · Biological Chemistry · doi:10.1515/bc.2002.007 · Cited by 91

Heparin-binding Epidermal Growth Factor-like Growth Factor (HB-EGF) is a Mediator of Multiple Physiological and Pathological Pathways

Nishi, E., & Klagsbrun, M. (2004) · Growth Factors · doi:10.1080/08977190400008448 · Cited by 74

BMP, Wnt and Hedgehog signals: how far can they go?

Christian, J. L. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)00082-4 · Cited by 74

BAG-1 Is a Novel Cytoplasmic Binding Partner of the Membrane Form of Heparin-binding EGF-like Growth Factor

Lin, J., Hutchinson, L., Gaston, S. M., Raab, G., & Freeman, M. R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010237200 · Cited by 68

Signal transduction in yeast mating: Receptors, transcription factors, and the kinase connection

SPRAGUEJR, G. (1991) · Trends in Genetics · doi:10.1016/0168-9525(91)90262-o · Cited by 65

Nonspecific B and T Cell-Stimulatory Activity Mediated by Mast CellsIs Associated with Exosomes

Skokos, D., Panse, S. L., Villa, I., Rousselle, J.-C., Péronet, R., Namane, A., David, B., & Mécheri, S. (2001) · International Archives of Allergy and Immunology · doi:10.1159/000053691 · Cited by 64

Membranes and sorting

Mellman, I. (1996) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(96)80026-3 · Cited by 63

Direct stimulation of T cells by membrane vesicles from antigen-presenting cells

Kovář, M., Boyman, O., Shen, X., Hwang, I., Kohler, R. E., & Sprent, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603466103 · Cited by 61

Immunoregulatory properties of mast cell-derived exosomes

Dimitris, S., Goubran‐Botros, H., Roa, M., & Mécheri, S. (2002) · Molecular Immunology · doi:10.1016/s0161-5890(02)00088-3 · Cited by 56

The potential of exosomes in immunotherapy

Chaput, N., Taïeb, J., André, F., & Zitvogel, L. (2005) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.5.6.737 · Cited by 52

The control of gene expression by regulated nuclear transport

Schwoebel, E. D., & Moore, M. S. (2000) · Essays in Biochemistry · doi:10.1042/bse0360105 · Cited by 30

Dendritic cell-based immunotherapy of cancer

Zitvogel, L., Angevin, E., & Tursz, T. (2000) · Annals of Oncology · doi:10.1093/annonc/11.suppl_3.199 · Cited by 30

Biological properties of extracellular vesicles and their physiological functions

Yáñez‐Mó, M., Siljander, P. R. ‐., Andreu, Z., Bedina Zavec, A., Borràs, F. E., Buzas, E. I., Buzas, K., Casal, E., Cappello, F., Carvalho, J., et al. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.27066 · Cited by 5,926

Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury

Lai, R. C., Arslan, F., Lee, M. M., Sze, N. S. K., Choo, A., Chen, T. S., Salto-Tellez, M., Timmers, L., Lee, C. N., El Oakley, R. M., et al. (2010) · Stem Cell Research · doi:10.1016/j.scr.2009.12.003 · Cited by 2,215

Vesiclepedia: A Compendium for Extracellular Vesicles with Continuous Community Annotation

Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V. C., Borràs, F. E., Breakefield, X., Budnik, V., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001450 · Cited by 1,367

Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance

Mashouri, L., Yousefi, H., Aref, A. R., Ahadi, A. M., Molaei, F., & Alahari, S. K. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0991-5 · Cited by 1,363

Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival

Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., & Vekrellis, K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5699-09.2010 · Cited by 1,115