Precise analysis of single small extracellular vesicles using flow cytometry.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 Mar 2024
Historique:
received: 22 06 2023
accepted: 23 03 2024
medline: 30 3 2024
pubmed: 30 3 2024
entrez: 30 3 2024
Statut: epublish

Résumé

Methods that enable specific and sensitive quantification of small extracellular vesicles (sEVs) using flow cytometry are still under development. Aggregation or adsorption of antibodies causes sub-nano sized particles or non-specific binding and largely affects the results of flow cytometric analysis of single sEVs. Comparison of control IgG and target-specific IgG is inappropriate because they have different characters. Here, we evaluate four preparation methods for flow cytometry, including ultracentrifugation, density gradient centrifugation, size exclusion chromatography (SEC), and the TIM4-affinity method by using tetraspanin-deficient sEVs. The ultracentrifugation or density gradient centrifugation preparation method has large false-positive rates for tetraspanin staining. Conversely, preparation methods using SEC or the TIM4-affinity method show specific detection of single sEVs, which elucidate the roles of sEV biogenesis regulators in the generation of sEV subpopulations. The methods are also useful for the detection of rare disease-related markers, such as PD-L1. Flow cytometric analysis using SEC or the TIM4-affinity method could accelerate research into sEV biogenesis and the development of sEV-based diagnostics and therapies.

Identifiants

pubmed: 38553534
doi: 10.1038/s41598-024-57974-3
pii: 10.1038/s41598-024-57974-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7465

Subventions

Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : No. 21K07173
Organisme : Core Research for Evolutional Science and Technology
ID : No. JPMJCR18H4

Informations de copyright

© 2024. The Author(s).

Références

Colombo, M., Raposo, G. & Théry, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell. Dev. Biol. 30, 255–289 (2014).
doi: 10.1146/annurev-cellbio-101512-122326 pubmed: 25288114
Wollert, T. & Hurley, J. H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864–869 (2010).
doi: 10.1038/nature08849 pubmed: 20305637 pmcid: 2851844
Baietti, M. F. et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell. Biol. 14, 677–685 (2012).
doi: 10.1038/ncb2502 pubmed: 22660413
Trajkovic, K. et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244–1247 (2008).
doi: 10.1126/science.1153124 pubmed: 18309083
Wei, H. et al. Regulation of exosome production and cargo sorting. Int. J. Biol. Sci. 17, 163–177 (2021).
doi: 10.7150/ijbs.53671 pubmed: 33390841 pmcid: 7757038
Kalluri, R. & LeBleu, V. S. The biology, function, and biomedical applications of exosomes. Science 367, eaau6977 (2020).
doi: 10.1126/science.aau6977 pubmed: 32029601 pmcid: 7717626
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 pubmed: 30949308 pmcid: 6442110
Liu, H. et al. Analysis of extracellular vesicle DNA at the single-vesicle level by nano-flow cytometry. J. Extracell. Vesicle 11, e12206 (2022).
doi: 10.1002/jev2.12206
Tertel, T. et al. HIGH-RESOLUTION imaging flow cytometry reveals impact of incubation temperature on labeling of extracellular vesicles with antibodies. Cytometry 97, 602–609 (2020).
doi: 10.1002/cyto.a.24034 pubmed: 32415810
Théry, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell. Biol. 30, 3–22 (2006).
doi: 10.1002/0471143030.cb0322s30
Raposo, G. et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161–1172 (1996).
doi: 10.1084/jem.183.3.1161 pubmed: 8642258
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
Nakai, W. et al. A novel affinity-based method for the isolation of highly purified extracellular vesicles. Sci. Rep. 6, 33935 (2016).
doi: 10.1038/srep33935 pubmed: 27659060 pmcid: 5034288
Ishisaki, A. et al. Identification and characterization of autocrine-motility-factor-like activity in oral squamous-cell-carcinoma cells. Int. J. Cancer 59, 783–788 (1994).
doi: 10.1002/ijc.2910590613 pubmed: 7989119
Araki, Y. et al. Osteosarcoma-derived small extracellular vesicles enhance tumor metastasis and suppress osteoclastogenesis by miR-146a-5p. Front. Oncol. 11, 667109 (2021).
doi: 10.3389/fonc.2021.667109 pubmed: 34017686 pmcid: 8130824
Welsh, J. A. et al. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J. Extracell. Vesicle 13, e12404 (2024).
doi: 10.1002/jev2.12404
Welsh, J. A. et al. MIFlowCyt-EV: A framework for standardized reporting of extracellular vesicle flow cytometry experiments. J. Extracell. Vesicles 9, 1713526 (2020).
doi: 10.1080/20013078.2020.1713526 pubmed: 32128070 pmcid: 7034442
Yurtsever, A. et al. Structural and mechanical characteristics of exosomes from osteosarcoma cells explored by 3D-atomic force microscopy. Nanoscale 13, 6661–6677 (2021).
doi: 10.1039/D0NR09178B pubmed: 33885545
Sajidah, E. S. et al. Spatiotemporal tracking of small extracellular vesicle nanotopology in response to physicochemical stresses revealed by HS-AFM. J. Extracell. Vesicle 11, 12275 (2022).
doi: 10.1002/jev2.12275
Kim, D. H. et al. Exosomal PD-L1 promotes tumor growth through immune escape in non-small cell lung cancer. Exp. Mol. Med. 51, 1–13 (2019).
pubmed: 31827074 pmcid: 6881327
Poggio, M. et al. Suppression of exosomal PD-L1 induces systemic anti-tumor immunity and memory. Cell 177, 414–427 (2019).
doi: 10.1016/j.cell.2019.02.016 pubmed: 30951669 pmcid: 6499401
Matsumoto, A. et al. Phosphatidylserine-deficient small extracellular vesicle is a major somatic cell-derived sEV subpopulation in blood. iScience 24, 102839 (2021).
doi: 10.1016/j.isci.2021.102839 pubmed: 34368655 pmcid: 8326202
Monypenny, J. et al. ALIX regulates tumor-mediated immunosuppression by controlling EGFR activity and PD-L1 presentation. Cell Rep. 24, 630–641 (2018).
doi: 10.1016/j.celrep.2018.06.066 pubmed: 30021161 pmcid: 6077252
Tian, Y. et al. Quality and efficiency assessment of six extracellular vesicle isolation methods by nano-flow cytometry. J. Extracell. Vesicles 9, 1697028 (2020).
doi: 10.1080/20013078.2019.1697028 pubmed: 31839906

Auteurs

Hisano Kobayashi (H)

Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.
Oral and Maxillofacial Surgery, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.

Takayuki Shiba (T)

Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.
Institute of Science and Engineering, Faculty of Frontier Engineering, Kanazawa University, Kanazawa, Ishikawa, Japan.

Takeshi Yoshida (T)

Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan. t-yoshida@med.kanazawa-u.ac.jp.
WPI Nano Life Science Institute (NanoLSI), Kanazawa University, Kanazawa, Ishikawa, Japan. t-yoshida@med.kanazawa-u.ac.jp.

Dilireba Bolidong (D)

Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.
WPI Nano Life Science Institute (NanoLSI), Kanazawa University, Kanazawa, Ishikawa, Japan.

Koroku Kato (K)

Oral and Maxillofacial Surgery, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.

Yoshiki Sato (Y)

Meiwafosis Co. LTD, Tokyo, Japan.

Mao Mochizuki (M)

Meiwafosis Co. LTD, Tokyo, Japan.

Takafumi Seto (T)

Institute of Science and Engineering, Faculty of Frontier Engineering, Kanazawa University, Kanazawa, Ishikawa, Japan.

Shuichi Kawashiri (S)

Oral and Maxillofacial Surgery, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan.

Rikinari Hanayama (R)

Department of Immunology, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan. rikinari-hanayama@umin.ac.jp.
WPI Nano Life Science Institute (NanoLSI), Kanazawa University, Kanazawa, Ishikawa, Japan. rikinari-hanayama@umin.ac.jp.

Classifications MeSH