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
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

9410

Subventions

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

Auteurs

Nele De Langhe (N)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.
HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent, Belgium.
Department of Internal Medicine and Infectious Diseases, Ghent University Hospital, Ghent, Belgium.

Sofie Van Dorpe (S)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.
Department of Gynecology, Ghent University Hospital, Ghent, Belgium.

Niké Guilbert (N)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.

Amélie Vander Cruyssen (A)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.

Quentin Roux (Q)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.
CRCI²NA, Nantes Université, INSERM, CNRS, Nantes, France.

Sarah Deville (S)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.
Laboratory for Molecular Diagnostics, Department of Clinical Biology, Jessa Hospital, Hasselt, Belgium.

Sándor Dedeyne (S)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.

Philippe Tummers (P)

Department of Gynecology, Ghent University Hospital, Ghent, Belgium.

Hannelore Denys (H)

Cancer Research Institute Ghent, Ghent, Belgium.
Department of Medical Oncology, Ghent University Hospital, Ghent, Belgium.

Linos Vandekerckhove (L)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent, Belgium.
Department of Internal Medicine and Infectious Diseases, Ghent University Hospital, Ghent, Belgium.

Olivier De Wever (O)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Cancer Research Institute Ghent, Ghent, Belgium.

An Hendrix (A)

Laboratory of Experimental Cancer Research, Department of Human Structure and Repair, Ghent University, Ghent, Belgium. an.hendrix@ugent.be.
Cancer Research Institute Ghent, Ghent, Belgium. an.hendrix@ugent.be.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH