Mapping bacterial extracellular vesicle research: insights, best practices and knowledge gaps.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
31 Oct 2024
31 Oct 2024
Historique:
received:
28
04
2024
accepted:
07
10
2024
medline:
1
11
2024
pubmed:
1
11
2024
entrez:
1
11
2024
Statut:
epublish
Résumé
Bacterial extracellular vesicles (BEVs) enable communication between bacteria and their natural habitats, including multicellular organisms such as humans. Consequently, the study of BEVs has rapidly gained attention with recent research raising the prospect of developing BEVs as biomarkers and treatments to manage (mal)functioning of natural habitats. Although diverse technologies are available, the composition of their source, their heterogeneity in biophysical and biochemical features, and their multifaceted cargo composition challenges the analysis of BEVs. To map current practices in BEV research, we analyzed 845 publications released in 2015-2021, reporting 3338 BEV-related experiments. The extracted data are accessible via the publicly available EV-TRACK knowledgebase ( https://evtrack.org/ ). We identify the need for transparent reporting, delineate knowledge gaps, outline available best practices and define areas in need of guidance to ensure advances in BEV research and accelerate BEV applications.
Identifiants
pubmed: 39482295
doi: 10.1038/s41467-024-53279-1
pii: 10.1038/s41467-024-53279-1
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
9410Subventions
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 101045156
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : S000319N
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : S000319N
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : S000319N
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 Marie Skłodowska-Curie Actions (H2020 Excellent Science - Marie Skłodowska-Curie Actions)
ID : 722148
Informations de copyright
© 2024. The Author(s).
Références
Hendrix, A. & De Wever, O. Systemically circulating bacterial extracellular vesicles: origin, fate, and function. Trends Microbiol. 30, 213–216 (2022).
doi: 10.1016/j.tim.2021.12.012
pubmed: 35033427
Hendrix, A. et al. Extracellular vesicle analysis. Nat. Rev. Methods Primers 3, 56 (2023).
Toyofuku, M., Nomura, N. & Eberl, L. Types and origins of bacterial membrane vesicles. Nat. Rev. Microbiol. 17, 13–24 (2019).
doi: 10.1038/s41579-018-0112-2
pubmed: 30397270
Toyofuku, M., Schild, S., Kaparakis-Liaskos, M. & Eberl, L. Composition and functions of bacterial membrane vesicles. Nat. Rev. Microbiol. 21, 415–430 (2023).
doi: 10.1038/s41579-023-00875-5
pubmed: 36932221
Tulkens, J. et al. Increased levels of systemic LPS-positive bacterial extracellular vesicles in patients with intestinal barrier dysfunction. Gut 69, 191–193 (2020).
doi: 10.1136/gutjnl-2018-317726
pubmed: 30518529
Tulkens, J., De Wever, O. & Hendrix, A. Analyzing bacterial extracellular vesicles in human body fluids by orthogonal biophysical separation and biochemical characterization. Nat. Protoc. 15, 40–67 (2020).
doi: 10.1038/s41596-019-0236-5
pubmed: 31776460
Deo, P. et al. Mitochondrial dysfunction caused by outer membrane vesicles from Gram-negative bacteria activates intrinsic apoptosis and inflammation. Nat. Microbiol. 5, 1418–1427 (2020).
doi: 10.1038/s41564-020-0773-2
pubmed: 32807891
Kaparakis-Liaskos, M. & Ferrero, R. L. Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol. 15, 375–387 (2015).
doi: 10.1038/nri3837
pubmed: 25976515
Kim, O. Y. et al. Bacterial outer membrane vesicles suppress tumor by interferon-γ-mediated antitumor response. Nat. Commun. 8, 626 (2017).
Bai, X., Findlow, J. & Borrow, R. Recombinant protein meningococcal serogroup B vaccine combined with outer membrane vesicles. Expert Opin. Biol. Ther. 11, 969–985 (2011).
doi: 10.1517/14712598.2011.585965
pubmed: 21615224
Micoli, F. & MacLennan, C. A. Outer membrane vesicle vaccines. Semin Immunol. 50, 101433 (2020).
doi: 10.1016/j.smim.2020.101433
pubmed: 33309166
Wang, X., Thompson, C. D., Weidenmaier, C. & Lee, J. C. Release of Staphylococcus aureus extracellular vesicles and their application as a vaccine platform. Nat. Commun. 9, 1379 (2018).
doi: 10.1038/s41467-018-03847-z
pubmed: 29643357
pmcid: 5895597
Liu, H. et al. Bacterial extracellular vesicles-based therapeutic strategies for bone and soft tissue tumors therapy. Theranostics 12, 6576–6594 (2022).
doi: 10.7150/thno.78034
pubmed: 36185613
pmcid: 9516228
Liu, H. et al. Bacterial extracellular vesicles as bioactive nanocarriers for drug delivery: advances and perspectives. Bioactive Mater. 14, 169–181 (2022).
Biller, S. J. et al. Bacterial vesicles in marine ecosystems. Science 343, 183–186 (2014).
doi: 10.1126/science.1243457
pubmed: 24408433
Ñahui Palomino, R. A. et al. Extracellular vesicles from symbiotic vaginal lactobacilli inhibit HIV-1 infection of human tissues. Nat. Commun. 10, 5656 (2019).
doi: 10.1038/s41467-019-13468-9
pubmed: 31827089
pmcid: 6906448
Welsh, J. A. et al. Minimal information for studies of extracellular vesicles (MISEV2023): from basic to advanced approaches. J. Extracell. Vesicles 13, e12404 (2024).
Thery, C. et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018). J. Extracell. Vesicles 7, 1535750 (2018).
doi: 10.1080/20013078.2018.1535750
pubmed: 30637094
pmcid: 6322352
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
pubmed: 28245209
De Wever, O. & Hendrix, A. A supporting ecosystem to mature extracellular vesicles into clinical application. EMBO J. 38, e101412 (2019).
Arab, T. et al. Characterization of extracellular vesicles and synthetic nanoparticles with four orthogonal single-particle analysis platforms. J. Extracell. Vesicles 10, e12079 (2021).
Ruiz, N. & Silhavy, T. J. How Escherichia coli became the flagship bacterium of molecular biology. J. Bacteriol. 204, e00230-22 (2022).
Connon, S. A. & Giovannoni, S. J. High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl. Environ. Microbiol. 68, 3878–3885 (2002).
doi: 10.1128/AEM.68.8.3878-3885.2002
pubmed: 12147485
pmcid: 124033
Staley, J. T. & Konopka, A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39, 321–346 (1985).
doi: 10.1146/annurev.mi.39.100185.001541
pubmed: 3904603
Jean-Christophe, L. et al. The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin. Microbiol. Rev. 28, 237–264 (2015).
doi: 10.1128/CMR.00014-14
Epstein, S. S. The phenomenon of microbial uncultivability. Curr. Opin. Microbiol. 16, 636–642 (2013).
doi: 10.1016/j.mib.2013.08.003
pubmed: 24011825
Gelibter, S. et al. The impact of storage on extracellular vesicles: a systematic study. J. Extracell. Vesicles 11, e12162 (2022).
Pathirana, R. D. & Kaparakis-Liaskos, M. Bacterial membrane vesicles: Biogenesis, immune regulation and pathogenesis. Cell. Microbiol. 18, 1518–1524 (2016).
Chronopoulos, A. & Kalluri, R. Emerging role of bacterial extracellular vesicles in cancer. Oncogene 39, 6951–6960 (2020).
Shen, Y. et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12, 509–520 (2012).
doi: 10.1016/j.chom.2012.08.004
pubmed: 22999859
pmcid: 3895402
Brown, L., Wolf, J. M., Prados-Rosales, R. & Casadevall, A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol. 13, 620–630 (2015).
Ellis, T. N. & Kuehn, M. J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74, 81–94 (2010).
doi: 10.1128/MMBR.00031-09
pubmed: 20197500
pmcid: 2832350
Schwechheimer, C. & Kuehn, M. J. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13, 605–619 (2015).
Schoch, C. L. et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database 2020, baaa062 (2020).
doi: 10.1093/database/baaa062
pubmed: 32761142
pmcid: 7408187