12,717
Views
206
CrossRef citations to date
0
Altmetric
Research Article

Comparison of small extracellular vesicles isolated from plasma by ultracentrifugation or size-exclusion chromatography: yield, purity and functional potential

ORCID Icon, & ORCID Icon
Article: 1560809 | Received 18 Jun 2018, Accepted 06 Dec 2018, Published online: 28 Dec 2018

References

  • Lawson C, Vicencio JM, Yellon DM, et al. Microvesicles and exosomes: new players in metabolic and cardiovascular disease. J Endocrinol. 2016;228:R57–R71.
  • van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19:213–18.
  • Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113:E968–E77.
  • Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983;33:967–978.
  • 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.
  • Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006; Chapter3:Unit 3.22. DOI:10.1002/0471143030.cb0322s30
  • Davidson SM, Takov K, Yellon DM. Exosomes and cardiovascular protection. Cardiovasc Drugs Ther. 2017;31:77–86.
  • Rodrigues ML, Nimrichter L, Oliveira DL, et al. Vesicular trans-cell wall transport in fungi: a mechanism for the delivery of virulence-associated macromolecules? Lipid Insights. 2008;2:27–40.
  • Guescini M, Genedani S, Stocchi V, et al. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J Neural Transm. 2010;117:1–4.
  • Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180.
  • Waldenström A, Gennebäck N, Hellman U, et al. Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One. 2012;7:e34653.
  • Thakur BK, Zhang H, Becker A, et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24:766–769.
  • Quinn JF, Patel T, Wong D, et al. Extracellular RNAs: development as biomarkers of human disease. J Extracell Vesicles. 2015;4:27495.
  • Vicencio JM, Yellon DM, Sivaraman V, et al. Plasma exosomes protect the myocardium from ischemia-reperfusion injury. J Am Coll Cardiol. 2015;65:1525–1536.
  • Davidson SM, Riquelme JA, Takov K, et al. Cardioprotection mediated by exosomes is impaired in the setting of type II diabetes but can be rescued by the use of non-diabetic exosomes in vitro. J Cell Mol Med. 2018;22:141–151.
  • Davidson SM, Yellon DM. Exosomes and cardioprotection – A critical analysis. Mol Aspects Med. 2017;1–11. DOI:10.1016/j.mam.2017.11.004
  • Cavallari C, Ranghino A, Tapparo M, et al. Serum-derived extracellular vesicles (EVs) impact on vascular remodeling and prevent muscle damage in acute hind limb ischemia. Sci Rep. 2017;7:8180.
  • Jia L, Zhou X, Huang X, et al. Maternal and umbilical cord serum-derived exosomes enhance endothelial cell proliferation and migration. FASEB J. 2018;fj201701337RR. DOI:10.1096/fj.201701337RR
  • Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC, et al. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation. 1997;96:3534–3541.
  • Lipets E, Vlasova O, Urnova E, et al. Circulating contact-pathway-activating microparticles together with factors IXa and XIa induce spontaneous clotting in plasma of hematology and cardiologic patients. PLoS One. 2014;9:e87692.
  • Welton JL, Webber JP, Botos L, et al. Ready-made chromatography columns for extracellular vesicle isolation from plasma. J Extracell Vesicles. 2015;4:27269.
  • Webber J, Clayton A. How pure are your vesicles? J Extracell vesicles. 2013;2:1–6.
  • Baranyai T, Herczeg K, Onódi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. PLoS One. 2015;10:e0145686.
  • Sódar BW, Á K, Pálóczi K, et al. Low-density lipoprotein mimics blood plasma-derived exosomes and microvesicles during isolation and detection. Sci Rep. 2016;6:24316.
  • Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014;3:1–14.
  • Witwer KW, Buzás EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:1–25.
  • Yuana Y, Levels J, Grootemaat A, et al. Co-isolation of extracellular vesicles and high-density lipoproteins using density gradient ultracentrifugation. J Extracell Vesicles. 2014;3:1–5.
  • Simonsen JB. What are we looking at? Extracellular vesicles, lipoproteins, or both? Circ Res. 2017;121:920–922.
  • Zhang Z, Wang C, Li T, et al. Comparison of ultracentrifugation and density gradient separation methods for isolating Tca8113 human tongue cancer cell line-derived exosomes. Oncol Lett. 2014;8:1701–1706.
  • Nordin JZ, Lee Y, Vader P, et al. Ultrafiltration with size-exclusion liquid chromatography for high yield isolation of extracellular vesicles preserving intact biophysical and functional properties. Nanomedicine. 2015;11:879–883.
  • Stranska R, Gysbrechts L, Wouters J, et al. Comparison of membrane affinity-based method with size-exclusion chromatography for isolation of exosome-like vesicles from human plasma. J Transl Med. 2018;16:1.
  • Mol EA, Goumans M-J, Doevendans PA, et al. Higher functionality of extracellular vesicles isolated using size-exclusion chromatography compared to ultracentrifugation. Nanomedicine. 2017;13:2061–2065.
  • de Menezes-Neto A, Mjf S, Lozano-Ramos I, et al. Size-exclusion chromatography as a stand-alone methodology identifies novel markers in mass spectrometry analyses of plasma-derived vesicles from healthy individuals. J Extracell Vesicles. 2015;4:27378.
  • Gardiner C, Di Vizio D, Sahoo S, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles. 2016;5:32945.
  • Böing AN, van der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014;3:1–11.
  • Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4:27031.
  • Takov K, Yellon DM, Davidson SM. Confounding factors in vesicle uptake studies using fluorescent lipophilic membrane dyes. J Extracell Vesicles. 2017;6:1388731.
  • Karimi N, Cvjetkovic A, Jang SC, et al. Detailed analysis of the plasma extracellular vesicle proteome after separation from lipoproteins. Cell Mol Life Sci. 2018;1–14. DOI:10.1007/s00018-018-2773-4
  • Todorova D, Simoncini S, Lacroix R, et al. Extracellular vesicles in angiogenesis. Circ. Res. 2017;120:1658–1673.
  • Gardiner C, Ferreira YJ, Dragovic RA, et al. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013;2:1–11.
  • Osteikoetxea X, Sódar B, Németh A, et al. Differential detergent sensitivity of extracellular vesicle subpopulations. Org Biomol Chem. 2015;13:9775–9782.
  • Van Deun J, Mestdagh P, Agostinis P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14:228–232.
  • Lacroix R, Judicone C, Mooberry M, et al. Standardization of pre-analytical variables in plasma microparticle determination: results of the international society on thrombosis and haemostasis SSC collaborative workshop. J Thromb Haemost. 2013;11:1190–1193.
  • Zhang H, Freitas D, Kim HS, et al. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol. 2018;20:332–343.
  • Sluijter JPG, Davidson SM, Boulanger CM, et al. Extracellular vesicles in diagnostics and therapy of the ischaemic heart: position paper from the working group on cellular biology of the heart of the European society of Cardiology. Cardiovasc Res. 2018;114:19–34.
  • Salani D, Taraboletti G, Rosanò L, et al. Endothelin-1 induces an angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Am J Pathol. 2000;157:1703–1711.
  • Daher Z, Noël J, Claing A. Endothelin-1 promotes migration of endothelial cells through the activation of ARF6 and the regulation of FAK activity. Cell Signal. 2008;20:2256–2265.
  • Mahley RW, Innerarity TL, Rall SC, et al. Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res. 1984;25:1277–1294.
  • Linares R, Tan S, Gounou C, et al. High-speed centrifugation induces aggregation of extracellular vesicles. J Extracell Vesicles. 2015;4:29509.
  • van der Pol E, Coumans FAW, Grootemaat AE, 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.
  • van der Pol E, Böing AN, Gool EL, et al. Recent developments in the nomenclature, presence, isolation, detection and clinical impact of extracellular vesicles. J Thromb Haemost. 2016;14:48–56.
  • Coumans FAW, Brisson AR, Buzas EI, et al. Methodological guidelines to study extracellular vesicles. Circ Res. 2017;120:1632–1648.
  • Hoefs JC. Serum protein concentration and portal pressure determine the ascitic fluid protein concentration in patients with chronic liver disease. J Lab Clin Med. 1983;102:260–273.
  • Lowry OH, Hunter TH. The determination of serum protein concentration with a gradient tube. J Biol Chem. 1945;159:465–474.
  • Vergauwen G, Dhondt B, Van Deun J, et al. Confounding factors of ultrafiltration and protein analysis in extracellular vesicle research. Sci Rep. 2017;7:1–12.