Tetraspanins in Extracellular Vesicle Formation and Function

Zoraida Andreu1, María Yáñez-MÃ
1Unidad de Investigación, Hospital Santa Cristina, Instituto de Investigación Sanitaria Princesa, Madrid, Spain

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Raposo, 2013, Extracellular vesicles: exosomes, microvesicles, and friends, J Cell Biol, 200, 373, 10.1083/jcb.201211138

Cocucci, 2009, Shedding microvesicles: artefacts no more, Trends Cell Biol, 19, 43, 10.1016/j.tcb.2008.11.003

Simons, 2009, Exosomes – vesicular carriers for intercellular communication, Curr Opin Cell Biol, 21, 575, 10.1016/j.ceb.2009.03.007

Lakkaraju, 2008, Itinerant exosomes: emerging roles in cell and tissue polarity, Trends Cell Biol, 18, 199, 10.1016/j.tcb.2008.03.002

Tickner, 2014, Functions and therapeutic roles of exosomes in cancer, Front Oncol, 4, 127, 10.3389/fonc.2014.00127

Chivet, 2012, Emerging role of neuronal exosomes in the central nervous system, Front Physiol, 3, 145, 10.3389/fphys.2012.00145

Lamichhane, 2014, Emerging roles for extracellular vesicles in tissue engineering and regenerative medicine, Tissue Eng Part B Rev, 10.1089/ten.teb.2014.0300

Bobrie, 2011, Exosome secretion: molecular mechanisms and roles in immune responses, Traffic, 12, 1659, 10.1111/j.1600-0854.2011.01225.x

Charrin, 2009, Lateral organization of membrane proteins: tetraspanins spin their web, Biochem J, 420, 133, 10.1042/BJ20082422

Hemler, 2005, Tetraspanin functions and associated microdomains, Nat Rev Mol Cell Biol, 6, 801, 10.1038/nrm1736

Yanez-Mo, 2009, Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes, Trends Cell Biol, 19, 434, 10.1016/j.tcb.2009.06.004

Berditchevski, 2007, Tetraspanins as regulators of protein trafficking, Traffic, 8, 89, 10.1111/j.1600-0854.2006.00515.x

Stipp, 2003, Functional domains in tetraspanin proteins, Trends Biochem Sci, 28, 106, 10.1016/S0968-0004(02)00014-2

Hemler, 2008, Targeting of tetraspanin proteins – potential benefits and strategies, Nat Rev Drug Discov, 7, 747, 10.1038/nrd2659

Hemler, 2001, Specific tetraspanin functions, J Cell Biol, 155, 1103, 10.1083/jcb.200108061

Masciopinto, 2001, The small extracellular loop of CD81 is necessary for optimal surface expression of the large loop, a putative HCV receptor, Virus Res, 80, 1, 10.1016/S0168-1702(01)00245-3

Kitadokoro, 2001, CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs, EMBO J, 20, 12, 10.1093/emboj/20.1.12

Seigneuret, 2001, Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion, J Biol Chem, 276, 40055, 10.1074/jbc.M105557200

Hemler, 2003, Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain, Annu Rev Cell Dev Biol, 19, 397, 10.1146/annurev.cellbio.19.111301.153609

Boucheix, 2001, Tetraspanins, Cell Mol Life Sci, 58, 1189, 10.1007/PL00000933

Dornier, 2012, TspanC8 tetraspanins regulate ADAM10/Kuzbanian trafficking and promote Notch activation in flies and mammals, J Cell Biol, 199, 481, 10.1083/jcb.201201133

Haining, 2012, The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression, J Biol Chem, 287, 39753, 10.1074/jbc.M112.416503

Kohl, 1998, The role of the peripherin/RDS gene in retinal dystrophies, Acta Anat, 162, 75, 10.1159/000046471

Bienstock, 2001, KAI1, a prostate metastasis suppressor: prediction of solvated structure and interactions with binding partners; integrins, cadherins, and cell-surface receptor proteins, Mol Carcinog, 32, 139, 10.1002/mc.1073

Gratkowski, 2001, Polar side chains drive the association of model transmembrane peptides, Proc Natl Acad Sci U S A, 98, 880, 10.1073/pnas.98.3.880

Kovalenko, 2005, Structural organization and interactions of transmembrane domains in tetraspanin proteins, BMC Struct Biol, 5, 11, 10.1186/1472-6807-5-11

Rous, 2002, Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes, Mol Biol Cell, 13, 1071, 10.1091/mbc.01-08-0409

Bonifacino, 2003, Signals for sorting of transmembrane proteins to endosomes and lysosomes, Annu Rev Biochem, 72, 395, 10.1146/annurev.biochem.72.121801.161800

Escola, 1998, Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes, J Biol Chem, 273, 20121, 10.1074/jbc.273.32.20121

Latysheva, 2006, Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63, Mol Cell Biol, 26, 7707, 10.1128/MCB.00849-06

Baietti, 2012, Syndecan-syntenin-ALIX regulates the biogenesis of exosomes, Nat Cell Biol, 14, 677, 10.1038/ncb2502

Neisch, 2011, Ezrin, radixin and moesin: key regulators of membrane-cortex interactions and signaling, Curr Opin Cell Biol, 23, 377, 10.1016/j.ceb.2011.04.011

Sala-Valdes, 2006, EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins, J Biol Chem, 281, 19665, 10.1074/jbc.M602116200

Barreiro, 2005, Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation, Blood, 105, 2852, 10.1182/blood-2004-09-3606

Tejera, 2013, CD81 regulates cell migration through its association with Rac GTPase, Mol Biol Cell, 24, 261, 10.1091/mbc.E12-09-0642

Gordon-Alonso, 2012, EWI-2 association with alpha-actinin regulates T cell immune synapses and HIV viral infection, J Immunol, 189, 689, 10.4049/jimmunol.1103708

Lagaudriere-Gesbert, 1998, Signaling through the tetraspanin CD82 triggers its association with the cytoskeleton leading to sustained morphological changes and T cell activation, Eur J Immunol, 28, 4332, 10.1002/(SICI)1521-4141(199812)28:124332::AID-IMMU43323.0.CO;2-8

Zhang, 2001, Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta(1) integrins, J Biol Chem, 276, 25005, 10.1074/jbc.M102156200

Zhang, 2002, Function of the tetraspanin CD151-alpha6beta1 integrin complex during cellular morphogenesis, Mol Biol Cell, 13, 1, 10.1091/mbc.01-10-0481

Little, 2004, Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association, Mol Biol Cell, 15, 2375, 10.1091/mbc.E03-12-0886

Andre, 2002, Tumor-derived exosomes: a new source of tumor rejection antigens, Vaccine, 20, A28, 10.1016/S0264-410X(02)00384-5

Quast, 2011, CD81 is essential for the formation of membrane protrusions and regulates Rac1-activation in adhesion-dependent immune cell migration, Blood, 118, 1818, 10.1182/blood-2010-12-326595

Resh, 1999, Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins, Biochim Biophys Acta, 1451, 1, 10.1016/S0167-4889(99)00075-0

Yang, 2002, Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology, Mol Biol Cell, 13, 767, 10.1091/mbc.01-05-0275

Berditchevski, 2002, Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling, J Biol Chem, 277, 36991, 10.1074/jbc.M205265200

Charrin, 2002, Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation, FEBS Lett, 516, 139, 10.1016/S0014-5793(02)02522-X

Charrin, 2003, A physical and functional link between cholesterol and tetraspanins, Eur J Immunol, 33, 2479, 10.1002/eji.200323884

Regina Todeschini, 2008, Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains, Biochim Biophys Acta, 1780, 421, 10.1016/j.bbagen.2007.10.008

Yanez-Mo, 2011, Functional interplay between tetraspanins and proteases, Cell Mol Life Sci, 68, 3323, 10.1007/s00018-011-0746-y

Gould, 2013, As we wait: coping with an imperfect nomenclature for extracellular vesicles, J Extracell Vesicles, 2, 20389, 10.3402/jev.v2i0.20389

Heijnen, 1999, Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules, Blood, 94, 3791, 10.1182/blood.V94.11.3791

Deregibus, 2007, Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA, Blood, 110, 2440, 10.1182/blood-2007-03-078709

Booth, 2006, Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane, J Cell Biol, 172, 923, 10.1083/jcb.200508014

Simpson, 2012, ExoCarta as a resource for exosomal research, J Extracell Vesicles, 1, 18374, 10.3402/jev.v1i0.18374

Kim, 2013, EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles, J Extracell Vesicles, 2, 20384, 10.3402/jev.v2i0.20384

Thery, 1999, Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73, J Cell Biol, 147, 599, 10.1083/jcb.147.3.599

Pols, 2009, Trafficking and function of the tetraspanin CD63, Exp Cell Res, 315, 1584, 10.1016/j.yexcr.2008.09.020

Lenassi, 2010, HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells, Traffic, 11, 110, 10.1111/j.1600-0854.2009.01006.x

Fang, 2007, Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes, PLoS Biol, 5, e158, 10.1371/journal.pbio.0050158

Bobrie, 2012, Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation, J Extracell Vesicles, 1, 18397, 10.3402/jev.v1i0.18397

Crescitelli, 2013, Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes, J Extracell Vesicles, 2, 20677, 10.3402/jev.v2i0.20677

Ostrowski, 2010, Rab27a and Rab27b control different steps of the exosome secretion pathway, Nat Cell Biol, 12, 19, 10.1038/ncb2000

Saunderson, 2008, Induction of exosome release in primary B cells stimulated via CD40 and the IL-4 receptor, J Immunol, 180, 8146, 10.4049/jimmunol.180.12.8146

Henne, 2011, The ESCRT pathway, Dev Cell, 21, 77, 10.1016/j.devcel.2011.05.015

Colombo, 2013, Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles, J Cell Sci, 126, 5553, 10.1242/jcs.128868

Buschow, 2005, Exosomes contain ubiquitinated proteins, Blood Cells Mol Dis, 35, 398, 10.1016/j.bcmd.2005.08.005

Thery, 2001, Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles, J Immunol, 166, 7309, 10.4049/jimmunol.166.12.7309

Tamai, 2010, Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein, Biochem Biophys Res Commun, 399, 384, 10.1016/j.bbrc.2010.07.083

Geminard, 2004, Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TFR for sorting into exosomes, Traffic, 5, 181, 10.1111/j.1600-0854.2004.0167.x

Yu, 2006, The regulation of exosome secretion: a novel function of the p53 protein, Cancer Res, 66, 4795, 10.1158/0008-5472.CAN-05-4579

Manohar, 2011, Chromatin modifying protein 1A (Chmp1A) of the endosomal sorting complex required for transport (ESCRT)-III family activates ataxia telangiectasia mutated (ATM) for PanC-1 cell growth inhibition, Cell Cycle, 10, 2529, 10.4161/cc.10.15.15926

Stuffers, 2009, Multivesicular endosome biogenesis in the absence of ESCRTs, Traffic, 10, 925, 10.1111/j.1600-0854.2009.00920.x

Buschow, 2009, MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways, Traffic, 10, 1528, 10.1111/j.1600-0854.2009.00963.x

Trajkovic, 2008, Ceramide triggers budding of exosome vesicles into multivesicular endosomes, Science, 319, 1244, 10.1126/science.1153124

van Niel, 2011, The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis, Dev Cell, 21, 708, 10.1016/j.devcel.2011.08.019

Chairoungdua, 2010, Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling, J Cell Biol, 190, 1079, 10.1083/jcb.201002049

Petersen, 2011, The role of tetraspanin CD63 in antigen presentation via MHC class II, Eur J Immunol, 41, 2556, 10.1002/eji.201141438

Piccin, 2007, Circulating microparticles: pathophysiology and clinical implications, Blood Rev, 21, 157, 10.1016/j.blre.2006.09.001

Nydegger, 2006, Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1, J Cell Biol, 173, 795, 10.1083/jcb.200508165

Bari, 2011, Tetraspanins regulate the protrusive activities of cell membrane, Biochem Biophys Res Commun, 415, 619, 10.1016/j.bbrc.2011.10.121

Wrigley, 2000, Peripherin/rds influences membrane vesicle morphology. Implications for retinopathies, J Biol Chem, 275, 13191, 10.1074/jbc.C900853199

Shoham, 2006, Building of the tetraspanin web: distinct structural domains of CD81 function in different cellular compartments, Mol Cell Biol, 26, 1373, 10.1128/MCB.26.4.1373-1385.2006

Shoham, 2003, The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment, J Immunol, 171, 4062, 10.4049/jimmunol.171.8.4062

Zhang, 2003, EWI2/PGRL associates with the metastasis suppressor KAI1/CD82 and inhibits the migration of prostate cancer cells, Cancer Res, 63, 2665

Odintsova, 2000, Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/KAI-1, Curr Biol, 10, 1009, 10.1016/S0960-9822(00)00652-7

Odintsova, 2013, Metastasis suppressor tetraspanin CD82/KAI1 regulates ubiquitylation of epidermal growth factor receptor, J Biol Chem, 288, 26323, 10.1074/jbc.M112.439380

Liu, 2007, Tetraspanin CD151 promotes cell migration by regulating integrin trafficking, J Biol Chem, 282, 31631, 10.1074/jbc.M701165200

Yauch, 1998, Highly stoichiometric, stable, and specific association of integrin alpha3beta1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration, Mol Biol Cell, 9, 2751, 10.1091/mbc.9.10.2751

Rana, 2011, Activation-induced internalization differs for the tetraspanins CD9 and Tspan8: impact on tumor cell motility, Int J Biochem Cell Biol, 43, 106, 10.1016/j.biocel.2010.10.002

Luga, 2012, Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration, Cell, 151, 1542, 10.1016/j.cell.2012.11.024

Abache, 2007, The transferrin receptor and the tetraspanin web molecules CD9, CD81, and CD9P-1 are differentially sorted into exosomes after TPA treatment of K562 cells, J Cell Biochem, 102, 650, 10.1002/jcb.21318

Mazurov, 2013, Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes, FEBS J, 280, 1200, 10.1111/febs.12110

Arduise, 2008, Tetraspanins regulate ADAM10-mediated cleavage of TNF-alpha and epidermal growth factor, J Immunol, 181, 7002, 10.4049/jimmunol.181.10.7002

Gutierrez-Lopez, 2011, The sheddase activity of ADAM17/TACE is regulated by the tetraspanin CD9, Cell Mol Life Sci, 68, 3275, 10.1007/s00018-011-0639-0

Stoeck, 2006, A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44, Biochem J, 393, 609, 10.1042/BJ20051013

Keller, 2009, Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes, Cancer Lett, 278, 73, 10.1016/j.canlet.2008.12.028

Soderberg, 2007, Redox-signaling transmitted in trans to neighboring cells by melanoma-derived TNF-containing exosomes, Free Radic Biol Med, 43, 90, 10.1016/j.freeradbiomed.2007.03.026

Lee, 2013, HIV Nef, paxillin, and Pak1/2 regulate activation and secretion of TACE/ADAM10 proteases, Mol Cell, 49, 668, 10.1016/j.molcel.2012.12.004

Blanchard, 2002, TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex, J Immunol, 168, 3235, 10.4049/jimmunol.168.7.3235

Wubbolts, 2003, Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation, J Biol Chem, 278, 10963, 10.1074/jbc.M207550200

Perez-Hernandez, 2013, The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes, J Biol Chem, 288, 11649, 10.1074/jbc.M112.445304

Nazarenko, 2010, Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation, Cancer Res, 70, 1668, 10.1158/0008-5472.CAN-09-2470

Nolte-’t Hoen, 2012, Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions, Nucleic Acids Res, 40, 9272, 10.1093/nar/gks658

Villarroya-Beltri, 2014, Sorting it out: regulation of exosome loading, Semin Cancer Biol, 28, 3, 10.1016/j.semcancer.2014.04.009

Villarroya-Beltri, 2013, Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs, Nat Commun, 4, 2980, 10.1038/ncomms3980

Columba Cabezas, 2013, Sequences within RNA coding for HIV-1 Gag p17 are efficiently targeted to exosomes, Cell Microbiol, 15, 412, 10.1111/cmi.12046

Hollas, 2006, Annexin A2 recognises a specific region in the 3’-UTR of its cognate messenger RNA, Biochim Biophys Acta, 1763, 1325, 10.1016/j.bbamcr.2006.08.043

Schorey, 2008, Exosome function: from tumor immunology to pathogen biology, Traffic, 9, 871, 10.1111/j.1600-0854.2008.00734.x

Berditchevski, 1999, Characterization of integrin-tetraspanin adhesion complexes: role of tetraspanins in integrin signaling, J Cell Biol, 146, 477, 10.1083/jcb.146.2.477

Hwang, 2003, Direct stimulation of naive T cells by membrane vesicles from antigen-presenting cells: distinct roles for CD54 and B7 molecules, Proc Natl Acad Sci U S A, 100, 6670, 10.1073/pnas.1131852100

Nolte-’t Hoen, 2009, Activated T cells recruit exosomes secreted by dendritic cells via LFA-1, Blood, 113, 1977, 10.1182/blood-2008-08-174094

Segura, 2005, ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming, Blood, 106, 216, 10.1182/blood-2005-01-0220

Lee, 2010, A membranous form of ICAM-1 on exosomes efficiently blocks leukocyte adhesion to activated endothelial cells, Biochem Biophys Res Commun, 397, 251, 10.1016/j.bbrc.2010.05.094

Rana, 2012, Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection, Int J Biochem Cell Biol, 44, 1574, 10.1016/j.biocel.2012.06.018

Feng, 2010, Cellular internalization of exosomes occurs through phagocytosis, Traffic, 11, 675, 10.1111/j.1600-0854.2010.01041.x

Fitzner, 2011, Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis, J Cell Sci, 124, 447, 10.1242/jcs.074088

Fruhbeis, 2013, Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication, PLoS Biol, 11, e1001604, 10.1371/journal.pbio.1001604

Parolini, 2009, Microenvironmental pH is a key factor for exosome traffic in tumor cells, J Biol Chem, 284, 34211, 10.1074/jbc.M109.041152

Scheffer, 2013, Tetraspanin CD151 mediates papillomavirus type 16 endocytosis, J Virol, 87, 3435, 10.1128/JVI.02906-12

Raposo, 1996, B lymphocytes secrete antigen-presenting vesicles, J Exp Med, 183, 1161, 10.1084/jem.183.3.1161

Szajnik, 2010, Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg), PLoS One, 5, e11469, 10.1371/journal.pone.0011469

Zitvogel, 1998, Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes, Nat Med, 4, 594, 10.1038/nm0598-594

Admyre, 2006, Direct exosome stimulation of peripheral human T cells detected by ELISPOT, Eur J Immunol, 36, 1772, 10.1002/eji.200535615

Muntasell, 2007, T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes, EMBO J, 26, 4263, 10.1038/sj.emboj.7601842

Bhatnagar, 2007, Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory, J Biol Chem, 282, 25779, 10.1074/jbc.M702277200

Walker, 2009, Cytomegalovirus-infected human endothelial cells can stimulate allogeneic CD4+ memory T cells by releasing antigenic exosomes, J Immunol, 182, 1548, 10.4049/jimmunol.182.3.1548

Wolfers, 2001, Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming, Nat Med, 7, 297, 10.1038/85438

Montecalvo, 2008, Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition, J Immunol, 180, 3081, 10.4049/jimmunol.180.5.3081

Qazi, 2009, Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism, Blood, 113, 2673, 10.1182/blood-2008-04-153536

Viaud, 2011, Updated technology to produce highly immunogenic dendritic cell-derived exosomes of clinical grade: a critical role of interferon-gamma, J Immunother, 34, 65, 10.1097/CJI.0b013e3181fe535b

Karlsson, 2001, “Tolerosomes” are produced by intestinal epithelial cells, Eur J Immunol, 31, 2892, 10.1002/1521-4141(2001010)31:102892::AID-IMMU28923.0.CO;2-I

Peche, 2003, Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection, Transplantation, 76, 1503, 10.1097/01.TP.0000092494.75313.38

Taylor, 2006, Pregnancy-associated exosomes and their modulation of T cell signaling, J Immunol, 176, 1534, 10.4049/jimmunol.176.3.1534

Tarazona, 2011, Human prostasomes express CD48 and interfere with NK cell function, Immunobiology, 216, 41, 10.1016/j.imbio.2010.03.002

Hedlund, 2009, Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function, J Immunol, 183, 340, 10.4049/jimmunol.0803477

Admyre, 2007, Exosomes with immune modulatory features are present in human breast milk, J Immunol, 179, 1969, 10.4049/jimmunol.179.3.1969

Andre, 2002, Malignant effusions and immunogenic tumour-derived exosomes, Lancet, 360, 295, 10.1016/S0140-6736(02)09552-1

Clayton, 2007, Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2, Cancer Res, 67, 7458, 10.1158/0008-5472.CAN-06-3456

Clayton, 2008, Human tumor-derived exosomes down-modulate NKG2D expression, J Immunol, 180, 7249, 10.4049/jimmunol.180.11.7249

Liu, 2006, Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function, J Immunol, 176, 1375, 10.4049/jimmunol.176.3.1375

Valenti, 2006, Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes, Cancer Res, 66, 9290, 10.1158/0008-5472.CAN-06-1819

Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat Commun, 2, 282, 10.1038/ncomms1285

Gutierrez-Vazquez, 2013, Transfer of extracellular vesicles during immune cell-cell interactions, Immunol Rev, 251, 125, 10.1111/imr.12013

Levy, 2005, The tetraspanin web modulates immune-signalling complexes, Nat Rev Immunol, 5, 136, 10.1038/nri1548

Kropshofer, 2002, Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes, Nat Immunol, 3, 61, 10.1038/ni750

Mittelbrunn, 2002, Cutting edge: dynamic redistribution of tetraspanin CD81 at the central zone of the immune synapse in both T lymphocytes and APC, J Immunol, 169, 6691, 10.4049/jimmunol.169.12.6691

Rocha-Perugini, 2013, CD81 controls sustained T cell activation signaling and defines the maturation stages of cognate immunological synapses, Mol Cell Biol, 33, 3644, 10.1128/MCB.00302-13

Imai, 1995, Molecular analyses of the association of CD4 with two members of the transmembrane 4 superfamily, CD81 and CD82, J Immunol, 155, 1229, 10.4049/jimmunol.155.3.1229

Witherden, 2000, CD81 and CD28 costimulate T cells through distinct pathways, J Immunol, 165, 1902, 10.4049/jimmunol.165.4.1902

Miyazaki, 1997, Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81, EMBO J, 16, 4217, 10.1093/emboj/16.14.4217

Maecker, 1997, Normal lymphocyte development but delayed humoral immune response in CD81-null mice, J Exp Med, 185, 1505, 10.1084/jem.185.8.1505

Rocha-Perugini, 2014, Tetraspanins CD9 and CD151 at the immune synapse support T-cell integrin signaling, Eur J Immunol, 44, 1967, 10.1002/eji.201344235

Wright, 2004, Tetraspanin microdomains in immune cell signalling and malignant disease, Tissue Antigens, 64, 533, 10.1111/j.1399-0039.2004.00321.x

Poloso, 2006, CDw78 defines MHC class II-peptide complexes that require Ii chain-dependent lysosomal trafficking, not localization to a specific tetraspanin membrane microdomain, J Immunol, 177, 5451, 10.4049/jimmunol.177.8.5451

Unternaehrer, 2007, The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface, Proc Natl Acad Sci U S A, 104, 234, 10.1073/pnas.0609665104

Sheng, 2009, Tetraspanins CD37 and CD151 differentially regulate Ag presentation and T-cell co-stimulation by DC, Eur J Immunol, 39, 50, 10.1002/eji.200838798