The generation and use of recombinant extracellular vesicles as biological reference material.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
23 07 2019
23 07 2019
Historique:
received:
30
11
2018
accepted:
26
06
2019
entrez:
25
7
2019
pubmed:
25
7
2019
medline:
6
2
2020
Statut:
epublish
Résumé
Recent years have seen an increase of extracellular vesicle (EV) research geared towards biological understanding, diagnostics and therapy. However, EV data interpretation remains challenging owing to complexity of biofluids and technical variation introduced during sample preparation and analysis. To understand and mitigate these limitations, we generated trackable recombinant EV (rEV) as a biological reference material. Employing complementary characterization methods, we demonstrate that rEV are stable and bear physical and biochemical traits characteristic of sample EV. Furthermore, rEV can be quantified using fluorescence-, RNA- and protein-based technologies available in routine laboratories. Spiking rEV in biofluids allows recovery efficiencies of commonly implemented EV separation methods to be identified, intra-method and inter-user variability induced by sample handling to be defined, and to normalize and improve sensitivity of EV enumerations. We anticipate that rEV will aid EV-based sample preparation and analysis, data normalization, method development and instrument calibration in various research and biomedical applications.
Identifiants
pubmed: 31337761
doi: 10.1038/s41467-019-11182-0
pii: 10.1038/s41467-019-11182-0
pmc: PMC6650486
doi:
Substances chimiques
Biomarkers
0
Culture Media, Conditioned
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3288Références
Van Niel, G., D’Angelo, G. & Raposo, G. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19, 213–228 (2018).
doi: 10.1038/nrm.2017.125
Maas, S. L. N., Breakefield, X. O. & Weaver, A. M. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 27, 172–188 (2017).
doi: 10.1016/j.tcb.2016.11.003
Kalluri, R. The biology and function of exosomes in cancer. J. Clin. Invest. 126, 1208–1215 (2016).
doi: 10.1172/JCI81135
Van Deun, J. et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat. Methods 14, 228–232 (2017).
doi: 10.1038/nmeth.4185
Théry, C. et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 7, 1535750 (2018).
doi: 10.1080/20013078.2018.1535750
Witwer, K. W. et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles 2, 20360 (2013).
doi: 10.3402/jev.v2i0.20360
Valkonen, S. et al. Biological reference materials for extracellular vesicle studies. Eur. J. Pharm. Sci. 98, 4–16 (2017).
doi: 10.1016/j.ejps.2016.09.008
Van Der Pol, E., Coumans, F. A. W., Sturk, A., Nieuwland, R. & Van Leeuwen, T. G. Refractive index determination of nanoparticles in suspension using nanoparticle tracking analysis. Nano Lett. 14, 6195–6201 (2014).
doi: 10.1021/nl503371p
Gardiner, C., Ferreira, Y. J., Dragovic, R. A., Redman, C. W. G. & Sargent, I. L. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J. of Extracell. Vesicles 2, 19671 (2013).
Varga, Z. et al. Hollow organosilica beads as reference particles for optical detection of extracellular vesicles. J. Thromb. Haemost. 16, 1646–1655 (2018).
doi: 10.1111/jth.14193
Lozano-Andrés, E. et al. Tetraspanin-decorated extracellular vesicle-mimetics as a novel adaptable reference material. J. Extracell. Vesicles 8, 1573052 (2019).
doi: 10.1080/20013078.2019.1573052
Görgens, A. et al. Optimisation of imaging flow cytometry for the analysis of single extracellular vesicles by using fluorescence-tagged vesicles as biological reference material. J. Extracell. Vesicles 8, 1587567 (2019).
doi: 10.1080/20013078.2019.1587567
Fujii, K., Hurley, J. H. & Freed, E. O. Beyond Tsg101: the role of Alix in ‘ESCRTing’ HIV-1. Nat. Rev. Microbiol. 5, 912–916 (2007).
doi: 10.1038/nrmicro1790
Gould, S. J., Booth, A. M. & Hildreth, J. E. K. The Trojan exosome hypothesis. Proc. Natl Acad. Sci. USA. 100, 10592–10597 (2003).
doi: 10.1073/pnas.1831413100
Booth, A. M. et al. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923–935 (2006).
doi: 10.1083/jcb.200508014
Tavernier, J. et al. Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat. Commun. 5, 4767 (2014).
doi: 10.1038/ncomms5767
Eyckerman, S. et al. Trapping mammalian protein complexes in viral particles. Nat. Commun. 7, 11416 (2016).
doi: 10.1038/ncomms11416
Dettenhofer, M. & Yu, X. F. Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif in virions. J. Virol. 73, 1460–1467 (1999).
pubmed: 9882352
pmcid: 103971
Böing, A. N. et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J. Extracell. Vesicles 3, 23430 (2014).
doi: 10.3402/jev.v3.23430
Tulkens, J. et al. Increased levels of systemic LPS-positive bacterial extracellular vesicles in patients with intestinal barrier dysfunction. Gut gutjnl-2018-317726 https://gut.bmj.com/content/early/2018/12/15/gutjnl-2018-317726.info (2018).
Théry, C., Clayton, A., Amigorena, S. & Raposo, G. Isolation and characterization of exosomes from cell culture supernatants. Curr. Protoc. Cell Biol. Ch. 3, Unit 3.22 (2006).
De Wever, O. & Hendrix, A. A supporting ecosystem to mature extracellular vesicles into clinical application. EMBO J. 38, e101412 (2019).
Van Deun, J. et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 3, 24858 (2014).
Zhao, C., Ao, Z. & Yao, X. Current advances in virus-like particles as a vaccination approach against HIV infection. Vaccines 4, 2 (2016).
Cashikar, A. G. et al. Structure of cellular ESCRT-III spirals and their relationship to HIV budding. Elife 3, e02184 (2014).
Bieniasz, P. D. Late budding domains and host proteins in enveloped virus release. Virology 344, 55–63 (2006).
doi: 10.1016/j.virol.2005.09.044
Jouvenet, N. et al. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4, e435 (2006).
doi: 10.1371/journal.pbio.0040435
Comas-Garcia, M. et al. Dissection of specific binding of HIV-1 Gag to the ‘packaging signal’ in viral RNA. Elife 6, e27055 (2017).
Rulli, S. J. et al. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J. Virol. 81, 6623–6631 (2007).
doi: 10.1128/JVI.02833-06
Campbell, S. & Alan, R. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 67, 5550–5561 (1999).
Pastuzyn, E. D. et al. The neuronal gene arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell 172, 275–288.e18 (2018).
doi: 10.1016/j.cell.2017.12.024
Chatterjee, D. K., Kaczmarczyk, S. J., Sitaraman, K., Hughes, S. H. & Young, H. A. Protein delivery using engineered virus-like particles. Proc. Natl Acad. Sci. USA 108, 16998–17003 (2011).
doi: 10.1073/pnas.1101874108
Lai, C. P. et al. Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat. Commun. 6, 7029 (2015).
doi: 10.1038/ncomms8029
Hardwick, S. A., Deveson, I. W. & Mercer, T. R. Reference standards for next-generation sequencing. Nat. Rev. Genet. 18, 473–484 (2017).
doi: 10.1038/nrg.2017.44
Plant, A. L., Locascio, L. E., May, W. E. & Gallagher, P. D. Improved reproducibility by assuring confidence in measurements in biomedical research. Nat. Methods 11, 895–898 (2014).
doi: 10.1038/nmeth.3076
Pi, F. et al. Nanoparticle orientation to control RNA loading and ligand display on extracellular vesicles for cancer regression. Nat. Nanotechnol. 13, 82–89 (2018).
doi: 10.1038/s41565-017-0012-z
Onódi, Z. et al. Isolation of high-purity extracellular vesicles by the combination of iodixanol density gradient ultracentrifugation and bind-elute chromatography from blood plasma. Front. Physiol. 9, 1479 (2018).
doi: 10.3389/fphys.2018.01479
Simonsen, J. B. What are we looking at? extracellular vesicles, lipoproteins, or both? Circ. Res. 121, 920–922 (2017).
doi: 10.1161/CIRCRESAHA.117.311767
De Wever, O. et al. Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J. 18, 1016–1018 (2004).
doi: 10.1096/fj.03-1110fje
Vergauwen, G. et al. Confounding factors of ultrafiltration and protein analysis in extracellular vesicle research. Sci. Rep. 7, 2704 (2017).
doi: 10.1038/s41598-017-02599-y
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. 7, 1311–1326 (2012).
doi: 10.1038/nprot.2012.065