Extracellular vesicles in cardiovascular disease: Are they Jedi or Sith?

Journal of Physiology

Volumn 594, Issue 11, 2016, Pages 2881-2894

  Osteikoetxea, Xabier ^a   Németh, Andrea ^a   Sódar, Barbara W ^a   Vukman, Krisztina V ^a   Buzás, Edit Irén ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8;

CARDIOVASCULAR DISEASE; CELL FUNCTION; CELL ISOLATION; CELLULAR SECRETION; CYTOKINE RELEASE; EXOSOME; HEART INFARCTION SIZE; HUMAN; IMMUNOLOGICAL TOLERANCE; LIMIT OF DETECTION; LYMPHOCYTE PROLIFERATION; PARTICLE SIZE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; UPREGULATION; ANIMAL; MEMBRANE MICROPARTICLE; METABOLISM; PATHOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; CELL-DERIVED MICROPARTICLES; EXOSOMES; EXTRACELLULAR VESICLES; HUMANS;

EID: 84961821100     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271336     Document Type: Review

References (98)

1. Alexy T, Rooney K, Weber M, Gray WD & Searles CD (2014). TNF-α alters the release and transfer of microparticle-encapsulated miRNAs from endothelial cells. Physiol Genomics 46, 833-840.
2. Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S & Brisson AR (2014). Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost 12, 614-627.
3. Arslan F, Lai RC, Smeets MB, Akeroyd L, Choo A, Aguor ENE, Timmers L, van Rijen HV, Doevendans PA, Pasterkamp G, Lim SK & de Kleijn DP (2013). Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res 10, 301-312.
4. Azevedo L, Janiszewski M, Pontieri V, Pedro M, Bassi E, Tucci P & Laurindo F (2007). Platelet-derived exosomes from septic shock patients induce myocardial dysfunction. Crit Care 11, R120.
5. Balaj L, Atai NA, Chen W, Mu D, Tannous BA, Breakefield XO, Skog J & Maguire CA (2015). Heparin affinity purification of extracellular vesicles. Sci Rep 5, 10266.
6. Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, Ponimaskin E, Schmiedl A, Yin X, Mayr M, Halder R, Fischer A, Engelhardt S, Wei Y, Schober A, Fiedler J & Thum T (2014). Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest 124, 2136-2146.
7. Bilyy RO, Shkandina T, Tomin A, Munoz LE, Franz S, Antonyuk V, Kit YY, Zirngibl M, Furnrohr BG, Janko C, Lauber K, Schiller M, Schett G, Stoika RS & Herrmann M (2012). Macrophages discriminate glycosylation patterns of apoptotic cell-derived microparticles. J Biol Chem 287, 496-503.
8. Biró É, Sturk-Maquelin KN, Vogel GMT, Meuleman DG, Smit MJ, Hack CE, Sturk A & Nieuwland R (2003). Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 1, 2561-2568.
9. Böing AN, van der Pol E, Grootemaat AE, Coumans FAW, Sturk A & Nieuwland R (2014). Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles 3, doi: 10.3402/jev.v3.23430.
10. Boon RA & Horrevoets AJ (2009). Key transcriptional regulators of the vasoprotective effects of shear stress. Hamostaseologie 29, 39-40, 41-33.
11. Brownlee Z, Lynn KD, Thorpe PE & Schroit AJ (2014). A novel "salting-out" procedure for the isolation of tumor-derived exosomes. J Immunol Methods 407, 120-126.
12. Buzás EI, Gyorgy B, Nagy G, Falus A & Gay S (2014). Emerging role of extracellular vesicles in inflammatory diseases. Nat Rev Rheumatol 10, 356-364.
13. Caby MP (2005). Exosomal-like vesicles are present in human blood plasma. Int Immunol 17, 879-887.
14. Carayon K, Chaoui K, Ronzier E, Lazar I, Bertrand-Michel J, Roques V, Balor S, Terce F, Lopez A, Salome L & Joly E (2011). Proteolipidic composition of exosomes changes during reticulocyte maturation. J Biol Chem 286, 34426-34439.
15. Chen C, Skog J, Hsu C-H, Lessard RT, Balaj L, Wurdinger T, Carter BS, Breakefield XO, Toner M & Irimia D (2010). Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 10, 505-511.
16. Chen L, Wang Y, Pan Y, Zhang L, Shen C, Qin G, Ashraf M, Weintraub N, Ma G & Tang Y (2013). Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury. Biochem Biophys Res Commun 431, 566-571.
17. Choi D-S, Kim D-K, Kim Y-K & Gho YS (2013). Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 13, 1554-1571.
18. Crescitelli R, Lässer C, Szabó TG, Kittel A, Eldh M, Dianzani I, Buzás EI & Lötvall J (2013). Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2, doi: 10.3402/jev.v2i0.20677.
19. Davies RT, Kim J, Jang SC, Choi E-J, Gho YS & Park J (2012). Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip 12, 5202.
20. Dhalla NS, Temsah RM & Netticadan T (2000). Role of oxidative stress in cardiovascular diseases. J Hypertens 18, 655-673.
21. Escrevente C, Grammel N, Kandzia S, Zeiser J, Tranfield EM, Conradt HS & Costa J (2013). Sialoglycoproteins and N-glycans from secreted exosomes of ovarian carcinoma cells. PLoS One 8, e78631.
22. Feng Y, Huang W, Wani M, Yu X & Ashraf M (2014). Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One 9, e88685.
23. Gambim M, de Oliveira do Carmo A, Marti L, Veríssimo-Filho S, Lopes L & Janiszewski M (2007). Platelet-derived exosomes induce endothelial cell apoptosis through peroxynitrite generation: experimental evidence for a novel mechanism of septic vascular dysfunction. Crit Care 11, R107.
24. Gardiner C, Ferreira YJ, Dragovic RA, Redman CWG & Sargent IL (2013). Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles 2, doi: 10.3402/jev.v2i0.
25. Giricz Z, Varga ZV, Baranyai T, Sipos P, Pálóczi K, Kittel Á, Buzás EI & Ferdinandy P (2014). Cardioprotection by remote ischemic preconditioning of the rat heart is mediated by extracellular vesicles. J Mol Cell Cardiol 68, 75-78.
26. György B, Módos K, Pállinger É, Pálóczi K, Pásztói M, Misják P, Deli MA, Sipos Á, Szalai A, Voszka I, Polgár A, Tóth K, Csete M, Nagy G, Gay S, Falus A, Kittel Á & Buzás EI (2010). Detection and isolation of cell-derived microparticles are compromised by protein complexes due to shared biophysical parameters. Blood 117, e39-e48.
27. György B, Szabó T, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger É, Pap E, Kittel Á, Nagy G, Falus A & Buzás E (2011). Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68, 2667-2688.
28. Halkein J, Tabruyn SP, Ricke-Hoch M, Haghikia A, Nguyen N-Q-N, Scherr M, Castermans K, Malvaux L, Lambert V, Thiry M, Sliwa K, Noel A, Martial JA, Hilfiker-Kleiner D & Struman I (2013). MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J Clin Invest 123, 2143-2154.
29. He M, Crow J, Roth M, Zeng Y & Godwin AK (2014). Integrated immunoisolation and protein analysis of circulating exosomes using microfluidic technology. Lab Chip 14, 3773.
30. Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJG, Zeiher AM, Scheffer MP, Frangakis AS, Yin X, Mayr M, Braun T, Urbich C, Boon RA & Dimmeler S (2012). Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 14, 249-256.
31. Hilfiker-Kleiner D, Kaminski K, Podewski E, Bonda T, Schaefer A, Sliwa K, Forster O, Quint A, Landmesser U, Doerries C, Luchtefeld M, Poli V, Schneider MD, Balligand J-L, Desjardins F, Ansari A, Struman I, Nguyen NQN, Zschemisch NH, Klein G, Heusch G, Schulz R, Hilfiker A & Drexler H (2007). A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 128, 589-600.
32. Nolte-'t Hoen EN, van der Vlist EJ, Aalberts M, Mertens HCH, Bosch BJ, Bartelink W, Mastrobattista E, van Gaal EVB, Stoorvogel W, Arkesteijn GJA & Wauben MHM (2012). Quantitative and qualitative flow cytometric analysis of nanosized cell-derived membrane vesicles. Nanomedicine 8, 712-720.
33. Hong B, Cho J-H, Kim H, Choi E-J, Rho S, Kim J, Kim J, Choi D-S, Kim Y-K, Hwang D & Gho Y (2009). Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genom 10, 556.
34. Hong CS, Muller L, Whiteside TL & Boyiadzis M (2014). Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia. Front Immunol 5, 160.
35. Ibrahim Ahmed G-E, Cheng K & Marbán E (2014). Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Rep 2, 606-619.
36. Im H, Shao H, Park YI, Peterson VM, Castro CM, Weissleder R & Lee H (2014). Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat Biotechnol 32, 490-495.
37. Janiszewski M, do Carmo AO, Pedro MA, Silva E, Knobel E & Laurindo FRM (2004). Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: A novel vascular redox pathway. Crit Care Med 32, 818-825.
38. Jansen F, Yang X, Hoelscher M, Cattelan A, Schmitz T, Proebsting S, Wenzel D, Vosen S, Franklin BS, Fleischmann BK, Nickenig G & Werner N (2013). Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 128, 2026-2038.
39. Jansen F, Yang X, Proebsting S, Hoelscher M, Przybilla D, Baumann K, Schmitz T, Dolf A, Endl E, Franklin BS, Sinning JM, Vasa-Nicotera M, Nickenig G & Werner N (2014). MicroRNA expression in circulating microvesicles predicts cardiovascular events in patients with coronary artery disease. J Am Heart Assoc 3, e001249.
40. Jeanneteau J, Hibert P, Martinez MC, Tual-Chalot S, Tamareille S, Furber A, Andriantsitohaina R & Prunier F (2012). Microparticle release in remote ischemic conditioning mechanism. Am J Physiol Heart Circ Physiol 303, H871-H877.
41. Kanwar SS, Dunlay CJ, Simeone DM & Nagrath S (2014). Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 14, 1891.
42. Kawamoto A, Iwasaki H, Kusano K, Murayama T, Oyamada A, Silver M, Hulbert C, Gavin M, Hanley A, Ma H, Kearney M, Zak V, Asahara T & Losordo DW (2006). CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation 114, 2163-2169.
43. Keerthikumar S, Gangoda L, Liem M, Fonseka P, Atukorala I, Ozcitti C, Mechler A, Adda CG, Ang C-S & Mathivanan S (2015). Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget 6, 15375-15396.
44. Kim G, Yoo CE, Kim M, Kang HJ, Park D, Lee M & Huh N (2012). Noble polymeric surface conjugated with zwitterionic moieties and antibodies for the isolation of exosomes from human serum. Bioconjug Chem 23, 2114-2120.
45. Lai RC, Arslan F, Lee MM, Sze NSK, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM, Pasterkamp G, de Kleijn DPV & Lim SK (2010). Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 4, 214-222.
46. Lee C, Mitsialis SA, Aslam M, Vitali SH, Vergadi E, Konstantinou G, Sdrimas K, Fernandez-Gonzalez A & Kourembanas S (2012). Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 126, 2601-2611.
47. Li X, Li J-J, Yang J-Y, Wang D-S, Zhao W, Song W-J, Li W-M, Wang J-F, Han W, Zhang Z-C, Yu Y, Cao D-Y & Dou K-F (2012). Tolerance induction by exosomes from immature dendritic cells and rapamycin in a mouse cardiac allograft model. PLoS One 7, e44045.
48. Llorente A, Skotland T, Sylvänne T, Kauhanen D, Róg T, Orłowski A, Vattulainen I, Ekroos K & Sandvig K (2013). Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta 1831, 1302-1309.
49. Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, Amrani D, Ewenstein BM, Riedel N, Story K, Barker K, Povsic TJ, Harrington RA & Schatz RA (2011). Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ Res 109, 428-436.
50. Lötvall J, Hill AF, Hochberg F, Buzás EI, Di Vizio D, Gardiner C, Song Gho Y, Kurochkin IV, Mathivanan S, Quesenberry P, Sahoo S, Tahara H, Wauben MH, Witwer KW & Théry C (2014). Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles 3, doi: 10.3402/jev.v3.26913.
51. Lvovich V, Srikanthan S & Silverstein RL (2010). A novel broadband impedance method for detection of cell-derived microparticles. Biosens Bioelectron 26, 444-451.
52. Maas SLN, De Vrij J & Broekman MLD (2014). Quantification and size-profiling of extracellular vesicles using tunable resistive pulse sensing. J Vis Exp, e51623.
53. Marzesco AM, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D & Huttner WB (2005). Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118, 2849-2858.
54. Mezentsev A, Merks RMH, O'Riordan E, Chen J, Mendelev N, Goligorsky MS & Brodsky SV (2005). Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol 289, H1106-H1114.
55. Musante L, Saraswat M, Ravida A, Byrne B & Holthofer H (2012). Recovery of urinary nanovesicles from ultracentrifugation supernatants. Nephrol Dial Transplant 28, 1425-1433.
56. Ogawa Y, Kanai-Azuma M, Akimoto Y, Kawakami H & Yanoshita R (2008). Exosome-like vesicles with dipeptidyl peptidase IV in human saliva. Biol Pharm Bull 31, 1059-1062.
57. Oh S, Kang D, Ahn SM, Simpson RJ, Lee BH & Moon MH (2007). Miniaturized asymmetrical flow field-flow fractionation: application to biological vesicles. J Sep Sci 30, 1082-1087.
58. Osteikoetxea X, Balogh A, Szabó-Taylor K, Németh A, Szabó TG, Pálóczi K, Sódar B, Kittel Á, György B, Pállinger É, Matkó J & Buzás EI (2015a). Improved characterization of EV preparations based on protein to lipid ratio and lipid properties. PLoS One 10, e0121184.
59. Osteikoetxea X, Sódar B, Németh A, Szabó-Taylor K, Pálóczi K, Vukman KV, Tamási V, Balogh A, Kittel Á, Pállinger É & Buzás EI (2015b). Differential detergent sensitivity of extracellular vesicle subpopulations. Org Biomol Chem 13, 9775-9782.
60. Pallet N, Sirois I, Bell C, Hanafi L-A, Hamelin K, Dieudé M, Rondeau C, Thibault P, Desjardins M & Hebert M-J (2013). A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 13, 1108-1120.
61. Patko D, Gyorgy B, Nemeth A, Szabó-Taylor KE, Kittel A, Buzas EI & Horvath R (2013). Label-free optical monitoring of surface adhesion of extracellular vesicles by grating coupled interferometry. Sens Actuators B Chem 188, 697-701.
62. Pêche H, Heslan M, Usal C, Amigorena S & Cuturi MC (2003). Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection1. Transplantation 76, 1503-1510.
63. Pêche H, Renaudin K, Beriou G, Merieau E, Amigorena S & Cuturi MC (2006). Induction of tolerance by exosomes and short-term immunosuppression in a fully MHC-mismatched rat cardiac allograft model. Am J Transplant 6, 1541-1550.
64. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ & Geuze HJ (1996). B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183, 1161-1172.
65. Rupert DLM, Lässer C, Eldh M, Block S, Zhdanov VP, Lotvall JO, Bally M & Höök F (2014). Determination of exosome concentration in solution using surface plasmon resonance spectroscopy. Anal Chem 86, 5929-5936.
66. Sahoo S, Klychko E, Thorne T, Misener S, Schultz KM, Millay M, Ito A, Liu T, Kamide C, Agrawal H, Perlman H, Qin G, Kishore R & Losordo DW (2011). Exosomes from human CD34+ stem cells mediate their proangiogenic paracrine activity. Circ Res 109, 724-728.
67. Sitar S, Kejžar A, Pahovnik D, Kogej K, Tušek-Žnidarič M, Lenassi M & Žagar E (2015). Size characterization and quantification of exosomes by asymmetrical-flow field-flow fractionation. Anal Chem 87, 9225-9233.
68. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Curry WT, Carter BS, Krichevsky AM & Breakefield XO (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10, 1470-1476.
69. Sokolova V, Ludwig A-K, Hornung S, Rotan O, Horn PA, Epple M & Giebel B (2011). Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf B Biointerfaces 87, 146-150.
70. Song J, Chen X, Wang M, Xing Y, Zheng Z & Hu S (2014). Cardiac endothelial cell-derived exosomes induce specific regulatory B cells. Sci Rep 4, 7583.
71. Szabó GT, Tarr B, Pálóczi K, Éder K, Lajkó E, Kittel Á, Tóth S, György B, Pásztói M, Németh A, Osteikoetxea X, Pállinger É, Falus A, Szabó-Taylor K & Buzás EI (2014). Critical role of extracellular vesicles in modulating the cellular effects of cytokines. Cell Mol Life Sci 71, 4055-4067.
72. Tatischeff I, Larquet E, Falcón-Pérez JM, Turpin P-Y & Kruglik SG (2012). Fast characterisation of cell-derived extracellular vesicles by nanoparticles tracking analysis, cryo-electron microscopy, and Raman tweezers microspectroscopy. J Extracell Vesicles 1, doi: 10.3402/jev.v1i0.19179.
73. Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J, Williams C, Rodriguez-Barrueco R, Silva JM, Zhang W, Hearn S, Elemento O, Paknejad N, Manova-Todorova K, Welte K, Bromberg J, Peinado H & Lyden D (2014). Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res 24, 766-769.
74. Théry C (2011). Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3, 15.
75. Théry C, Amigorena S, Raposo G & Clayton A (2001a). Isolation and characterization of exosomes from cell culture supernatants and biological fluids Curr Protoc Cell Biol Chapter 3, Unit 3.22.
76. Théry C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J & Amigorena S (2001b). Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166, 7309-7318.
77. Théry C, Ostrowski M & Segura E (2009). Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9, 581-593.
78. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B & Simons M (2008). Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247.
79. Tsiantoulas D, Perkmann T, Afonyushkin T, Mangold A, Prohaska TA, Papac-Milicevic N, Millischer V, Bartel C, Hörkkö S, Boulanger CM, Tsimikas S, Fischer MB, Witztum JL, Lang IM & Binder CJ (2014). Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies. J Lipid Res 56, 440-448.
80. Tsutsui H, Kinugawa S & Matsushima S (2011). Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 301, H2181-H2190.
81. Turiák L, Misják P, Szabó TG, Aradi B, Pálóczi K, Ozohanics O, Drahos L, Kittel Á, Falus A, Buzás EI & Vékey K (2011). Proteomic characterization of thymocyte-derived microvesicles and apoptotic bodies in BALB/c mice. J Proteom 74, 2025-2033.
82. Vaidyanathan R, Naghibosadat M, Rauf S, Korbie D, Carrascosa LG, Shiddiky MJA & Trau M (2014). Detecting exosomes specifically: a multiplexed device based on alternating current electrohydrodynamic induced nanoshearing. Anal Chem 86, 11125-11132.
83. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ & Lötvall JO (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659.
84. van der Pol E, Coumans FAW, Grootemaat AE, Gardiner C, Sargent IL, Harrison P, Sturk A, van Leeuwen TG & Nieuwland R (2014). Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 12, 1182-1192.
85. van der Vlist EJ, Nolte-'t Hoen ENM, Stoorvogel W, Arkesteijn GJA & Wauben MHM (2012). Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc 7, 1311-1326.
86. Van Deun J, Mestdagh P, Sormunen R, Cocquyt V, Vermaelen K, Vandesompele J, Bracke M, De Wever O & Hendrix A (2014). The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles 3, doi: 10.3402/jev.v3.24858.
87. Wahlgren J, Karlson TDL, Glader P, Telemo E & Valadi H (2012). Activated human T cells secrete exosomes that participate in IL-2 mediated immune response signaling. PLoS One 7, e49723.
88. Waldenström A, Gennebäck N, Hellman U & Ronquist G (2012). Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One 7, e34653.
89. Wang X, Huang W, Liu G, Cai W, Millard RW, Wang Y, Chang J, Peng T & Fan G-C (2014). Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol 74, 139-150.
90. Wang Z, Wu H-j, Fine D, Schmulen J, Hu Y, Godin B, Zhang JXJ & Liu X (2013). Ciliated micropillars for the microfluidic-based isolation of nanoscale lipid vesicles. Lab Chip 13, 2879.
91. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, Nolte-'t Hoen EN, Piper MG, Sivaraman S, Skog J, Thery C, Wauben MH & Hochberg F (2013). Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2, doi: 10.3402/jev.v2i0.20360.
92. Wubbolts R, Leckie RS, Veenhuizen PTM, Schwarzmann G, Mobius W, Hoernschemeyer J, Slot JW, Geuze HJ & Stoorvogel W (2003). Proteomic and biochemical analyses of human B cell-derived exosomes: potential implications for their function and multivesicular body formation. J Biol Chem 278, 10963-10972.
93. Yamaguchi T, Izumi Y, Nakamura Y, Yamazaki T, Shiota M, Sano S, Tanaka M, Osada-Oka M, Shimada K, Miura K, Yoshiyama M & Iwao H (2015). Repeated remote ischemic conditioning attenuates left ventricular remodeling via exosome-mediated intercellular communication on chronic heart failure after myocardial infarction. Int J Cardiol 178, 239-246.
94. Yáñez-Mó M, Siljander PRM, Andreu Z, Bedina Zavec A, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NHH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers E-M, Laitinen S, Lässer C, Lener T, Ligeti E, Line A, Lipps G, Llorente A, Lötvall J, Manček-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen ENM, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger É, del Portillo HA, Reventós J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, Santarém N, Schallmoser K, Stampe Ostenfeld M, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MHM & De Wever O (2015). Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 4, doi: 10.3402/jev.v4.27066.
95. Yu X, Deng L, Wang D, Li N, Chen X, Cheng X, Yuan J, Gao X, Liao M, Wang M & Liao Y (2012). Mechanism of TNF-α autocrine effects in hypoxic cardiomyocytes: Initiated by hypoxia inducible factor 1α, presented by exosomes. J Mol Cell Cardiol 53, 848-857.
96. Yuana Y, Oosterkamp TH, Bahatyrova S, Ashcroft B, Garcia Rodriguez P, Bertina RM & Osanto S (2010). Atomic force microscopy: a novel approach to the detection of nanosized blood microparticles. J Thromb Haemost 8, 315-323.
97. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Koppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A & Weber C (2009). Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2, ra81-ra81.
98. Zonneveld MI, Brisson AR, van Herwijnen MJC, Tan S, van de Lest CHA, Redegeld FA, Garssen J, Wauben MHM & Nolte-'t Hoen ENM (2014). Recovery of extracellular vesicles from human breast milk is influenced by sample collection and vesicle isolation procedures. J Extracell Vesicles 3, doi: 10.3402/jev.v3.24215.