Role of extracellular vesicles in autoimmune diseases

Autoimmunity Reviews

Volumn 15, Issue 2, 2016, Pages 174-183

  Turpin, Delphine ^a   Truchetet, Marie Elise ^a,b   Faustin, Benjamin ^b   Augusto, Jean François ^b   Contin Bordes, Cécile ^a,b   Brisson, Alain ^c   Blanco, Patrick ^a,b   Duffau, Pierre ^b,d  

^a University Hospital Bordeaux   (France)

^b CNRS Bordeaux Segalen University   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d University Hospital Bordeaux 2   (France)

Author keywords

Autoimmune diseases; Exosomes; Extracellular vesicles; Microparticles; Rheumatoid arthritis; Systemic lupus erythematosus

Indexed keywords

BIOLOGICAL MARKER;

ANCA ASSOCIATED VASCULITIS; ANGIOGENESIS; ANTIPHOSPHOLIPID SYNDROME; AUTOIMMUNE DISEASE; CANCER IMMUNOLOGY; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MEMBRANE; CELL PROLIFERATION; CELL STRESS; EXOSOME; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; MEMBRANE MICROPARTICLE; MULTIPLE SCLEROSIS; MULTIVESICULAR BODY; PATHOPHYSIOLOGY; REVIEW; RHEUMATOID ARTHRITIS; SENESCENCE; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; IMMUNOLOGY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

AUTOIMMUNE DISEASES; BIOLOGICAL TRANSPORT; CELL COMMUNICATION; EXTRACELLULAR VESICLES; HUMANS; SIGNAL TRANSDUCTION;

EID: 84954378557     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2015.11.004     Document Type: Review

References (141)

1. Van der Pol E., Boing A.N., Harrison P., Sturk A., Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 2012, 64:676-705.
2. György B., Szabó T.G., Pásztói M., Pál Z., Misják P., Aradi B., et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 2011, 68:2667-2688.
3. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013, 200:373-383.
4. Beyer C., Pisetsky D.S. The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 2010, 6:21-29.
5. Burger D., Schock S., Thompson C.S., Montezano A.C., Hakim A.M., Touyz R.M. Microparticles: biomarkers and beyond. Clin Sci 2013, 124:423-441.
6. Buzas E.I., György B., Nagy G., Falus A., Gay S. Emerging role of extracellular vesicles in inflammatory diseases. Nat Rev Rheumatol 2014, 10:356-364.
7. Colombo M., Raposo G., Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014, 30:255-289.
8. Chaput N., Théry C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 2011, 33:419-440.
9. Denzer K., Kleijmeer M.J., Heijnen H.F., Stoorvogel W., Geuze H.J. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000, 113(Pt 19):3365-3374.
10. Simons M., Raposo G. Exosomes - vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009, 21:575-581.
11. Bobrie A., Colombo M., Raposo G., Théry C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011, 12:1659-1668.
12. Théry C., Boussac M., Véron P., Ricciardi-Castagnoli P., Raposo G., Garin J., et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001, 166:7309-7318.
13. Muntasell A., Berger A.C., Roche P.A. T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes. EMBO J 2007, 26:4263-4272.
14. Arita S., Baba E., Shibata Y., Niiro H., Shimoda S., Isobe T., et al. B cell activation regulates exosomal HLA production. Eur J Immunol 2008, 38:1423-1434.
15. Mathivanan S., Fahner C.J., Reid G.E., Simpson R.J. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 2012, 40:D1241-D1244.
16. Kalra H., Simpson R.J., Ji H., Aikawa E., Altevogt P., Askenase P., et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012, 10. 10.1371/journal.pbio.1001450.
17. Laulagnier K., Motta C., Hamdi S., Roy S., Fauvelle F., Pageaux J.-F., et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 2004, 380:161-171.
18. Subra C., Laulagnier K., Perret B., Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 2007, 89:205-212.
19. Dignat-George F., Boulanger C.M. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 2011, 31:27-33.
20. Batool S., Abbasian N., Burton J.O., Stover C. Microparticles and their roles in inflammation: a review. Open Immunol J 2013, 6:1-14.
21. Théry C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9:581-593.
22. Morelli A.E., Larregina A.T., Shufesky W.J., Sullivan M.L.G., Stolz D.B., Papworth G.D., et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004, 104:3257-3266.
23. Urbanelli L., Magini A., Buratta S., Brozzi A., Sagini K., Polchi A., et al. Signaling pathways in exosomes biogenesis, secretion and fate. Genes 2013, 4:152-170.
24. Théry C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002, 2:569-579.
25. Hugel B., Martínez M.C., Kunzelmann C., Freyssinet J.-M. Membrane microparticles: two sides of the coin. Physiology (Bethesda) 2005, 20:22-27.
26. Piccin A., Murphy W.G., Smith O.P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev 2007, 21:157-171.
27. Zwaal R.F., Schroit A.J. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997, 89:1121-1132.
28. Morel O., Toti F., Hugel B., Freyssinet J.-M. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol 2004, 11:156-164.
29. Distler J.H.W., Huber L.C., Gay S., Distler O., Pisetsky D.S. Microparticles as mediators of cellular cross-talk in inflammatory disease. Autoimmunity 2006, 39:683-690.
30. Bevers E.M., Comfurius P., van Rijn J.L., Hemker H.C., Zwaal R.F. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem FEBS 1982, 122:429-436.
31. Schroit A.J., Tanaka Y., Madsen J., Fidler I.J. The recognition of red blood cells by macrophages: role of phosphatidylserine and possible implications of membrane phospholipid asymmetry. Biol Cell Auspices Eur Cell Biol Organ 1984, 51:227-238.
32. Li M.O., Sarkisian M.R., Mehal W.Z., Rakic P., Flavell R.A. Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 2003, 302:1560-1563.
33. Pisetsky D.S., Ullal A.J., Gauley J., Ning T.C. Microparticles as mediators and biomarkers of rheumatic disease. Rheumatology (Oxford) 2012, 51:1737-1746.
34. Shet A.S. Characterizing blood microparticles: technical aspects and challenges. Vasc Health Risk Manag 2008, 4:769-774.
35. Arraud N., Linares R., Tan S., Gounou C., Pasquet J.-M., Mornet S., et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost 2014, 12:614-627.
36. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009, 19:43-51.
37. Horstman L.L., Jy W., Jimenez J.J., Bidot C., Ahn Y.S. New horizons in the analysis of circulating cell-derived microparticles. Keio J Med 2004, 53:210-230.
38. Lacroix R., Judicone C., Poncelet P., Robert S., Arnaud L., Sampol J., et al. Impact of pre-analytical parameters on the measurement of circulating microparticles: towards standardization of protocol: pre-analytics influence on microparticles analysis. J Thromb Haemost 2012, 10:437-446.
39. Witwer K.W., Buzás E.I., Bemis L.T., Bora A., Lässer C., Lötvall J., et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013, 2. 10.3402/jev.v2i0.20360.
40. Théry C., Amigorena S., Raposo G., Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006, (Al, Chapter 3:Unit 3.22). J. Bonifacino (Ed.).
41. Jy W., Horstman L.L., Jimenez J.J., Ahn Y.S., Biró E., Nieuwland R., et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004, 2:1842-1851.
42. Van Der Pol E., Van Gemert M.J.C., Sturk A., Nieuwland R., Van Leeuwen T.G. Single vs. swarm detection of microparticles and exosomes by flow cytometry. J Thromb Haemost 2012, 10:919-930.
43. Arraud N., Gounou C., Turpin D., Brisson A.R. Fluorescence triggering: a general strategy for enumerating and phenotyping extracellular vesicles by flow cytometry: phenotyping of EVs by fluorescence triggering in FCM. Cytometry A 2015, 10.1002/cyto.a.22669.
44. Chandler W.L., Yeung W., Tait J.F. A new microparticle size calibration standard for use in measuring smaller microparticles using a new flow cytometer. J Thromb Haemost 2011, 9:1216-1224.
45. Van der Vlist E.J., Nolte-'t Hoen E.N.M., Stoorvogel W., Arkesteijn G.J.A., Wauben M.H.M. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc 2012, 7:1311-1326.
46. Nolan J.P., Stoner S.A. A trigger channel threshold artifact in nanoparticle analysis. Cytom Part J Int Soc Anal Cytol 2013, 83:301-305.
47. Arraud N., Gounou C., Linares R., Brisson A.R. A simple flow cytometry method improves the detection of phosphatidylserine-exposing extracellular vesicles. J Thromb Haemost 2015, 13:237-247.
48. Zhu S., Ma L., Wang S., Chen C., Zhang W., Yang L., et al. Light-scattering detection below the level of single fluorescent molecules for high-resolution characterization of functional nanoparticles. ACS Nano 2014, 8:10998-11006.
49. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967, 13:269-288.
50. Heijnen H.F., Schiel A.E., Fijnheer R., Geuze H.J., Sixma J.J. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999, 94:3791-3799.
51. Aalberts M., van Dissel-Emiliani F.M.F., van Adrichem N.P.H., van Wijnen M., Wauben M.H.M., Stout T.A.E., et al. Identification of distinct populations of proteasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod 2012, 86:82.
52. Cloutier N., Tan S., Boudreau L.H., Cramb C., Subbaiah R., Lahey L., et al. The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes: Immune complexes contain microparticles. EMBO Mol Med 2013, 5:235-249.
53. Zonneveld M.I., Brisson A.R., van Herwijnen M.J.C., Tan S., van de Lest C.H.A., Redegeld F.A., et al. Recovery of extracellular vesicles from human breast milk is influenced by sample collection and vesicle isolation procedures. J Extracell Vesicles 2014, 3. 10.3402/jev.v3.24215.
54. Nomura S., Shouzu A., Taomoto K., Togane Y., Goto S., Ozaki Y., et al. Assessment of an ELISA kit for platelet-derived microparticles by joint research at many institutes in Japan. J Atheroscler Thromb 2009, 16:878-887.
55. Revenfeld A.L.S., Bæk R., Nielsen M.H., Stensballe A., Varming K., Jørgensen M. Diagnostic and prognostic potential of extracellular vesicles in peripheral blood. Clin Ther 2014, 36:830-846.
56. Dragovic R.A., Gardiner C., Brooks A.S., Tannetta D.S., Ferguson D.J.P., Hole P., et al. Sizing and phenotyping of cellular vesicles using nanoparticle tracking analysis. Nanomed Nanotechnol Biol Med 2011, 7:780-788.
57. Van der Pol E., Coumans F.A.W., Grootemaat A.E., Gardiner C., Sargent I.L., Harrison P., et al. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 2014, 12:1182-1192.
58. Coumans F.A.W., van der Pol E., Böing A.N., Hajji N., Sturk G., van Leeuwen T.G., et al. Reproducible extracellular vesicle size and concentration determination with tunable resistive pulse sensing. J Extracell Vesicles 2014, 3:25922. 10.3402/jev.v3.25922.
59. Maas S.L.N., de Vrij J., van der Vlist E.J., Geragousian B., van Bloois L., Mastrobattista E., et al. Possibilities and limitations of current technologies for quantification of biological extracellular vesicles and synthetic mimics. J Control Release Off J Control Release Soc 2015, 200:87-96.
60. Pizzirani C., Ferrari D., Chiozzi P., Adinolfi E., Sandonà D., Savaglio E., et al. Stimulation of P2 receptors causes release of IL-1beta-loaded microvesicles from human dendritic cells. Blood 2007, 109:3856-3864.
61. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall 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.
62. Clayton A., Turkes A., Dewitt S., Steadman R., Mason M.D., Hallett M.B. Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J Off Publ Fed Am Soc Exp Biol 2004, 18:977-979.
63. Skokos D., Botros H.G., Demeure C., Morin J., Peronet R., Birkenmeier G., et al. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J Immunol Baltim Md 1950 2003, 170:3037-3045.
64. Admyre C., Johansson S.M., Paulie S., Gabrielsson S. Direct exosome stimulation of peripheral human T cells detected by ELISPOT. Eur J Immunol 2006, 36:1772-1781.
65. Nielsen C.T., Østergaard O., Stener L., Iversen L.V., Truedsson L., Gullstrand B., et al. Increased IgG on cell-derived plasma microparticles in systemic lupus erythematosus is associated with autoantibodies and complement activation. Arthritis Rheum 2012, 64:1227-1236.
66. Ullal A.J., Reich C.F., Clowse M., Criscione-Schreiber L.G., Tochacek M., Monestier M., et al. Microparticles as antigenic targets of antibodies to DNA and nucleosomes in systemic lupus erythematosus. J Autoimmun 2011, 36:173-180.
67. Clayton A., Court J., Navabi H., Adams M., Mason M.D., Hobot J.A., et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J Immunol Methods 2001, 247:163-174.
68. Raposo G., Nijman H.W., Stoorvogel W., Liejendekker R., Harding C.V., Melief C.J., et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996, 183:1161-1172.
69. Admyre C., Bohle B., Johansson S.M., Focke-Tejkl M., Valenta R., Scheynius A., et al. B cell-derived exosomes can present allergen peptides and activate allergen-specific T cells to proliferate and produce TH2-like cytokines. J Allergy Clin Immunol 2007, 120:1418-1424.
70. Luketic L., Delanghe J., Sobol P.T., Yang P., Frotten E., Mossman K.L., et al. Antigen presentation by exosomes released from peptide-pulsed dendritic cells is not suppressed by the presence of active CTL. J Immunol Baltim Md 1950 2007, 179:5024-5032.
71. Utsugi-Kobukai S., Fujimaki H., Hotta C., Nakazawa M., Minami M. MHC class I-mediated exogenous antigen presentation by exosomes secreted from immature and mature bone marrow derived dendritic cells. Immunol Lett 2003, 89:125-131.
72. Hwang I., Shen X., Sprent J. 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 2003, 100:6670-6675.
73. Vincent-Schneider H., Stumptner-Cuvelette P., Lankar D., Pain S., Raposo G., Benaroch P., et al. Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int Immunol 2002, 14:713-722.
74. Théry C., Duban L., Segura E., Véron P., Lantz O., Amigorena S. Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 2002, 3:1156-1162.
75. André F., Chaput N., Schartz N.E.C., Flament C., Aubert N., Bernard J., et al. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J Immunol Baltim Md 1950 2004, 172:2126-2136.
76. Mallegol J., Van Niel G., Lebreton C., Lepelletier Y., Candalh C., Dugave C., et al. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 2007, 132:1866-1876.
77. Montecalvo A., Shufesky W.J., Stolz D.B., Sullivan M.G., Wang Z., Divito S.J., et al. Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition. J Immunol Baltim Md 1950 2008, 180:3081-3090.
78. Segura E., Nicco C., Lombard B., Véron P., Raposo G., Batteux F., et al. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 2005, 106:216-223.
79. Obregon C., Rothen-Rutishauser B., Gitahi S.K., Gehr P., Nicod L.P. Exovesicles from human activated dendritic cells fuse with resting dendritic cells, allowing them to present alloantigens. Am J Pathol 2006, 169:2127-2136.
80. 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.
81. Nakao R., Hasegawa H., Ochiai K., Takashiba S., Ainai A., Ohnishi M., et al. Outer membrane vesicles of Porphyromonas gingivalis elicit a mucosal immune response. PLoS One 2011, 6. 10.1371/journal.pone.0026163.
82. Hong S.-W., Kim M.-R., Lee E.-Y., Kim J.H., Kim Y.-S., Jeon S.G., et al. Extracellular vesicles derived from Staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy 2011, 66:351-359.
83. Prados-Rosales R., Baena A., Martinez L.R., Luque-Garcia J., Kalscheuer R., Veeraraghavan U., et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest 2011, 121:1471-1483.
84. Théry C., Regnault A., Garin J., Wolfers J., Zitvogel L., Ricciardi-Castagnoli P., et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 1999, 147:599-610.
85. Beninson L.A., Maslanik T., Murphy M.J., Fleshner M. 116. The functional role of exosome associated extracellular heat shock protein 72 following exposure to acute stress. Brain Behav Immun 2012, 26(Suppl. 1):S32-S33.
86. Zhang B., Yin Y., Lai R.C., Lim S.K. Immunotherapeutic potential of extracellular vesicles. Front Immunol 2014, 5:518.
87. Pisetsky D.S., Lipsky P.E. Microparticles as autoadjuvants in the pathogenesis of SLE. Nat Rev Rheumatol 2010, 6:368-372.
88. Maugeri N., Rovere-Querini P., Baldini M., Baldissera E., Sabbadini M.G., Bianchi M.E., et al. Oxidative stress elicits platelet/leukocyte inflammatory interactions via HMGB1: a candidate for microvessel injury in sytemic sclerosis. Antioxid Redox Signal 2014, 20:1060-1074.
89. Gentili M., Kowal J., Tkach M., Satoh T., Lahaye X., Conrad C., et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 2015, 349:1232-1236.
90. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:148-155.
91. Peterson D.B., Sander T., Kaul S., Wakim B.T., Halligan B., Twigger S., et al. Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics 2008, 8:2430-2446.
92. Boilard E., Nigrovic P.A., Larabee K., Watts G.F.M., Coblyn J.S., Weinblatt M.E., et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010, 327:580-583.
93. Berckmans R.J., Nieuwland R., Kraan M.C., Schaap M.C.L., Pots D., Smeets T.J.M., et al. Synovial microparticles from arthritic patients modulate chemokine and cytokine release by synoviocytes. Arthritis Res Ther 2005, 7:R536-R544.
94. Zhang H.-G., Liu C., Su K., Su K., Yu S., Zhang L., et al. A membrane form of TNF-alpha presented by exosomes delays T cell activation-induced cell death. J Immunol Baltim Md 1950 2006, 176:7385-7393.
95. Barry O.P., Pratico D., Lawson J.A., FitzGerald G.A. Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles. J Clin Invest 1997, 99:2118-2127.
96. Esser J., Gehrmann U., D'Alexandri F.L., Hidalgo-Estévez A.M., Wheelock C.E., Scheynius A., et al. Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration. J Allergy Clin Immunol 2010, 126:1032-1040.
97. Distler J.H.W., Jüngel A., Huber L.C., Seemayer C.A., Reich C.F., Gay R.E., et al. The induction of matrix metalloproteinase and cytokine expression in synovial fibroblasts stimulated with immune cell microparticles. Proc Natl Acad Sci U S A 2005, 102:2892-2897.
98. Lo Cicero A., Majkowska I., Nagase H., Di Liegro I., Troeberg L. Microvesicles shed by oligodendroglioma cells and rheumatoid synovial fibroblasts contain aggrecanase activity. Matrix Biol J Int Soc Matrix Biol 2012, 31:229-233.
99. Sáenz-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.
100. EL Andaloussi S., Mäger I., Breakefield X.O., Wood M.J.A. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013, 12:347-357.
101. Silvariño R., Danza Á., Mérola V., Bérez A., Méndez E., Espinosa G., et al. Venous thromboembolic disease in systemic autoimmune diseases: an association to keep in mind. Autoimmun Rev 2012, 12:289-294.
102. Michelson A.D., Rajasekhar D., Bednarek F.J., Barnard M.R. Platelet and platelet-derived microparticle surface factor V/Va binding in whole blood: differences between neonates and adults. Thromb Haemost 2000, 84:689-694.
103. Müller I., Klocke A., Alex M., Kotzsch M., Luther T., Morgenstern E., et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J Off Publ Fed Am Soc Exp Biol 2003, 17:476-478.
104. Scholz T., Temmler U., Krause S., Heptinstall S., Lösche W. Transfer of tissue factor from platelets to monocytes: role of platelet-derived microvesicles and CD62P. Thromb Haemost 2002, 88:1033-1038.
105. Teixeira P.C., Ferber P., Vuilleumier N., Cutler P. Biomarkers for cardiovascular risk assessment in autoimmune diseases. Proteomics Clin Appl 2015, 9:48-57.
106. Brodsky S.V., Zhang F., Nasjletti A., Goligorsky M.S. Endothelium-derived microparticles impair endothelial function in vitro. Am J Physiol Heart Circ Physiol 2004, 286:H1910-H1915.
107. Pfister S.L. Role of platelet microparticles in the production of thromboxane by rabbit pulmonary artery. Hypertension 2004, 43:428-433.
108. Mezentsev A., Merks R.M.H., O'Riordan E., Chen J., Mendelev N., Goligorsky M.S., et al. Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol 2005, 289:H1106-H1114.
109. Zhou L., Lu G., Shen L., Wang L., Wang M. Serum levels of three angiogenic factors in systemic lupus erythematosus and their clinical significance. BioMed Res Int 2014, 2014:627126.
110. Rautou P.-E., Vion A.-C., Amabile N., Chironi G., Simon A., Tedgui A., et al. Microparticles, vascular function, and atherothrombosis. Circ Res 2011, 109:593-606.
111. Reich N., Beyer C., Gelse K., Akhmetshina A., Dees C., Zwerina J., et al. Microparticles stimulate angiogenesis by inducing ELR(+) CXC-chemokines in synovial fibroblasts. J Cell Mol Med 2011, 15:756-762.
112. Knijff-Dutmer E.A.J., Koerts J., Nieuwland R., Kalsbeek-Batenburg E.M., van de Laar M.A. Elevated levels of platelet microparticles are associated with disease activity in rheumatoid arthritis. Arthritis Rheum 2002, 46:1498-1503.
113. Umekita K., Hidaka T., Ueno S., Takajo I., Kai Y., Nagatomo Y., et al. Leukocytapheresis (LCAP) decreases the level of platelet-derived microparticles (MPs) and increases the level of granulocytes-derived MPs: a possible connection with the effect of LCAP on rheumatoid arthritis. Mod Rheumatol Jpn Rheum Assoc 2009, 19:265-272.
114. Berckmans R.J., Nieuwland R., Tak P.P., Böing A.N., Romijn F.P.H.T.M., Kraan M.C., et al. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum 2002, 46:2857-2866.
115. Pamuk G.E., Vural O., Turgut B., Demir M., Pamuk O.N., Cakir N. Increased platelet activation markers in rheumatoid arthritis: are they related with subclinical atherosclerosis?. Platelets 2008, 19:146-154.
116. Boilard E., Blanco P., Nigrovic P.A. Platelets: active players in the pathogenesis of arthritis and SLE. Nat Rev Rheumatol 2012, 8:534-542.
117. Pereira J., Alfaro G., Goycoolea M., Quiroga T., Ocqueteau M., Massardo L., et al. Circulating platelet-derived microparticles in systemic lupus erythematosus. Association with increased thrombin generation and procoagulant state. Thromb Haemost 2006, 95:94-99.
118. Sellam J., Proulle V., Jungel A., Ittah M., Miceli Richard C., Gottenberg J.-E., et al. Increased levels of circulating microparticles in primary Sjogren's syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity. Arthritis Res Ther 2009, 11:R156.
119. Joseph J.E., Harrison P., Mackie I.J., Isenberg D.A., Machin S.J. Increased circulating platelet-leucocyte complexes and platelet activation in patients with antiphospholipid syndrome, systemic lupus erythematosus and rheumatoid arthritis. Br J Haematol 2001, 115:451-459.
120. Nielsen C.T. Circulating microparticles in systemic lupus erythematosus. Dan Med J 2012, 59:B4548.
121. Dignat-George F., Camoin-Jau L., Sabatier F., Arnoux D., Anfosso F., Bardin N., et al. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thromb Haemost 2004, 91:667-673.
122. Jy W., Tiede M., Bidot C.J., Horstman L.L., Jimenez J.J., Chirinos J., et al. Platelet activation rather than endothelial injury identifies risk of thrombosis in subjects positive for antiphospholipid antibodies. Thromb Res 2007, 121:319-325.
123. Ardoin S.P., Shanahan J.C., Pisetsky D.S. The role of microparticles in inflammation and thrombosis. Scand J Immunol 2007, 66:159-165.
124. Nomura S., Inami N., Ozaki Y., Kagawa H., Fukuhara S. Significance of microparticles in progressive systemic sclerosis with interstitial pneumonia. Platelets 2008, 19:192-198.
125. Guiducci S., Distler J.H.W., Jüngel A., Huscher D., Huber L.C., Michel B.A., et al. The relationship between plasma microparticles and disease manifestations in patients with systemic sclerosis. Arthritis Rheum 2008, 58:2845-2853.
126. Iversen L.V., Østergaard O., Ullman S., Nielsen C.T., Halberg P., Karlsmark T., et al. Circulating microparticles and plasma levels of soluble E- and P-selectins in patients with systemic sclerosis. Scand J Rheumatol 2013, 42:473-482.
127. Jennette J.C., Falk R.J., Hu P., Xiao H. Pathogenesis of antineutrophil cytoplasmic autoantibody-associated small-vessel vasculitis. Annu Rev Pathol 2013, 8:139-160.
128. Halbwachs L., Lesavre P. Endothelium-neutrophil interactions in ANCA-associated diseases. J Am Soc Nephrol 2012, 23:1449-1461.
129. Daniel L., Fakhouri F., Joly D., Mouthon L., Nusbaum P., Grunfeld J.-P., et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int 2006, 69:1416-1423.
130. Erdbruegger U., Grossheim M., Hertel B., Wyss K., Kirsch T., Woywodt A., et al. Diagnostic role of endothelial microparticles in vasculitis. Rheumatol Oxf Engl 2008, 47:1820-1825.
131. Hong Y., Eleftheriou D., Hussain A.A.K., Price-Kuehne F.E., Savage C.O., Jayne D., et al. Anti-neutrophil cytoplasmic antibodies stimulate release of neutrophil microparticles. J Am Soc Nephrol 2012, 23:49-62.
132. Kambas K., Chrysanthopoulou A., Vassilopoulos D., Apostolidou E., Skendros P., Girod A., et al. Tissue factor expression in neutrophil extracellular traps and neutrophil derived microparticles in antineutrophil cytoplasmic antibody associated vasculitis may promote thromboinflammation and the thrombophilic state associated with the disease. Ann Rheum Dis 2014, 73:1854-1863.
133. Sun D., Zhuang X., Xiang X., Liu Y., Zhang S., Liu C., et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther J Am Soc Gene Ther 2010, 18:1606-1614.
134. Yin W., Ouyang S., Li Y., Xiao B., Yang H. Immature dendritic cell-derived exosomes: a promise subcellular vaccine for autoimmunity. Inflammation 2013, 36:232-240.
135. Bianco N.R., Kim S.H., Ruffner M.A., Robbins P.D. Therapeutic effect of exosomes from indoleamine 2,3-dioxygenase-positive dendritic cells in collagen-induced arthritis and delayed-type hypersensitivity disease models. Arthritis Rheum 2009, 60:380-389.
136. Kim S.H., Bianco N., Menon R., Lechman E.R., Shufesky W.J., Morelli A.E., et al. Exosomes derived from genetically modified DC expressing FasL are anti-inflammatory and immunosuppressive. Mol Ther J Am Soc Gene Ther 2006, 13:289-300.
137. Yang C., Robbins P.D. Immunosuppressive exosomes: a new approach for treating arthritis. Int J Rheumatol 2012, 2012:573528.
138. Kim S.H., Bianco N.R., Shufesky W.J., Morelli A.E., Robbins P.D. Effective treatment of inflammatory disease models with exosomes derived from dendritic cells genetically modified to express IL-4. J Immunol Baltim Md 1950 2007, 179:2242-2249.
139. Kim S.-H., Lechman E.R., Bianco N., Menon R., Keravala A., Nash J., et al. Exosomes derived from IL-10-treated dendritic cells can suppress inflammation and collagen-induced arthritis. J Immunol Baltim Md 1950 2005, 174:6440-6448.
140. Kreimer S., Belov A.M., Ghiran I., Murthy S.K., Frank D.A., Ivanov A.R. Mass-spectrometry-based molecular characterization of extracellular vesicles: lipidomics and proteomics. J Proteome Res 2015, 14:2367-2384.
141. Vader P., Breakefield X.O., Wood M.J.A. Extracellular vesicles: emerging targets for cancer therapy. Trends Mol Med 2014, 20:385-393.