Regulation of immune responses by extracellular vesicles

Robbins, Paul D.; Morelli, Adrian E.

doi:10.1038/nri3622

Cited by 2,260Extracellular vesicles in diseaseCellular transport and secretionNanoparticle-Based Drug Delivery

Regulation of immune responses by extracellular vesicles

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Robbins, Paul D., Morelli, Adrian E.·2014·Nature Reviews Immunology

DOI 10.1038/nri3622PMC PMC4350779

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Abstract

Extracellular vesicles, including exosomes, are small membrane vesicles derived from multivesicular bodies or from the plasma membrane. Most, if not all, cell types release extracellular vesicles, which then enter the bodily fluids. These vesicles contain a subset of proteins, lipids and nucleic acids that are derived from the parent cell. It is thought that extracellular vesicles have important roles in intercellular communication, both locally and systemically, as they transfer their contents, including proteins, lipids and RNAs, between cells. Extracellular vesicles are involved in numerous physiological processes, and vesicles from both non-immune and immune cells have important roles in immune regulation. Moreover, extracellular vesicle-based therapeutics are being developed and clinically tested for the treatment of inflammatory diseases, autoimmune disorders and cancer. Given the tremendous therapeutic potential of extracellular vesicles, this Review focuses on their role in modulating immune responses, as well as their potential therapeutic applications.

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EVs sourced from immune cells, such as dendritic cells, macrophages, and natural killer cells, demonstrate an increased ability to evade immune clearance.
“EVs sourced from immune cells, such as DCs, macrophages, and natural killer (NK) cells, demonstrate an increased ability to evade immune clearance [38].”
From Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions (2024) · cites this paper as [38]
In “Therapeutic applications of immunoregulatory extracellular vesicles > APC-derived extracellular vesicles” (page unavailable), the review says injected dendritic-cell-derived EVs are rapidly cleared by phagocytic leukocytes—the opposite of the claimed ability to evade clearance. It does not establish increased clearance evasion for macrophage- or NK-cell-derived EVs. (LLM, conf=0.82)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
EVs are membranous vesicles secreted by all cell types, including healthy, diseased, stem, and transformed cells.
“These are membranous vesicles that are secreted by all cell types, such as healthy, diseased, stem, and transformed cells [37, 38].”
From Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions (2024) · cites this paper as [38]
The Introduction describes EVs as membrane vesicles released by almost all cell types; the sections on RNA transfer and stem cell-derived EVs discuss normal, cancer, and stem cells. The claim’s unqualified “all cell types” is stronger than the paper’s “almost all” or “most, if not all.” Page numbers are not available in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
EVs represent a class of bilayer lipid membranous vesicles secreted by virtually all cell types, including healthy cells, diseased cells, stem cells, and transformed cells.
“EVs represent a class of bilayer lipid membranous vesicles secreted by virtually all cell types, including not only healthy cells but also diseased cells, stem cells, and transformed cells [37, 38].”
From Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions (2024) · cites this paper as [38]

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Buschow, S. I., Hoen, E. N. M. N., van Niel, G., Pols, M. S., ten Broeke, T., Lauwen, M. M., OSSENDORP, F. A., Melief, C. J. M., Raposo, G., Wubbolts, R., et al. (2009) · Traffic · doi:10.1111/j.1600-0854.2009.00963.x · Cited by 430 · see citing works
Tumor exosomes inhibit differentiation of bone marrow dendritic cells
Yu, S., Liu, C., Su, K., Wang, J., Liu, Y., Zhang, L., Li, C., Cong, Y., Kimberly, R., Grizzle, W. E., et al. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.6867 · Cited by 425 · see citing works
Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid
Admyre, C., Grünewald, J., Thyberg, J., Gripenbäck, S., Tornling, G., Eklúnd, A., Scheynius, A., & Gabrielsson, S. (2003) · European Respiratory Journal · doi:10.1183/09031936.03.00041703 · Cited by 383 · see citing works
Exosomes Derived from IL-10-Treated Dendritic Cells Can Suppress Inflammation and Collagen-Induced Arthritis
Kim, S., Lechman, E. R., Bianco, N. R., Menon, R., Keravala, A., Nash, J. A., Mi, Z., Watkins, S. C., Gambotto, A. A., & Robbins, P. D. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.10.6440 · Cited by 380 · see citing works
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Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands
Munich, S. A., Sobo-Vujanovic, A., Buchser, W., Beer–Stolz, D., & Vujanović, N. L. (2012) · OncoImmunology · doi:10.4161/onci.20897 · Cited by 360 · see citing works
Antigen‐presenting cell exosomes are protected from complement‐mediated lysis by expression of CD55 and CD59
Clayton, A., Harris, C. L., Court, J., Mason, M. D., & Morgan, B. P. (2003) · European Journal of Immunology · doi:10.1002/immu.200310028 · Cited by 347 · see citing works
CD44v6 Dependence of Premetastatic Niche Preparation by Exosomes
Jung, T., Castellana, D., Klingbeil, P., Hernández, I. C., Vitacolonna, M., Orlicky, D. J., Roffler, S. R., Brodt, P., & Zöller, M. (2009) · Neoplasia · doi:10.1593/neo.09822 · Cited by 341 · see citing works
Adhesion and signaling by B cell‐derived exosomes: the role of integrins
Clayton, A., Turkes, A., Dewitt, S., Steadman, R., Mason, M. D., & Hallett, M. B. (2004) · The FASEB Journal · doi:10.1096/fj.03-1094fje · Cited by 339 · see citing works
Dynamics of exosome internalization and trafficking
Tian, T., Zhu, Y., Hu, F., Wang, Y., Huang, N., & Xiao, Z. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.24304 · Cited by 336 · see citing works
Mast Cell-Dependent B and T Lymphocyte Activation Is Mediated by the Secretion of Immunologically Active Exosomes
Skokos, D., Panse, S. L., Villa, I., Rousselle, J.-C., Péronet, R., David, B., Namane, A., & Mécheri, S. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.868 · Cited by 333 · see citing works
Specific Isolation of Placenta‐Derived Exosomes from the Circulation of Pregnant Women and Their Immunoregulatory Consequences1
Sabapatha, A., Gercel‐Taylor, C., & Taylor, D. D. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2006.00435.x · Cited by 333 · see citing works
Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection
Wakim, L. M., & Bevan, M. J. (2011) · Nature · doi:10.1038/nature09863 · Cited by 307 · see citing works
Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages
Barrès, C., Blanc, L., Bette‐Bobillo, P., André, S., Mamoun, R. Z., Gabius, H., & Vidal, M. (2009) · Blood · doi:10.1182/blood-2009-07-231449 · Cited by 295 · see citing works
Targeting Tumor Antigens to Secreted Membrane Vesicles In vivo Induces Efficient Antitumor Immune Responses
Zeelenberg, I. S., Ostrowski, M., Krumeich, S., Bobrie, A., Jancic, C. C., Boissonnas, A., Delcayre, A. X., Pecq, J. L., Combadière, B., Amigorena, S., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-3163 · Cited by 286 · see citing works
Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells
Vincent-Schneider, H. (2002) · International Immunology · doi:10.1093/intimm/dxf048 · Cited by 285 · see citing works
Direct exosome stimulation of peripheral humanT cells detected by ELISPOT
Admyre, C., Johansson, S. M., Paulie, S., & Gabrielsson, S. (2006) · European Journal of Immunology · doi:10.1002/eji.200535615 · Cited by 281 · see citing works
Stimulation of P2 receptors causes release of IL-1β–loaded microvesicles from human dendritic cells
Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandonà, D., Savaglio, E., & Virgilio, F. D. (2006) · Blood · doi:10.1182/blood-2005-06-031377 · Cited by 280 · see citing works
T cell‐induced secretion of MHC class II–peptide complexes on B cell exosomes
Muntasell, A., Berger, A. C., & Roche, P. A. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601842 · Cited by 278 · see citing works
CD8+ Dendritic Cells Use LFA-1 to Capture MHC-Peptide Complexes from Exosomes In Vivo
Segura, É., Guérin, C. L., Hogg, N., Amigorena, S., & Théry, C. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1489 · Cited by 278 · see citing works
A Membrane Form of TNF-α Presented by Exosomes Delays T Cell Activation-Induced Cell Death
Zhang, H., Liu, C., Su, K., Yu, S., Zhang, L., Zhang, S., Wang, J., Cao, X., Grizzle, W. E., & Kimberly, R. P. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.12.7385 · Cited by 271 · see citing works
T84-Intestinal Epithelial Exosomes Bear MHC Class II/Peptide Complexes Potentiating Antigen Presentation by Dendritic Cells
Mallegol, J., van Niel, G., Lebreton, C., Lepelletier, Y., Candalh, C., Dugave, C., Heath, J. K., Raposo, G., Cerf–Bensussan, N., & Heyman, M. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.02.043 · Cited by 271 · see citing works
Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral Latent Membrane Protein 1 and the immunomodulatory protein galectin 9
Keryer, C., Pioche‐Durieu, C., Villemant, C., Souquère, S., Nishi, N., Hirashima, M., Middeldorp, J. M., & Busson, P. (2006) · BMC Cancer · doi:10.1186/1471-2407-6-283 · Cited by 270 · see citing works
Differential Secretion of Fas Ligand- or APO2 Ligand/TNF-Related Apoptosis-Inducing Ligand-Carrying Microvesicles During Activation-Induced Death of Human T Cells
Monleón, I., Martínez‐Lorenzo, M. J., Monteagudo, L. V., Lasierra, P., Taulés, M., Iturralde, M., Piñeiro, A., Larrad, L., Álava, M. A., Naval, J., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.12.6736 · Cited by 265 · see citing works
Exosomes As a Short-Range Mechanism to Spread Alloantigen between Dendritic Cells during T Cell Allorecognition
Montecalvo, A., Shufesky, W. J., Stolz, D. B., Sullivan, M., Wang, Z., Divito, S. J., Papworth, G. D., Watkins, S. C., Robbins, P. D., Larregina, A. T., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.5.3081 · Cited by 265 · see citing works
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Platelet-mediated modulation of adaptive immunity: unique delivery of CD154 signal by platelet-derived membrane vesicles
Sprague, D. L., Elzey, B. D., Crist, S. A., Waldschmidt, T. J., Jensen, R. J., & Ratliff, T. L. (2008) · Blood · doi:10.1182/blood-2007-06-097410 · Cited by 264 · see citing works
RNA Trafficking by Acute Myelogenous Leukemia Exosomes
Huan, J., Hornick, N. I., Shurtleff, M. J., Skinner, A. M., Goloviznina, N. A., Roberts, C. T., & Kurre, P. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-2184 · Cited by 259 · see citing works
Association of citrullinated proteins with synovial exosomes
Skriner, K., Adolph, K., Jungblut, P. R., & Burmester, G. R. (2006) · Arthritis & Rheumatism · doi:10.1002/art.22276 · Cited by 257 · see citing works
Exosomes Derived from M. Bovis BCG Infected Macrophages Activate Antigen-Specific CD4+ and CD8+ T Cells In Vitro and In Vivo
Giri, P. K., & Schorey, J. S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002461 · Cited by 255 · see citing works
Membrane Microvesicles as Actors in the Establishment of a Favorable Prostatic Tumoral Niche: A Role for Activated Fibroblasts and CX3CL1-CX3CR1 Axis
Castellana, D., Zobairi, F., Martínez, M. C., Panaro, M. A., Mitolo, V., Freyssinet, J., & Kunzelmann, C. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-1946 · Cited by 255 · see citing works
Antigen-loaded exosomes alone induce Th1-type memory through a B cell–dependent mechanism
Qazi, K. R., Gehrmann, U., Jordö, E. D., Karlsson, M. C. I., & Gabrielsson, S. (2009) · Blood · doi:10.1182/blood-2008-04-153536 · Cited by 250 · see citing works
Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T‐lymphocyte responses and antitumour immunity
Hao, S., Bai, O., Li, F., Yuan, J., Laferté, S., & Xiang, J. (2006) · Immunology · doi:10.1111/j.1365-2567.2006.02483.x · Cited by 248 · see citing works
T-cell apoptosis and suppression of T-cell receptor/CD3-zeta by Fas ligand-containing membrane vesicles shed from ovarian tumors.
Taylor, D. D., Gerçel-Taylor, Ç., Lyons, K. S., Stanson, J., & Whiteside, T. L. (2003) · PubMed · Cited by 247 · see citing works
Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration
Esser, J., Gehrmann, U., D’Alexandri, F. L., Hidalgo-Estévez, A. M., Wheelock, C. E., Scheynius, A., Gabrielsson, S., & Rådmark, O. (2010) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2010.06.039 · Cited by 235 · see citing works
B cell–derived exosomes can present allergen peptides and activate allergen-specific T cells to proliferate and produce TH2-like cytokines
Admyre, C., Bohle, B., Johansson, S. M., Focke‐Tejkl, M., Valenta, R., Scheynius, A., & Gabrielsson, S. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.06.040 · Cited by 222 · see citing works
Contribution of MyD88 to the Tumor Exosome-Mediated Induction of Myeloid Derived Suppressor Cells
Liu, Y., Xiang, X., Zhuang, X., Zhang, S., Liu, C., Cheng, Z., Michalek, S., Grizzle, W. E., & Zhang, H. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090777 · Cited by 217 · see citing works
Exosomes Derived from Genetically Modified DC Expressing FasL Are Anti-inflammatory and Immunosuppressive
Kim, S. H., Bianco, N. R., Menon, R., Lechman, E. R., Shufesky, W. J., Morelli, A. E., & Robbins, P. D. (2005) · Molecular Therapy · doi:10.1016/j.ymthe.2005.09.015 · Cited by 217 · see citing works
Self-citation
Effective Treatment of Established Murine Collagen-Induced Arthritis by Systemic Administration of Dendritic Cells Genetically Modified to Express IL-4
Kim, S. H., Kim, S., Evans, C. H., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.5.3499 · Cited by 212 · see citing works
Efficient induction of antitumor T cell immunity by exosomes derived from heat‐shocked lymphoma cells
Chen, W., Wang, J., Shao, C.-S., et al. (2006) · European Journal of Immunology · doi:10.1002/eji.200535501 · Cited by 209 · see citing works
Human Embryonic Mesenchymal Stem Cell-Derived Conditioned Medium Rescues Kidney Function in Rats with Established Chronic Kidney Disease
van Koppen, A., Joles, J. A., van Balkom, B. W. M., Lim, S. K., de Kleijn, D. P. V., Giles, R. H., & Verhaar, M. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038746 · Cited by 204 · see citing works
Updated Technology to Produce Highly Immunogenic Dendritic Cell-derived Exosomes of Clinical Grade
Viaud, S., Ploix, S., Lapierre, V., Théry, C., Commère, P., Tramalloni, D., Gorrichon, K., Virault-Rocroy, P., Tursz, T., Lantz, O. J., et al. (2010) · Journal of Immunotherapy · doi:10.1097/cji.0b013e3181fe535b · Cited by 201 · see citing works
More Efficient Induction of HLA-A*0201-Restricted and Carcinoembryonic Antigen (CEA)–Specific CTL Response by Immunization with Exosomes Prepared from Heat-Stressed CEA-Positive Tumor Cells
Dai, S., Wan, T. Y., Wang, B., Zhou, X., Xiu, F., Chen, T., Wu, Y., & Cao, X. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0810 · Cited by 199 · see citing works
Exosome Display technology: Applications to the development of new diagnostics and therapeutics
Delcayre, A. X., Estellés, A., Sperinde, J. J., Roulon, T., PAZ, P. E., Aguilar, B. A., Villanueva, J. C., Khine, S., & Pecq, J. L. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.07.003 · Cited by 190 · see citing works
Exosomes released during reticulocyte maturation bind to fibronectin via integrin α4β1
Rieu, S., Géminard, C., Rabesandratana, H., Sainte‐Marie, J., & Vidal, M. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01036.x · Cited by 184 · see citing works
Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8
Kranich, J., Kräutler, N. J., Heinen, E., Polymenidou, M., Bridel, C., Schildknecht, A., Huber, C., Kosco‐Vilbois, M. H., Zinkernagel, R. M., Miele, G., et al. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20071019 · Cited by 181 · see citing works
Cytoplasmic microvesicular form of Fas ligand in human early placenta: switching the tissue immune privilege hypothesis from cellular to vesicular level
Frängsmyr, L., Baranov, V. I., Nagaeva, O., Stendahl, U., Kjellberg, L., & Mincheva‐Nilsson, L. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah129 · Cited by 179 · see citing works
Role of extracellular membrane vesicles in the pathogenesis of various diseases, including cancer, renal diseases, atherosclerosis, and arthritis
Anderson, H. C., Mulhall, D., & Garimella, R. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.152 · Cited by 177 · see citing works
Exosomes from Bronchoalveolar Fluid of Tolerized Mice Prevent Allergic Reaction
Prado, N., Marazuela, E. G., Segura, É., Fernández‐García, H., Villalba, M., Théry, C., Rodrı́guez, R., & Batanero, E. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.2.1519 · Cited by 176 · see citing works
MHC class I-mediated exogenous antigen presentation by exosomes secreted from immature and mature bone marrow derived dendritic cells
Utsugi-Kobukai, S., Fujimaki, H., Hotta, C., Nakazawa, M., & Minami, M. (2003) · Immunology Letters · doi:10.1016/s0165-2478(03)00128-7 · Cited by 176 · see citing works
Therapeutic effect of exosomes from indoleamine 2,3‐dioxygenase–positive dendritic cells in collagen‐induced arthritis and delayed‐type hypersensitivity disease models
Bianco, N. R., Kim, S. H., Ruffner, M. A., & Robbins, P. D. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24229 · Cited by 171 · see citing works
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Cytomegalovirus-Infected Human Endothelial Cells Can Stimulate Allogeneic CD4+ Memory T Cells by Releasing Antigenic Exosomes
Walker, J. D., Maier, C. L., & Pober, J. S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.3.1548 · Cited by 170 · see citing works
Exosomes as a Tumor Vaccine: Enhancing Potency Through Direct Loading of Antigenic Peptides
Hsu, D., PAZ, P. E., Villaflor, G., Rivas, A., Mehta-Damani, A., Angevin, E., Zitvogel, L., & Pecq, J. L. (2003) · Journal of Immunotherapy · doi:10.1097/00002371-200309000-00007 · Cited by 168 · see citing works
MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models
Cho, J.-A., Lee, Y.-S., Kim, S.-H., Ko, J., & Kim, C.-W. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.10.021 · Cited by 147 · see citing works
Tolerogenic dendritic cells for autoimmune disease and transplantation
Thomson, A. W., & Robbins, P. D. (2008) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2008.099176 · Cited by 142 · see citing works
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Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma
Bu, N., Wu, H., Sun, B.-Z., Zhang, G., Zhan, S., Zhang, R., & Zhou, L. (2011) · Journal of Neuro-Oncology · doi:10.1007/s11060-011-0537-1 · Cited by 137 · see citing works
Accumulation of MFG-E8/lactadherin on exosomes from immature dendritic cells
Véron, P., Segura, É., Sugano, G., Amigorena, S., & Théry, C. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.05.001 · Cited by 134 · see citing works
A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice
Beauvillain, C., Ruiz, S., Guiton, R., et al. (2007) · Microbes and Infection · doi:10.1016/j.micinf.2007.07.002 · Cited by 133 · see citing works
Induction of Tolerance by Exosomes and Short-Term Immunosuppression in a Fully MHC-Mismatched Rat Cardiac Allograft Model
Pêche, H., Renaudin, K., Bériou, G., Mérieau, E., Amigorena, S., & Cuturi, M. C. (2006) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2006.01344.x · Cited by 130 · see citing works
Mesenchymal Stem Cell Exosome Ameliorates Reperfusion Injury Through Proteomic Complementation
Lai, R. C., Yeo, R. W. Y., Tan, K. H., & Lim, S. K. (2013) · Regenerative Medicine · doi:10.2217/rme.13.4 · Cited by 129 · see citing works
Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation
Zuccato, E., Blott, E. J., Holt, O. J., Sigismund, S., Shaw, M. K., Bossi, G., & Griffiths, G. M. (2006) · Journal of Cell Science · doi:10.1242/jcs.03315 · Cited by 123 · see citing works
Tumor-Derived Exosomes Confer Antigen-Specific Immunosuppression in a Murine Delayed-Type Hypersensitivity Model
Yang, C., Kim, S.-H., Bianco, N. R., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022517 · Cited by 120 · see citing works
Tolerance Induction by Exosomes from Immature Dendritic Cells and Rapamycin in a Mouse Cardiac Allograft Model
Li, X., Li, J., Yang, J., Wang, D., Zhao, W., Song, W., Li, W., Wang, J.-F., Han, W., Zhang, Z., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044045 · Cited by 118 · see citing works
Increased induction of antitumor response by exosomes derived from interleukin-2 gene-modified tumor cells
Yang, Y., Xiu, F., Cai, Z., Wang, J., Wang, Q., Fu, Y., & Cao, X. (2007) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-006-0184-7 · Cited by 116 · see citing works
MHC Class II+ Exosomes in Plasma Suppress Inflammation in an Antigen-Specific and Fas Ligand/Fas-Dependent Manner
Kim, S. H., Bianco, N. R., Shufesky, W. J., Morelli, A. E., & Robbins, P. D. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.4.2235 · Cited by 114 · see citing works
Self-citation
Exosomes derived from IL-12-anchored renal cancer cells increase induction of specific antitumor response in vitro: a novel vaccine for renal cell carcinoma.
Zhang, Y., Luo, C.-L., He, B., et al. (2010) · PubMed · Cited by 114 · see citing works
Effective Treatment of Established Mouse Collagen-Induced Arthritis by Systemic Administration of Dendritic Cells Genetically Modified to Express FasL
KIM, S., Kim, S. J., Oligino, T., et al. (2002) · Molecular Therapy · doi:10.1016/s1525-0016(02)90712-4 · Cited by 102 · see citing works
Tolerosome‐induced oral tolerance is MHC dependent
Östman, S., Taube, M. B. P., & Telemo, E. (2005) · Immunology · doi:10.1111/j.1365-2567.2005.02245.x · Cited by 101 · see citing works
Follicular dendritic cells in health and disease
Shikh, M. E. E., & Pitzalis, C. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00292 · Cited by 87 · see citing works
Effective Treatment of Established Mouse Collagen-Induced Arthritis by Systemic Administration of Dendritic Cells Genetically Modified to Express FasL
Kim, S. H., Kim, S., Oligino, T., et al. (2002) · Molecular Therapy · doi:10.1006/mthe.2002.0712 · Cited by 87 · see citing works
Immunosuppressive Exosomes: A New Approach for Treating Arthritis
Yang, C., & Robbins, P. D. (2012) · International Journal of Rheumatology · doi:10.1155/2012/573528 · Cited by 85 · see citing works
Self-citation
TLR2-Mediated Expansion of MDSCs Is Dependent on the Source of Tumor Exosomes
Xiang, X., Liu, Y., Zhuang, X., Zhang, S., Michalek, S., Taylor, D. D., Grizzle, W. E., & Zhang, H. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.100245 · Cited by 84 · see citing works
Intercellular Transfer of MHC and Immunological Molecules: Molecular Mechanisms and Biological Significance
Smyth, L. A., Afzali, B., Tsang, J. Y., et al. (2007) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2007.01816.x · Cited by 76 · see citing works
Stem cell therapy market
Syed, B. A., & Evans, J. B. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd3953 · Cited by 69 · see citing works
Surface anchorage of superantigen SEA promotes induction of specific antitumor immune response by tumor-derived exosomes
Xiu, F., Cai, Z., Yang, Y., et al. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0154-1 · Cited by 69 · see citing works
Exosome-Driven Antigen Transfer for MHC Class II Presentation Facilitated by the Receptor Binding Activity of Influenza Hemagglutinin
Testa, J. S., Apcher, G., Comber, J. D., & Eisenlohr, L. (2010) · Journal of Immunology · doi:10.4049/jimmunol.1001768 · Cited by 59 · see citing works
B7‐1/2, but not PD‐L1/2 molecules, are required on IL‐10‐treated tolerogenic DC and DC‐derived exosomes for in vivo function
Ruffner, M. A., Kim, S. H., Bianco, N. R., Francisco, L. M., Sharpe, A. H., & Robbins, P. D. (2009) · European Journal of Immunology · doi:10.1002/eji.200939407 · Cited by 55 · see citing works
Self-citation
Sleuthing the Source of Regeneration by MSCs
Pittenger, M. F. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.06.013 · Cited by 54 · see citing works
Plasma‐derived MHC class II+ exosomes from tumor‐bearing mice suppress tumor antigen‐specific immune responses
Yang, C., Ruffner, M. A., Kim, S., et al. (2012) · European Journal of Immunology · doi:10.1002/eji.201141978 · Cited by 54 · see citing works
B cell activation regulates exosomal HLA production
Arita, S., Baba, E., Shibata, Y., Niiro, H., Shimoda, S., Isobe, T., Kusaba, H., Nakano, S., & Harada, M. (2008) · European Journal of Immunology · doi:10.1002/eji.200737694 · Cited by 54 · see citing works
B lymphocytes and macrophages release cell membrane deposited C3-fragments on exosomes with T cell response-enhancing capacity☆
Papp, K., Végh, P., Prechl, J., Kerekes, K., Kovács, J., Csikós, G., Bajtay, Z., & Erdei, A. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2007.11.021 · Cited by 53 · see citing works
Dendritic Cells Transduced to Express Interleukin 4 Reduce Diabetes Onset in Both Normoglycemic and Prediabetic Nonobese Diabetic Mice
Ruffner, M. A., & Robbins, P. D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011848 · Cited by 28 · see citing works
Self-citation
No Significant CTL Cross-Priming by Dendritic Cell-Derived Exosomes during Murine Lymphocytic Choriomeningitis Virus Infection
Coppieters, K. T., Barral, A. M., Juedes, A. E., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802578 · Cited by 24 · see citing works
Erratum: A membrane form of TNF-α presented by exosomes delays T cell activation-induced cell death (Journal of Immunology (2006) 176 (7385-7393))
Zhang, H., Liu, C., Su, K., et al. (2006) · The Journal of Immunology · Cited by 12 · see citing works

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The biology <b>,</b> function <b>,</b> and biomedical applications of exosomes
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Authors: Robbins, P. D., & Morelli, A. E.
Affiliations: Scripps Research Institute (US)
Corresponding author: Robbins, Paul D.
ORCID: Robbins, Paul D.
Venue: Nature Reviews Immunology
Publisher: Springer Science and Business Media LLC
Published: 2014-02-25
Volume: 14
Issue: 3
Pages: 195-208
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/nri3622
PMC: PMC4350779
OpenAlex: W2121725913
Cited by: 2,260
References: 150
Citations by year: 2026: 140 · 2025: 159 · 2024: 213 · 2023: 200 · 2022: 237 · 2021: 263 · 2020: 208 · 2019: 203 · 2018: 212 · 2017: 155 · 2016: 145 · 2015: 89 · 2014: 34
FWCI: 13.29
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Aging (P01AG043376, AG043376, R21AG033907, AG 024827, AG033907, P30AG024827)
National Heart, Lung, and Blood Institute (HL077545, HL 075512, R01HL077545, R01HL075512)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR051456, R01AR055373, AR055373, R01AR051456)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
Keywords: extracellular vesicles, exosomes, immune regulation, intercellular communication, vesicle cargo, RNA transfer, inflammatory diseases, autoimmune disease, cancer therapy
MeSH terms: Animals, Bacterial Proteins, Biological Transport, Cell Communication, Cell Membrane, Humans, Immunosuppression Therapy, Neoplasms, RNA, Messenger, T-Lymphocytes, Cytotoxic, MicroRNAs, Mice, Exosomes, Multivesicular Bodies

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