Focus on Extracellular Vesicles: Physiological Role and Signalling Properties of Extracellular Membrane Vesicles
Open accessAbstract
Extracellular vesicles (EVs) are a heterogeneous population of secreted membrane vesicles, with distinct biogenesis routes, biophysical properties and different functions both in physiological conditions and in disease. The release of EVs is a widespread biological process, which is conserved across species. In recent years, numerous studies have demonstrated that several bioactive molecules are trafficked with(in) EVs, such as microRNAs, mRNAs, proteins and lipids. The understanding of their final impact on the biology of specific target cells remains matter of intense debate in the field. Also, EVs have attracted great interest as potential novel cell-free therapeutics. Here we describe the proposed physiological and pathological functions of EVs, with a particular focus on their molecular content. Also, we discuss the advances in the knowledge of the mechanisms regulating the secretion of EV-associated molecules and the specific pathways activated upon interaction with the target cell, highlighting the role of EVs in the context of the immune system and as mediators of the intercellular signalling in the brain.
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EVs have potential as cell-free therapeutics.
“Given their unique biological and pharmacological characteristics, EVs have attracted interest as mediators of physiological and pathophysiological processes, and have potential as cell-free therapeutics4.”
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- [1]Gould S.J. Raposo G. As we wait: Coping with an imperfect nomenclature for extracellular vesicles J. Extracell. Vesicles 2013 2 10.3402/jev.v2i0.20389 24009890 PMC3760635 · DOI
- [2]Colombo M. Raposo G. Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles Annu. Rev. Cell Dev. Biol. 2014 30 255 289 10.1146/annurev-cellbio-101512-122326 25288114 · DOI · Paper page
- [3]Deatherage B.L. Cookson B.T. Membrane vesicle release in bacteria, eukaryotes, and archaea: A conserved yet underappreciated aspect of microbial life Infect. Immun. 2012 80 1948 1957 10.1128/IAI.06014-11 22409932 PMC3370574 · DOI
- [4]Kuehn M.J. Kesty N.C. Bacterial outer membrane vesicles and the host-pathogen interaction Genes Dev. 2005 19 2645 2655 10.1101/gad.1299905 16291643 · DOI
- [6]Bobrie A. Colombo M. Raposo G. Thery C. Exosome secretion: Molecular mechanisms and roles in immune responses Traffic 2011 12 1659 1668 10.1111/j.1600-0854.2011.01225.x 21645191 · DOI
- [7]Mittelbrunn M. Gutierrez-Vazquez C. Villarroya-Beltri C. Gonzalez S. Sanchez-Cabo F. Gonzalez M.A. Bernad A. Sanchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells Nat. Commun. 2011 2 10.1038/ncomms1285 21505438 PMC3104548 · DOI
- [8]Wiley R.D. Gummuluru S. Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection Proc. Natl. Acad. Sci. USA 2006 103 738 743 10.1073/pnas.0507995103 16407131 PMC1334656 · DOI
- [9]Bukong T.N. Momen-Heravi F. Kodys K. Bala S. Szabo G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90 PLoS Pathog. 2014 10 171 10.1371/journal.ppat.1004424 25275643 PMC4183590 · DOI
- [10]Longatti A. Boyd B. Chisari F.V. Virion-independent transfer of replication-competent hepatitis C virus RNA between permissive cells J. Virol. 2015 89 2956 2961 10.1128/JVI.02721-14 25505060 PMC4325714 · DOI
- [11]Fevrier B. Vilette D. Archer F. Loew D. Faigle W. Vidal M. Laude H. Raposo G. Cells release prions in association with exosomes Proc. Natl. Acad. Sci. USA 2004 101 9683 9688 10.1073/pnas.0308413101 15210972 PMC470735 · DOI
- [12]Eder C. Mechanisms of interleukin-1β release Immunobiology 2009 214 543 553 10.1016/j.imbio.2008.11.007 19250700 · DOI
- [13]Li J. Liu K. Liu Y. Xu Y. Zhang F. Yang H. Liu J. Pan T. Chen J. Wu M. Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity Nat. Immunol. 2013 14 793 803 10.1038/ni.2647 23832071 · DOI
- [14]Cossetti C. Iraci N. Mercer T.R. Leonardi T. Alpi E. Drago D. Alfaro-Cervello C. Saini H.K. Davis M.P. Schaeffer J. Extracellular vesicles from neural stem cells transfer IFN-γ via Ifngr1 to activate Stat1 signaling in target cells Mol. Cell 2014 56 193 204 10.1016/j.molcel.2014.08.020 25242146 PMC4578249 · DOI
- [15]Al-Nedawi K. Meehan B. Rak J. Microvesicles: Messengers and mediators of tumor progression Cell Cycle 2009 8 2014 2018 10.4161/cc.8.13.8988 19535896 · DOI
- [16]Raposo G. Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends J. Cell Biol. 2013 200 373 383 10.1083/jcb.201211138 23420871 PMC3575529 · DOI · Paper page
- [17]Smith J.A. Leonardi T. Huang B. Iraci N. Vega B. Pluchino S. Extracellular vesicles and their synthetic analogues in aging and age-associated brain diseases Biogerontology 2015 16 147 185 10.1007/s10522-014-9510-7 24973266 PMC4578234 · DOI
- [18]Cocucci E. Racchetti G. Meldolesi J. Shedding microvesicles: Artefacts no more Trends Cell Biol. 2009 19 43 51 10.1016/j.tcb.2008.11.003 19144520 · DOI · Paper page
- [19]Kalra H. Drummen G.P.C. Mathivanan S. Focus on extracellular vesicles: An introduction to the next small big thing Int. J. Mol. Sci. 2016 17 10.3390/ijms17020170 26861301 PMC4783904 · DOI
- [20]Kim D.K. Lee J. Simpson R.J. Lotvall J. Gho Y.S. EVpedia: A community web resource for prokaryotic and eukaryotic extracellular vesicles research Semin. Cell Dev. Biol. 2015 40 4 7 10.1016/j.semcdb.2015.02.005 25704310 · DOI
- [21]Kalra H. Simpson R.J. Ji H. Aikawa E. Altevogt P. Askenase P. Bond V.C. Borras F.E. Breakefield X. Budnik V. Vesiclepedia: A compendium for extracellular vesicles with continuous community annotation PLoS Biol. 2012 10 171 10.1371/journal.pbio.1001450 23271954 PMC3525526 · DOI · Paper page
- [22]Wilkinson G. Smeeton N. Skuse D. Fry J. Consultation for physical illnesses by patients diagnosed and treated for psychiatric disorders by a general practitioner: 20 year follow up study BMJ 1988 297 776 778 10.1136/bmj.297.6651.776 3142546 PMC1834412 · DOI
- [23]Ratajczak J. Miekus K. Kucia M. Zhang J. Reca R. Dvorak P. Ratajczak M.Z. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery Leukemia 2006 20 847 856 10.1038/sj.leu.2404132 16453000 · DOI
- [24]Valadi H. Ekstrom K. Bossios A. Sjostrand M. Lee J.J. Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 2007 9 654 659 10.1038/ncb1596 17486113 · DOI · Paper page
- [25]Skog J. Wurdinger T. van Rijn S. Meijer D.H. Gainche L. Sena-Esteves M. Curry W.T. Jr. Carter B.S. Krichevsky A.M. Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 2008 10 1470 1476 10.1038/ncb1800 19011622 PMC3423894 · DOI · Paper page
- [26]Balaj L. Lessard R. Dai L. Cho Y.J. Pomeroy S.L. Breakefield X.O. Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences Nat. Commun. 2011 2 10.1038/ncomms1180 21285958 PMC3040683 · DOI
- [27]Eldh M. Ekstrom K. Valadi H. Sjostrand M. Olsson B. Jernas M. Lotvall J. Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA PLoS ONE 2010 5 171 10.1371/journal.pone.0015353 21179422 PMC3003701 · DOI
- [28]Deregibus M.C. Cantaluppi V. Calogero R. Lo Iacono M. Tetta C. Biancone L. Bruno S. Bussolati B. Camussi G. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA Blood 2007 110 2440 2448 10.1182/blood-2007-03-078709 17536014 · DOI
- [29]Montecalvo A. Larregina A.T. Shufesky W.J. Stolz D.B. Sullivan M.L. Karlsson J.M. Baty C.J. Gibson G.A. Erdos G. Wang Z. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes Blood 2012 119 756 766 10.1182/blood-2011-02-338004 22031862 PMC3265200 · DOI · Paper page
- [30]Pegtel D.M. Cosmopoulos K. Thorley-Lawson D.A. van Eijndhoven M.A. Hopmans E.S. Lindenberg J.L. de Gruijl T.D. Wurdinger T. Middeldorp J.M. Functional delivery of viral miRNAs via exosomes Proc. Natl. Acad. Sci. USA 2010 107 6328 6333 10.1073/pnas.0914843107 20304794 PMC2851954 · DOI
- [31]Ismail N. Wang Y. Dakhlallah D. Moldovan L. Agarwal K. Batte K. Shah P. Wisler J. Eubank T.D. Tridandapani S. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer Blood 2013 121 984 995 10.1182/blood-2011-08-374793 23144169 PMC3567345 · DOI
- [32]Zhuang G. Wu X. Jiang Z. Kasman I. Yao J. Guan Y. Oeh J. Modrusan Z. Bais C. Sampath D. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway EMBO J. 2012 31 3513 3523 10.1038/emboj.2012.183 22773185 PMC3433782 · DOI
- [33]Zhang Y. Liu D. Chen X. Li J. Li L. Bian Z. Sun F. Lu J. Yin Y. Cai X. Secreted monocytic miR-150 enhances targeted endothelial cell migration Mol. Cell 2010 39 133 144 10.1016/j.molcel.2010.06.010 20603081 · DOI
- [34]Fabbri M. Paone A. Calore F. Galli R. Gaudio E. Santhanam R. Lovat F. Fadda P. Mao C. Nuovo G.J. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response Proc. Natl. Acad. Sci. USA 2012 109 E2110 E2116 10.1073/pnas.1209414109 22753494 PMC3412003 · DOI
- [35]Okoye I.S. Coomes S.M. Pelly V.S. Czieso S. Papayannopoulos V. Tolmachova T. Seabra M.C. Wilson M.S. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells Immunity 2014 41 89 103 10.1016/j.immuni.2014.05.019 25035954 PMC4104030 · DOI
- [36]Vojtech L. Woo S. Hughes S. Levy C. Ballweber L. Sauteraud R.P. Strobl J. Westerberg K. Gottardo R. Tewari M. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions Nucleic Acids Res. 2014 42 7290 7304 10.1093/nar/gku347 24838567 PMC4066774 · DOI
- [37]Bellingham S.A. Coleman B.M. Hill A.F. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells Nucleic Acids Res. 2012 40 10937 10949 10.1093/nar/gks832 22965126 PMC3505968 · DOI
- [38]Huang X. Yuan T. Tschannen M. Sun Z. Jacob H. Du M. Liang M. Dittmar R.L. Liu Y. Liang M. Characterization of human plasma-derived exosomal RNAs by deep sequencing BMC Genom. 2013 14 319 10.1186/1471-2164-14-319 23663360 PMC3653748 · DOI
- [40]Gezer U. Ozgur E. Cetinkaya M. Isin M. Dalay N. Long non-coding RNAs with low expression levels in cells are enriched in secreted exosomes Cell Biol. Int. 2014 38 1076 1079 10.1002/cbin.10301 24798520 · DOI
- [41]Takahashi K. Yan I.K. Kogure T. Haga H. Patel T. Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellular cancer FEBS Open Bio 2014 4 458 467 10.1016/j.fob.2014.04.007 24918061 PMC4050189 · DOI
- [42]Brandimarte C. Valesini G. de Berardinis P.G. Palange P. Serra P. Balsano F. Relapsing polychondritis: A case with anticartilage, anticardiolipin and anticentromere antibodies Recent. Prog. Med. 1988 79 67 69 3387656
- [43]Lee T.H. D’Asti E. Magnus N. Al-Nedawi K. Meehan B. Rak J. Microvesicles as mediators of intercellular communication in cancer—The emerging science of cellular “debris” Semin. Immunopathol. 2011 33 455 467 10.1007/s00281-011-0250-3 21318413 · DOI
- [44]Thakur B.K. Zhang H. Becker A. Matei I. Huang Y. Costa-Silva B. Zheng Y. Hoshino A. Brazier H. Xiang J. Double-stranded DNA in exosomes: A novel biomarker in cancer detection Cell Res. 2014 24 766 769 10.1038/cr.2014.44 24710597 PMC4042169 · DOI
- [45]Olsson I. Ronquist G. Nucleic acid association to human prostasomes Arch. Androl. 1990 24 1 10 10.3109/01485019008986852 1691619 · DOI
- [46]Tannetta D. Dragovic R. Alyahyaei Z. Southcombe J. Extracellular vesicles and reproduction-promotion of successful pregnancy Cell. Mol. Immunol. 2014 11 548 563 10.1038/cmi.2014.42 24954226 PMC4220835 · DOI
- [47]Ronquist G. Prostasomes are mediators of intercellular communication: From basic research to clinical implications J. Intern. Med. 2012 271 400 413 10.1111/j.1365-2796.2011.02487.x 22112042 · DOI
- [48]Thery C. Zitvogel L. Amigorena S. Exosomes: Composition, biogenesis and function Nat. Rev. Immunol. 2002 2 569 579 12154376
- [49]Zoller M. Tetraspanins: Push and pull in suppressing and promoting metastasis Nat. Rev. Cancer 2009 9 40 55 10.1038/nrc2543 19078974 · DOI
- [50]Rana S. Zoller M. Exosome target cell selection and the importance of exosomal tetraspanins: A hypothesis Biochem. Soc. Trans. 2011 39 559 562 10.1042/BST0390559 21428939 · DOI
- [51]Tauro B.J. Greening D.W. Mathias R.A. Ji H. Mathivanan S. Scott A.M. Simpson R.J. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes Methods 2012 56 293 304 10.1016/j.ymeth.2012.01.002 22285593 · DOI
- [52]Colombo M. Moita C. van Niel G. Kowal J. Vigneron J. Benaroch P. Manel N. Moita L.F. Thery C. Raposo G. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles J. Cell Sci. 2013 126 5553 5565 10.1242/jcs.128868 24105262 · DOI
- [53]Tauro B.J. Greening D.W. Mathias R.A. Mathivanan S. Ji H. Simpson R.J. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids Mol. Cell. Proteom. 2013 12 587 598 10.1074/mcp.M112.021303 23230278 PMC3591653 · DOI
- [54]Witwer K.W. Buzas E.I. Bemis L.T. Bora A. Lasser C. Lotvall J. Nolte-′t Hoen E.N. Piper M.G. Sivaraman S. Skog J. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research J. Extracell. Vesicles 2013 2 10.3402/jev.v2i0.20360 24009894 PMC3760646 · DOI
- [55]Lancaster G.I. Febbraio M.A. Exosome-dependent trafficking of HSP70: A novel secretory pathway for cellular stress proteins J. Biol. Chem. 2005 280 23349 23355 10.1074/jbc.M502017200 15826944 · DOI
- [56]Gastpar R. Gehrmann M. Bausero M.A. Asea A. Gross C. Schroeder J.A. Multhoff G. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells Cancer Res. 2005 65 5238 5247 10.1158/0008-5472.CAN-04-3804 15958569 PMC1785299 · DOI
- [57]Clayton A. Turkes A. Navabi H. Mason M.D. Tabi Z. Induction of heat shock proteins in B-cell exosomes J. Cell Sci. 2005 118 3631 3638 10.1242/jcs.02494 16046478 · DOI
- [58]Taylor A.R. Robinson M.B. Gifondorwa D.J. Tytell M. Milligan C.E. Regulation of heat shock protein 70 release in astrocytes: Role of signaling kinases Dev. Neurobiol. 2007 67 1815 1829 10.1002/dneu.20559 17701989 · DOI
- [59]Gupta S. Knowlton A.A. HSP60 trafficking in adult cardiac myocytes: Role of the exosomal pathway Am. J. Physiol. Heart Circ. Physiol. 2007 292 H3052 H3056 10.1152/ajpheart.01355.2006 17307989 · DOI
- [60]Zhan R. Leng X. Liu X. Wang X. Gong J. Yan L. Wang L. Wang Y. Wang X. Qian L.J. Heat shock protein 70 is secreted from endothelial cells by a non-classical pathway involving exosomes Biochem. Biophys. Res. Commun. 2009 387 229 233 10.1016/j.bbrc.2009.06.095 19555663 · DOI
- [61]De Jong O.G. Verhaar M.C. Chen Y. Vader P. Gremmels H. Posthuma G. Schiffelers R.M. Gucek M. van Balkom B.W. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes J. Extracell. Vesicles 2012 1 10.3402/jev.v1i0.18396 24009886 PMC3760650 · DOI
- [62]Beninson L.A. Fleshner M. Exosomes: An emerging factor in stress-induced immunomodulation Semin. Immunol. 2014 26 394 401 10.1016/j.smim.2013.12.001 24405946 · DOI
- [63]Kalamvoki M. Du T. Roizman B. Cells infected with herpes simplex virus 1 export to uninfected cells exosomes containing STING, viral mRNAs, and microRNAs Proc. Natl. Acad. Sci. USA 2014 111 E4991 E4996 10.1073/pnas.1419338111 25368198 PMC4246290 · DOI
- [64]Fevrier B. Vilette D. Laude H. Raposo G. Exosomes: A bubble ride for prions? Traffic 2005 6 10 17 10.1111/j.1600-0854.2004.00247.x 15569241 · DOI
- [65]Porto-Carreiro I. Fevrier B. Paquet S. Vilette D. Raposo G. Prions and exosomes: From PrPc trafficking to PrPsc propagation Blood Cells Mol. Dis. 2005 35 143 148 10.1016/j.bcmd.2005.06.013 16099696 · DOI
- [66]Kore R.A. Abraham E.C. Inflammatory cytokines, interleukin-1 β and tumor necrosis factor-α, upregulated in glioblastoma multiforme, raise the levels of CRYAB in exosomes secreted by U373 glioma cells Biochem. Biophys. Res. Commun. 2014 453 326 331 10.1016/j.bbrc.2014.09.068 25261722 PMC4278587 · DOI
- [67]Kato T. Miyaki S. Ishitobi H. Nakamura Y. Nakasa T. Lotz M.K. Ochi M. Exosomes from IL-1β stimulated synovial fibroblasts induce osteoarthritic changes in articular chondrocytes Arthritis Res. Ther. 2014 16 10.1186/ar4679 25092378 PMC4261911 · DOI
- [68]Ekstrom E.J. Bergenfelz C. von Bulow V. Serifler F. Carlemalm E. Jonsson G. Andersson T. Leandersson K. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells Mol. Cancer 2014 13 10.1186/1476-4598-13-88 24766647 PMC4022450 · DOI · Paper page
- [70]Villarroya-Beltri C. Gutierrez-Vazquez C. Sanchez-Cabo F. Perez-Hernandez D. Vazquez J. Martin-Cofreces N. Martinez-Herrera D.J. Pascual-Montano A. Mittelbrunn M. Sanchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs Nat. Commun. 2013 4 10.1038/ncomms3980 24356509 PMC3905700 · DOI
- [71]Wang K. Zhang S. Weber J. Baxter D. Galas D.J. Export of microRNAs and microRNA-protective protein by mammalian cells Nucleic Acids Res. 2010 38 7248 7259 10.1093/nar/gkq601 20615901 PMC2978372 · DOI · Paper page
- [72]Melo S.A. Sugimoto H. O’Connell J.T. Kato N. Villanueva A. Vidal A. Qiu L. Vitkin E. Perelman L.T. Melo C.A. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis Cancer Cell 2014 26 707 721 10.1016/j.ccell.2014.09.005 25446899 PMC4254633 · DOI
- [73]Munro T.P. Magee R.J. Kidd G.J. Carson J.H. Barbarese E. Smith L.M. Smith R. Mutational analysis of a heterogeneous nuclear ribonucleoprotein A2 response element for RNA trafficking J. Biol. Chem. 1999 274 34389 34295 10.1074/jbc.274.48.34389 10567417 · DOI
- [74]Levesque K. Halvorsen M. Abrahamyan L. Chatel-Chaix L. Poupon V. Gordon H. DesGroseillers L. Gatignol A. Mouland A.J. Trafficking of HIV-1 RNA is mediated by heterogeneous nuclear ribonucleoprotein A2 expression and impacts on viral assembly Traffic 2006 7 1177 1193 10.1111/j.1600-0854.2006.00461.x 17004321 · DOI
- [75]Booth A.M. Fang Y. Fallon J.K. Yang J.M. Hildreth J.E. Gould S.J. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane J. Cell Biol. 2006 172 923 935 10.1083/jcb.200508014 16533950 PMC2063735 · DOI
- [76]Koppers-Lalic D. Hackenberg M. Bijnsdorp I.V. van Eijndhoven M.A. Sadek P. Sie D. Zini N. Middeldorp J.M. Ylstra B. de Menezes R.X. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes Cell Rep. 2014 8 1649 1658 10.1016/j.celrep.2014.08.027 25242326 · DOI
- [77]Squadrito M.L. Baer C. Burdet F. Maderna C. Gilfillan G.D. Lyle R. Ibberson M. de Palma M. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells Cell Rep. 2014 8 1432 1446 10.1016/j.celrep.2014.07.035 25159140 · DOI · Paper page
- [78]Bolukbasi M.F. Mizrak A. Ozdener G.B. Madlener S. Strobel T. Erkan E.P. Fan J.B. Breakefield X.O. Saydam O. miR-1289 and “Zipcode”-like Sequence Enrich mRNAs in Microvesicles Mol. Ther. Nucleic Acids 2012 1 171 10.1038/mtna.2011.2 23344721 PMC3381601 · DOI
- [79]Batagov A.O. Kuznetsov V.A. Kurochkin I.V. Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles BMC Genom. 2011 12 10.1186/1471-2164-12-S3-S18 22369587 PMC3333177 · DOI
- [80]Szostak N. Royo F. Rybarczyk A. Szachniuk M. Blazewicz J. del Sol A. Falcon-Perez J.M. Sorting signal targeting mRNA into hepatic extracellular vesicles RNA Biol. 2014 11 836 844 10.4161/rna.29305 24921245 PMC4179958 · DOI
- [81]Villarroya-Beltri C. Baixauli F. Gutierrez-Vazquez C. Sanchez-Madrid F. Mittelbrunn M. Sorting it out: Regulation of exosome loading Semin. Cancer Biol. 2014 28 3 13 10.1016/j.semcancer.2014.04.009 24769058 PMC4640178 · DOI
- [82]Moreno-Gonzalo O. Villarroya-Beltri C. Sanchez-Madrid F. Post-translational modifications of exosomal proteins Front. Immunol. 2014 5 10.3389/fimmu.2014.00383 25157254 PMC4128227 · DOI
- [83]Henne W.M. Buchkovich N.J. Emr S.D. The ESCRT pathway Dev. Cell 2011 21 77 91 10.1016/j.devcel.2011.05.015 21763610 · DOI
- [84]Blot V. Perugi F. Gay B. Prevost M.C. Briant L. Tangy F. Abriel H. Staub O. Dokhelar M.C. Pique C. Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding J. Cell Sci. 2004 117 2357 2367 10.1242/jcs.01095 15126635 · DOI
- [85]Verweij F.J. van Eijndhoven M.A. Hopmans E.S. Vendrig T. Wurdinger T. Cahir-McFarland E. Kieff E. Geerts D. van der Kant R. Neefjes J. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-kappaB activation EMBO J. 2011 30 2115 2129 10.1038/emboj.2011.123 21527913 PMC3117644 · DOI
- [86]Shen B. Wu N. Yang J.M. Gould S.J. Protein targeting to exosomes/microvesicles by plasma membrane anchors J. Biol. Chem. 2011 286 14383 14395 10.1074/jbc.M110.208660 21300796 PMC3077638 · DOI
- [87]Yuyama K. Sun H. Mitsutake S. Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia J. Biol. Chem. 2012 287 10977 10989 10.1074/jbc.M111.324616 22303002 PMC3322859 · DOI
- [88]Trams E.G. Lauter C.J. Salem N. Jr. Heine U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles Biochim. Biophys. Acta 1981 645 63 70 10.1016/0005-2736(81)90512-5 6266476 · DOI
- [89]Stegmayr B. Ronquist G. Promotive effect on human sperm progressive motility by prostasomes Urol. Res. 1982 10 253 257 10.1007/BF00255932 6219486 · DOI
- [90]Harding C. Heuser J. Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes J. Cell Biol. 1983 97 329 339 10.1083/jcb.97.2.329 6309857 PMC2112509 · DOI · Paper page
- [91]Pan B.T. Johnstone R.M. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor Cell 1983 33 967 978 10.1016/0092-8674(83)90040-5 6307529 · DOI
- [92]Cossetti C. Smith J.A. Iraci N. Leonardi T. Alfaro-Cervello C. Pluchino S. Extracellular membrane vesicles and immune regulation in the brain Front. Physiol. 2012 3 10.3389/fphys.2012.00117 22557978 PMC3340916 · DOI
- [94]Denzer K. van Eijk M. Kleijmeer M.J. Jakobson E. de Groot C. Geuze H.J. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface J. Immunol. 2000 165 1259 1265 10.4049/jimmunol.165.3.1259 10903724 · DOI
- [95]Robbins P.D. Morelli A.E. Regulation of immune responses by extracellular vesicles Nat. Rev. Immunol. 2014 14 195 208 10.1038/nri3622 24566916 PMC4350779 · DOI · Paper page
- [96]Vincent-Schneider H. Stumptner-Cuvelette P. Lankar D. Pain S. Raposo G. Benaroch P. Bonnerot C. Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells Int. Immunol. 2002 14 713 722 10.1093/intimm/dxf048 12096030 · DOI
- [97]Mallegol J. van Niel G. Lebreton C. Lepelletier Y. Candalh C. Dugave C. Heath J.K. Raposo G. Cerf-Bensussan N. Heyman M. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells Gastroenterology 2007 132 1866 1876 10.1053/j.gastro.2007.02.043 17484880 · DOI
- [98]Morelli A.E. Larregina A.T. Shufesky W.J. Sullivan M.L. Stolz D.B. Papworth G.D. Zahorchak A.F. Logar A.J. Wang Z. Watkins S.C. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells Blood 2004 104 3257 3266 10.1182/blood-2004-03-0824 15284116 · DOI
- [99]Thery C. Duban L. Segura E. Veron P. Lantz O. Amigorena S. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes Nat. Immunol. 2002 3 1156 1162 10.1038/ni854 12426563 · DOI
- [100]Bedford P. Garner K. Knight S.C. MHC class II molecules transferred between allogeneic dendritic cells stimulate primary mixed leukocyte reactions Int. Immunol. 1999 11 1739 1744 10.1093/intimm/11.11.1739 10545477 · DOI
- [101]Patel D.M. Arnold P.Y. White G.A. Nardella J.P. Mannie M.D. Class II MHC/peptide complexes are released from APC and are acquired by T cell responders during specific antigen recognition J. Immunol. 1999 163 5201 5210 10553040
- [102]Thery C. Regnault A. Garin J. Wolfers J. Zitvogel L. Ricciardi-Castagnoli P. Raposo G. Amigorena S. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73 J. Cell Biol. 1999 147 599 610 10.1083/jcb.147.3.599 10545503 PMC2151184 · DOI
- [103]Zitvogel L. Regnault A. Lozier A. Wolfers J. Flament C. Tenza D. Ricciardi-Castagnoli P. Raposo G. Amigorena S. Eradication of established murine tumors using a novel cell-free vaccine: Dendritic cell-derived exosomes Nat. Med. 1998 4 594 600 10.1038/nm0598-594 9585234 · DOI
- [104]Segura E. Guerin C. Hogg N. Amigorena S. Thery C. CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo J. Immunol. 2007 179 1489 1496 10.4049/jimmunol.179.3.1489 17641014 · DOI
- [105]Nolte-′t Hoen E.N. Buschow S.I. Anderton S.M. Stoorvogel W. Wauben M.H. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1 Blood 2009 113 1977 1981 10.1182/blood-2008-08-174094 19064723 · DOI
- [106]Monks C.R. Freiberg B.A. Kupfer H. Sciaky N. Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells Nature 1998 395 82 86 9738502
- [107]Bhatnagar S. Shinagawa K. Castellino F.J. Schorey J.S. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo Blood 2007 110 3234 3244 10.1182/blood-2007-03-079152 17666571 PMC2200902 · DOI
- [108]Bhatnagar S. Schorey J.S. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory J. Biol. Chem. 2007 282 25779 25789 10.1074/jbc.M702277200 17591775 PMC3636815 · DOI
- [110]Ramachandra L. Qu Y. Wang Y. Lewis C.J. Cobb B.A. Takatsu K. Boom W.H. Dubyak G.R. Harding C.V. Mycobacterium tuberculosis synergizes with ATP to induce release of microvesicles and exosomes containing major histocompatibility complex class II molecules capable of antigen presentation Infect. Immun. 2010 78 5116 5125 10.1128/IAI.01089-09 20837713 PMC2981298 · DOI
- [111]Iero M. Valenti R. Huber V. Filipazzi P. Parmiani G. Fais S. Rivoltini L. Tumour-released exosomes and their implications in cancer immunity Cell Death Differ. 2008 15 80 88 10.1038/sj.cdd.4402237 17932500 · DOI
- [112]Zhang H.G. Grizzle W.E. Exosomes and cancer: A newly described pathway of immune suppression Clin. Cancer Res. 2011 17 959 964 10.1158/1078-0432.CCR-10-1489 21224375 PMC3155407 · DOI
- [113]Wieckowski E. Whiteside T.L. Human tumor-derived vs dendritic cell-derived exosomes have distinct biologic roles and molecular profiles Immunol. Res. 2006 36 247 254 10.1385/IR:36:1:247 17337785 · DOI
- [114]Clayton A. Mitchell J.P. Court J. Mason M.D. Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2 Cancer Res. 2007 67 7458 7466 10.1158/0008-5472.CAN-06-3456 17671216 · DOI
- [115]Andreola G. Rivoltini L. Castelli C. Huber V. Perego P. Deho P. Squarcina P. Accornero P. Lozupone F. Lugini L. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles J. Exp. Med. 2002 195 1303 1316 10.1084/jem.20011624 12021310 PMC2193755 · DOI
- [116]Huber V. Fais S. Iero M. Lugini L. Canese P. Squarcina P. Zaccheddu A. Colone M. Arancia G. Gentile M. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: Role in immune escape Gastroenterology 2005 128 1796 1804 10.1053/j.gastro.2005.03.045 15940614 · DOI
- [117]Szajnik M. Czystowska M. Szczepanski M.J. Mandapathil M. Whiteside T.L. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg) PLoS ONE 2010 5 171 10.1371/journal.pone.0011469 20661468 PMC2908536 · DOI
- [118]Zeelenberg I.S. Ostrowski M. Krumeich S. Bobrie A. Jancic C. Boissonnas A. Delcayre A. le Pecq J.B. Combadiere B. Amigorena S. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses Cancer Res. 2008 68 1228 1235 10.1158/0008-5472.CAN-07-3163 18281500 · DOI
- [119]Valenti R. Huber V. Filipazzi P. Pilla L. Sovena G. Villa A. Corbelli A. Fais S. Parmiani G. Rivoltini L. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-β-mediated suppressive activity on T lymphocytes Cancer Res. 2006 66 9290 9298 10.1158/0008-5472.CAN-06-1819 16982774 · DOI · Paper page
- [120]Liu C. Yu S. Zinn K. Wang J. Zhang L. Jia Y. Kappes J.C. Barnes S. Kimberly R.P. Grizzle W.E. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function J. Immunol. 2006 176 1375 1385 10.4049/jimmunol.176.3.1375 16424164 · DOI
- [121]Greening D.W. Gopal S.K. Xu R. Simpson R.J. Chen W. Exosomes and their roles in immune regulation and cancer Semin. Cell Dev. Biol. 2015 40 72 81 10.1016/j.semcdb.2015.02.009 25724562 · DOI
- [122]Hedlund M. Stenqvist A.C. Nagaeva O. Kjellberg L. Wulff M. Baranov V. Mincheva-Nilsson L. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: Evidence for immunosuppressive function J. Immunol. 2009 183 340 351 10.4049/jimmunol.0803477 19542445 · DOI
- [123]Van Niel G. Raposo G. Candalh C. Boussac M. Hershberg R. Cerf-Bensussan N. Heyman M. Intestinal epithelial cells secrete exosome-like vesicles Gastroenterology 2001 121 337 349 10.1053/gast.2001.26263 11487543 · DOI
- [124]Van Niel G. Mallegol J. Bevilacqua C. Candalh C. Brugiere S. Tomaskovic-Crook E. Heath J.K. Cerf-Bensussan N. Heyman M. Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice Gut 2003 52 1690 1697 10.1136/gut.52.12.1690 14633944 PMC1773888 · DOI
- [125]Qazi K.R. Torregrosa Paredes P. Dahlberg B. Grunewald J. Eklund A. Gabrielsson S. Proinflammatory exosomes in bronchoalveolar lavage fluid of patients with sarcoidosis Thorax 2010 65 1016 1024 10.1136/thx.2009.132027 20880880 · DOI
- [126]Prado N. Marazuela E.G. Segura E. Fernandez-Garcia H. Villalba M. Thery C. Rodriguez R. Batanero E. Exosomes from bronchoalveolar fluid of tolerized mice prevent allergic reaction J. Immunol. 2008 181 1519 1525 10.4049/jimmunol.181.2.1519 18606707 · DOI
- [127]De Carvalho J.V. de Castro R.O. da Silva E.Z. Silveira P.P. da Silva-Januario M.E. Arruda E. Jamur M.C. Oliver C. Aguiar R.S. daSilva L.L. Nef neutralizes the ability of exosomes from CD4+ T cells to act as decoys during HIV-1 infection PLoS ONE 2014 9 171 10.1371/journal.pone.0113691 25423108 PMC4244142 · DOI
- [128]Raivich G. Banati R. Brain microglia and blood-derived macrophages: Molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease Brain Res. Brain Res. Rev. 2004 46 261 281 10.1016/j.brainresrev.2004.06.006 15571769 · DOI
- [129]Streit W.J. Kincaid-Colton C.A. The brain’s immune system Sci. Am. 1995 273 58 61 10.1038/scientificamerican1195-54 8966536 · DOI
- [130]Kettenmann H. Hanisch U.K. Noda M. Verkhratsky A. Physiology of microglia Physiol. Rev. 2011 91 461 553 10.1152/physrev.00011.2010 21527731 · DOI · Paper page
- [131]Tremblay M.E. Stevens B. Sierra A. Wake H. Bessis A. Nimmerjahn A. The role of microglia in the healthy brain J. Neurosci. 2011 31 16064 16069 10.1523/JNEUROSCI.4158-11.2011 22072657 PMC6633221 · DOI · Paper page
- [132]Aloisi F. Ambrosini E. Columba-Cabezas S. Magliozzi R. Serafini B. Intracerebral regulation of immune responses Ann. Med. 2001 33 510 515 10.3109/07853890108995960 11730157 · DOI
- [133]Kettenmann H. Neuroscience: The brain’s garbage men Nature 2007 446 987 989 10.1038/nature05713 17410127 · DOI
- [136]Bianco F. Pravettoni E. Colombo A. Schenk U. Moller T. Matteoli M. Verderio C. Astrocyte-derived ATP induces vesicle shedding and IL-1 β release from microglia J. Immunol. 2005 174 7268 7277 10.4049/jimmunol.174.11.7268 15905573 · DOI · Paper page
- [137]Bianco F. Perrotta C. Novellino L. Francolini M. Riganti L. Menna E. Saglietti L. Schuchman E.H. Furlan R. Acid sphingomyelinase activity triggers microparticle release from glial cells EMBO J. 2009 28 1043 1054 10.1038/emboj.2009.45 19300439 PMC2664656 · DOI · Paper page
- [138]Verderio C. Muzio L. Turola E. Bergami A. Novellino L. Ruffini F. Riganti L. Corradini I. Francolini M. Garzetti L. Myeloid microvesicles are a marker and therapeutic target for neuroinflammation Ann. Neurol. 2012 72 610 624 10.1002/ana.23627 23109155 · DOI · Paper page
- [139]Kramer-Albers E.M. Bretz N. Tenzer S. Winterstein C. Mobius W. Berger H. Nave K.A. Schild H. Trotter J. Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: Trophic support for axons? Proteom. Clin. Appl. 2007 1 1446 1461 10.1002/prca.200700522 21136642 · DOI
- [140]Bakhti M. Winter C. Simons M. Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles J. Biol. Chem. 2011 286 787 796 10.1074/jbc.M110.190009 20978131 PMC3013037 · DOI
- [141]Lopez-Verrilli M.A. Picou F. Court F.A. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system Glia 2013 61 1795 1806 10.1002/glia.22558 24038411 · DOI · Paper page
- [142]Fitzner D. Schnaars M. van Rossum D. Krishnamoorthy G. Dibaj P. Bakhti M. Regen T. Hanisch U.K. Simons M. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis J. Cell Sci. 2011 124 447 458 10.1242/jcs.074088 21242314 · DOI · Paper page
- [143]Antonucci F. Turola E. Riganti L. Caleo M. Gabrielli M. Perrotta C. Novellino L. Clementi E. Giussani P. Viani P. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism EMBO J. 2012 31 1231 1240 10.1038/emboj.2011.489 22246184 PMC3297996 · DOI · Paper page
- [144]Wang S. Cesca F. Loers G. Schweizer M. Buck F. Benfenati F. Schachner M. Kleene R. Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes J. Neurosci. 2011 31 7275 7290 10.1523/JNEUROSCI.6476-10.2011 21593312 PMC6622588 · DOI · Paper page
- [145]Schiera G. Proia P. Alberti C. Mineo M. Savettieri G. di Liegro I. Neurons produce FGF2 and VEGF and secrete them at least in part by shedding extracellular vesicles J. Cell. Mol. Med. 2007 11 1384 1394 10.1111/j.1582-4934.2007.00100.x 18205708 PMC4401300 · DOI
- [146]Lachenal G. Pernet-Gallay K. Chivet M. Hemming F.J. Belly A. Bodon G. Blot B. Haase G. Goldberg Y. Sadoul R. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity Mol. Cell. Neurosci. 2011 46 409 418 10.1016/j.mcn.2010.11.004 21111824 · DOI
- [147]Korkut C. Ataman B. Ramachandran P. Ashley J. Barria R. Gherbesi N. Budnik V. Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless Cell 2009 139 393 404 10.1016/j.cell.2009.07.051 19837038 PMC2785045 · DOI · Paper page
- [148]Gross J.C. Chaudhary V. Bartscherer K. Boutros M. Active Wnt proteins are secreted on exosomes Nat. Cell Biol. 2012 14 1036 1045 10.1038/ncb2574 22983114 · DOI
- [149]Sheldon H. Heikamp E. Turley H. Dragovic R. Thomas P. Oon C.E. Leek R. Edelmann M. Kessler B. Sainson R.C. New mechanism for Notch signaling to endothelium at a distance by δ-like 4 incorporation into exosomes Blood 2010 116 2385 2394 10.1182/blood-2009-08-239228 20558614 · DOI
- [150]Panakova D. Sprong H. Marois E. Thiele C. Eaton S. Lipoprotein particles are required for Hedgehog and Wingless signalling Nature 2005 435 58 65 10.1038/nature03504 15875013 · DOI
- [151]Peinado H. Aleckovic M. Lavotshkin S. Matei I. Costa-Silva B. Moreno-Bueno G. Hergueta-Redondo M. Williams C. Garcia-Santos G. Ghajar C. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET Nat. Med. 2012 18 883 891 10.1038/nm.2753 22635005 PMC3645291 · DOI · Paper page
- [152]Costa-Silva B. Aiello N.M. Ocean A.J. Singh S. Zhang H. Thakur B.K. Becker A. Hoshino A. Mark M.T. Molina H. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver Nat. Cell Biol. 2015 17 816 826 10.1038/ncb3169 25985394 PMC5769922 · DOI · Paper page
- [154]Yeh Y.Y. Ozer H.G. Lehman A.M. Maddocks K. Yu L. Johnson A.J. Byrd J.C. Characterization of CLL exosomes reveals a distinct microRNA signature and enhanced secretion by activation of BCR signaling Blood 2015 125 3297 3305 10.1182/blood-2014-12-618470 25833959 PMC4440883 · DOI
- [155]Boelens M.C. Wu T.J. Nabet B.Y. Xu B. Qiu Y. Yoon T. Azzam D.J. Twyman-Saint Victor C. Wiemann B.Z. Ishwaran H. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways Cell 2014 159 499 513 10.1016/j.cell.2014.09.051 25417103 PMC4283810 · DOI
- [156]Ciardiello C. Cavallini L. Spinelli C. Yang J. Reis-Sobreiro M. de Candia P. Minciacchi V.R. di Vizio D. Focus on extracellular vesicles: New frontiers of cell-to-cell communication in cancer Int. J. Mol. Sci. 2016 17 10.3390/ijms17020175 26861306 PMC4783909 · DOI
- [157]Camussi G. Deregibus M.C. Bruno S. Grange C. Fonsato V. Tetta C. Exosome/microvesicle-mediated epigenetic reprogramming of cells Am. J. Cancer Res. 2011 1 98 110 21969178 PMC3180104
- [158]Mack M. Kleinschmidt A. Bruhl H. Klier C. Nelson P.J. Cihak J. Plachy J. Stangassinger M. Erfle V. Schlondorff D. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: A mechanism for cellular human immunodeficiency virus 1 infection Nat. Med. 2000 6 769 775 10.1038/77498 10888925 · DOI
- [159]Ross C.A. Poirier M.A. Opinion: What is the role of protein aggregation in neurodegeneration? Nat. Rev. Mol. Cell Biol. 2005 6 891 898 10.1038/nrm1742 16167052 · DOI
- [160]Bellingham S.A. Guo B.B. Coleman B.M. Hill A.F. Exosomes: Vehicles for the transfer of toxic proteins associated with neurodegenerative diseases? Front. Physiol. 2012 3 10.3389/fphys.2012.00124 22563321 PMC3342525 · DOI · Paper page
- [162]Vella L.J. Sharples R.A. Lawson V.A. Masters C.L. Cappai R. Hill A.F. Packaging of prions into exosomes is associated with a novel pathway of PrP processing J. Pathol. 2007 211 582 590 10.1002/path.2145 17334982 · DOI
- [163]Ghidoni R. Benussi L. Binetti G. Exosomes: The Trojan horses of neurodegeneration Med. Hypotheses 2008 70 1226 1227 10.1016/j.mehy.2007.12.003 18226468 · DOI
- [164]Peralta O.A. Eyestone W.H. Quantitative and qualitative analysis of cellular prion protein (PrPC) expression in bovine somatic tissues Prion 2009 3 161 170 10.4161/pri.3.3.9772 19806026 PMC2802781 · DOI
- [166]Mabbott N.A. MacPherson G.G. Prions and their lethal journey to the brain Nat. Rev. Microbiol. 2006 4 201 211 10.1038/nrmicro1346 16462753 · DOI
- [167]Gousset K. Schiff E. Langevin C. Marijanovic Z. Caputo A. Browman D.T. Chenouard N. de Chaumont F. Martino A. Enninga J. Prions hijack tunnelling nanotubes for intercellular spread Nat. Cell Biol. 2009 11 328 336 10.1038/ncb1841 19198598 · DOI
- [168]Schneider A. Simons M. Exosomes: Vesicular carriers for intercellular communication in neurodegenerative disorders Cell Tissue Res. 2013 352 33 47 10.1007/s00441-012-1428-2 22610588 PMC3602607 · DOI
- [169]Godsave S.F. Wille H. Kujala P. Latawiec D. DeArmond S.J. Serban A. Prusiner S.B. Peters P.J. Cryo-immunogold electron microscopy for prions: Toward identification of a conversion site J. Neurosci. 2008 28 12489 12499 10.1523/JNEUROSCI.4474-08.2008 19020041 PMC2796247 · DOI
- [170]Marijanovic Z. Caputo A. Campana V. Zurzolo C. Identification of an intracellular site of prion conversion PLoS Pathog. 2009 5 171 10.1371/journal.ppat.1000426 19424437 PMC2673690 · DOI
- [171]Avramopoulos D. Genetics of Alzheimer’s disease: Recent advances Genome Med. 2009 1 10.1186/gm34 19341505 PMC2664945 · DOI · Paper page
- [172]Murphy M.P. LeVine H. 3rd Alzheimer’s disease and the amyloid-β peptide J. Alzheimers Dis. 2010 19 311 323 20061647 PMC2813509
- [173]Avila J. Lucas J.J. Perez M. Hernandez F. Role of tau protein in both physiological and pathological conditions Physiol. Rev. 2004 84 361 384 10.1152/physrev.00024.2003 15044677 · DOI · Paper page
- [174]Rajendran L. Honsho M. Zahn T.R. Keller P. Geiger K.D. Verkade P. Simons K. Alzheimer’s disease β-amyloid peptides are released in association with exosomes Proc. Natl. Acad. Sci. USA 2006 103 11172 11177 10.1073/pnas.0603838103 16837572 PMC1544060 · DOI · Paper page
- [176]Guo J.L. Lee V.M. Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles J. Biol. Chem. 2011 286 15317 15331 10.1074/jbc.M110.209296 21372138 PMC3083182 · DOI · Paper page
- [178]Ravits J.M. La Spada A.R. ALS motor phenotype heterogeneity, focality, and spread: Deconstructing motor neuron degeneration Neurology 2009 73 805 811 10.1212/WNL.0b013e3181b6bbbd 19738176 PMC2739608 · DOI
- [180]Grad L.I. Yerbury J.J. Turner B.J. Guest W.C. Pokrishevsky E. O′Neill M.A. Yanai A. Silverman J.M. Zeineddine R. Corcoran L. Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms Proc. Natl. Acad. Sci. USA 2014 111 3620 3625 10.1073/pnas.1312245111 24550511 PMC3948312 · DOI
- [181]Gomes C. Keller S. Altevogt P. Costa J. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis Neurosci. Lett. 2007 428 43 46 10.1016/j.neulet.2007.09.024 17942226 · DOI
- [182]Compston A. Coles A. Multiple sclerosis Lancet 2008 372 1502 1517 10.1016/S0140-6736(08)61620-7 18970977 · DOI
- [183]Saenz-Cuesta M. Osorio-Querejeta I. Otaegui D. Extracellular vesicles in multiple sclerosis: what are they telling us? Front. Cell. Neurosci. 2014 8 10.3389/fncel.2014.00100 24734004 PMC3975116 · DOI
- [184]Minagar A. Jy W. Jimenez J.J. Sheremata W.A. Mauro L.M. Mao W.W. Horstman L.L. Ahn Y.S. Elevated plasma endothelial microparticles in multiple sclerosis Neurology 2001 56 1319 1324 10.1212/WNL.56.10.1319 11376181 · DOI
- [185]Sbai O. Ould-Yahoui A. Ferhat L. Gueye Y. Bernard A. Charrat E. Mehanna A. Risso J.J. Chauvin J.P. Fenouillet E. Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes Glia 2010 58 344 366 10.1002/glia.20927 19780201 · DOI
- [186]Jy W. Minagar A. Jimenez J.J. Sheremata W.A. Mauro L.M. Horstman L.L. Bidot C. Ahn Y.S. Endothelial microparticles (EMP) bind and activate monocytes: Elevated EMP-monocyte conjugates in multiple sclerosis Front. Biosci. 2004 9 3137 3144 10.2741/1466 15353343 · DOI
- [187]Sheremata W.A. Jy W. Delgado S. Minagar A. McLarty J. Ahn Y. Interferon-β1a reduces plasma CD31+ endothelial microparticles (CD31+EMP) in multiple sclerosis J. Neuroinflamm. 2006 3 10.1186/1742-2094-3-23 16952316 PMC1584221 · DOI
- [188]Siegel S.R. Mackenzie J. Chaplin G. Jablonski N.G. Griffiths L. Circulating microRNAs involved in multiple sclerosis Mol. Biol. Rep. 2012 39 6219 6225 10.1007/s11033-011-1441-7 22231906 · DOI
- [189]Gatson N.N. Williams J.L. Powell N.D. McClain M.A. Hennon T.R. Robbins P.D. Whitacre C.C. Induction of pregnancy during established EAE halts progression of CNS autoimmune injury via pregnancy-specific serum factors J. Neuroimmunol. 2011 230 105 113 10.1016/j.jneuroim.2010.09.010 20950868 PMC3021646 · DOI
- [190]Williams J.L. Gatson N.N. Smith K.M. Almad A. McTigue D.M. Whitacre C.C. Serum exosomes in pregnancy-associated immune modulation and neuroprotection during CNS autoimmunity Clin. Immunol. 2013 149 236 243 10.1016/j.clim.2013.04.005 23706172 PMC3778091 · DOI
- [191]Yu L. Yang F. Jiang L. Chen Y. Wang K. Xu F. Wei Y. Cao X. Wang J. Cai Z. Exosomes with membrane-associated TGF-β1 from gene-modified dendritic cells inhibit murine EAE independently of MHC restriction Eur. J. Immunol. 2013 43 2461 2472 10.1002/eji.201243295 23716181 · DOI
- [192]Davis S. Lees K. Donnan G. Treating the acute stroke patient as an emergency: Current practices and future opportunities Int. J. Clin. Pract. 2006 60 399 407 10.1111/j.1368-5031.2006.00873.x 16620351 PMC1448697 · DOI
- [193]Butcher K. Parsons M. Baird T. Barber A. Donnan G. Desmond P. Tress B. Davis S. Perfusion thresholds in acute stroke thrombolysis Stroke 2003 34 2159 2164 10.1161/01.STR.0000086529.83878.A2 12893953 · DOI
- [194]Reed S.D. Cramer S.C. Blough D.K. Meyer K. Jarvik J.G. Treatment with tissue plasminogen activator and inpatient mortality rates for patients with ischemic stroke treated in community hospitals Stroke 2001 32 1832 1840 10.1161/01.STR.32.8.1832 11486113 · DOI
- [195]Majid A. Neuroprotection in stroke: Past, present, and future ISRN Neurol. 2014 2014 10.1155/2014/515716 24579051 PMC3918861 · DOI
- [196]Anderson H.C. Garimella R. Tague S.E. The role of matrix vesicles in growth plate development and biomineralization Front. Biosci. 2005 10 822 837 10.2741/1576 15569622 · DOI
- [197]New S.E. Goettsch C. Aikawa M. Marchini J.F. Shibasaki M. Yabusaki K. Libby P. Shanahan C.M. Croce K. Aikawa E. Macrophage-derived matrix vesicles: An alternative novel mechanism for microcalcification in atherosclerotic plaques Circ. Res. 2013 113 72 77 10.1161/CIRCRESAHA.113.301036 23616621 PMC3703850 · DOI · Paper page
- [198]New S.E. Aikawa E. Role of extracellular vesicles in de novo mineralization: An additional novel mechanism of cardiovascular calcification Arterioscler. Thromb. Vasc. Biol. 2013 33 1753 1758 10.1161/ATVBAHA.112.300128 23766262 PMC3788633 · DOI
- [199]Hutcheson J.D. Goettsch C. Pham T. Iwashita M. Aikawa M. Singh S.A. Aikawa E. Enrichment of calcifying extracellular vesicles using density-based ultracentrifugation protocol J. Extracell. Vesicles 2014 3 10.3402/jev.v3.25129 25491249 PMC4261240 · DOI
- [200]Huang J. Choudhri T.F. Winfree C.J. McTaggart R.A. Kiss S. Mocco J. Kim L.J. Protopsaltis T.S. Zhang Y. Pinsky D.J. Postischemic cerebrovascular E-selectin expression mediates tissue injury in murine stroke Stroke 2000 31 3047 3053 10.1161/01.STR.31.12.3047 11108771 · DOI
- [201]Cherian P. Hankey G.J. Eikelboom J.W. Thom J. Baker R.I. McQuillan A. Staton J. Yi Q. Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes Stroke 2003 34 2132 2137 10.1161/01.STR.0000086466.32421.F4 12907813 · DOI
- [202]Lee S.T. Chu K. Jung K.H. Kim J.M. Moon H.J. Bahn J.J. Im W.S. Sunwoo J. Moon J. Kim M. Circulating CD62E+ microparticles and cardiovascular outcomes PLoS ONE 2012 7 171 10.1371/journal.pone.0035713 22563392 PMC3338519 · DOI
- [203]Jung K.H. Chu K. Lee S.T. Park H.K. Bahn J.J. Kim D.H. Kim J.H. Kim M. Kun Lee S. Roh J.K. Circulating endothelial microparticles as a marker of cerebrovascular disease Ann. Neurol. 2009 66 191 199 10.1002/ana.21681 19743467 · DOI
- [204]Martino G. Pluchino S. The therapeutic potential of neural stem cells Nat. Rev. Neurosci. 2006 7 395 406 10.1038/nrn1908 16760919 · DOI
- [205]Lee S.T. Chu K. Jung K.H. Kim S.J. Kim D.H. Kang K.M. Hong N.H. Kim J.H. Ban J.J. Park H.K. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke Brain 2008 131 616 629 10.1093/brain/awm306 18156155 · DOI · Paper page
- [207]Pluchino S. Quattrini A. Brambilla E. Gritti A. Salani G. Dina G. Galli R. Del Carro U. Amadio S. Bergami A. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis Nature 2003 422 688 694 10.1038/nature01552 12700753 · DOI
- [208]Pluchino S. Zanotti L. Rossi B. Brambilla E. Ottoboni L. Salani G. Martinello M. Cattalini A. Bergami A. Furlan R. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism Nature 2005 436 266 271 10.1038/nature03889 16015332 · DOI
- [209]Aharonowiz M. Einstein O. Fainstein N. Lassmann H. Reubinoff B. Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis PLoS ONE 2008 3 171 10.1371/journal.pone.0003145 18773082 PMC2522282 · DOI
- [210]Pluchino S. Gritti A. Blezer E. Amadio S. Brambilla E. Borsellino G. Cossetti C. Del Carro U. Comi G. t Hart B. Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates Ann. Neurol. 2009 66 343 354 10.1002/ana.21745 19798728 · DOI · Paper page
- [211]Pluchino S. Zanotti L. Brambilla E. Rovere-Querini P. Capobianco A. Alfaro-Cervello C. Salani G. Cossetti C. Borsellino G. Battistini L. Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function PLoS ONE 2009 4 171 10.1371/journal.pone.0005959 19543526 PMC2694997 · DOI
- [212]Pluchino S. Zanotti L. Deleidi M. Martino G. Neural stem cells and their use as therapeutic tool in neurological disorders Brain Res. Brain Res. Rev. 2005 48 211 219 10.1016/j.brainresrev.2004.12.011 15850660 · DOI
- [213]Einstein O. Fainstein N. Vaknin I. Mizrachi-Kol R. Reihartz E. Grigoriadis N. Lavon I. Baniyash M. Lassmann H. Ben-Hur T. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression Ann. Neurol. 2007 61 209 218 10.1002/ana.21033 17187374 · DOI
- [214]Einstein O. Karussis D. Grigoriadis N. Mizrachi-Kol R. Reinhartz E. Abramsky O. Ben-Hur T. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis Mol. Cell. Neurosci. 2003 24 1074 1082 10.1016/j.mcn.2003.08.009 14697670 · DOI
200 of 259 shown
- Authors
- Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S.
- Affiliations
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- European Bioinformatics Institute (GB)
- Corresponding author
- Pluchino, Stefano
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2016-02-06
- Volume
- 17
- Issue
- 2
- Pages
- 171
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC4783905
- OpenAlex
- W2269341591
- Cited by
- 301
- References
- 279
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 31 · 2023: 26 · 2022: 30 · 2021: 48 · 2020: 41 · 2019: 34 · 2018: 24 · 2017: 23 · 2016: 14
- FWCI
- 2.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Multiple Sclerosis Society (RG-4001-A1)
- Fondazione Italiana Sclerosi Multipla (RG 2010/R/31)
- Wellcome Trust (FP7/2007–2013)
- Multiple Sclerosis Society
- Ministero della Salute
- Cambridge Trust
- Evelyn Trust (RG69865, 69865)
- Gates Cambridge Trust
- Institute on the Environment, University of Minnesota
- Medical Research Council (MC_PC_12009)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Keywords
- extracellular vesicles, membrane vesicles, vesicle biogenesis, microRNA, mRNA, proteins, lipids, intercellular communication, immune system, brain
- MeSH terms
- Extracellular Vesicles, Animals, Biological Transport, Cell Communication, Cell Transformation, Neoplastic, Disease Susceptibility, Humans, Proteins, RNA, Signal Transduction, Drug Delivery Systems, Exosomes, Immunomodulation
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