Special considerations for studies of extracellular vesicles from parasitic helminths: A community-led roadmap to increase rigour and reproducibility
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
Grantová podpora
NC/P001521/1
National Centre for the Replacement, Refinement and Reduction of Animals in Research - United Kingdom
R01 CA164719
NCI NIH HHS - United States
PubMed
36604533
PubMed Central
PMC9816087
DOI
10.1002/jev2.12298
Knihovny.cz E-zdroje
- Klíčová slova
- EV guidelines, EV reporting, electron microscopy, extracellular vesicles, helminths, parasites,
- MeSH
- cizopasní červi * MeSH
- extracelulární vezikuly * fyziologie MeSH
- lidé MeSH
- reprodukovatelnost výsledků MeSH
- savci MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Over the last decade, research interest in defining how extracellular vesicles (EVs) shape cross-species communication has grown rapidly. Parasitic helminths, worm species found in the phyla Nematoda and Platyhelminthes, are well-recognised manipulators of host immune function and physiology. Emerging evidence supports a role for helminth-derived EVs in these processes and highlights EVs as an important participant in cross-phylum communication. While the mammalian EV field is guided by a community-agreed framework for studying EVs derived from model organisms or cell systems [e.g., Minimal Information for Studies of Extracellular Vesicles (MISEV)], the helminth community requires a supplementary set of principles due to the additional challenges that accompany working with such divergent organisms. These challenges include, but are not limited to, generating sufficient quantities of EVs for descriptive or functional studies, defining pan-helminth EV markers, genetically modifying these organisms, and identifying rigorous methodologies for in vitro and in vivo studies. Here, we outline best practices for those investigating the biology of helminth-derived EVs to complement the MISEV guidelines. We summarise community-agreed standards for studying EVs derived from this broad set of non-model organisms, raise awareness of issues associated with helminth EVs and provide future perspectives for how progress in the field will be achieved.
Department of Biochemical Sciences Faculty of Pharmacy Charles University Prague Czech Republic
Department of Clinical Medicine Aarhus University Aarhus Denmark
Department of Microbiology School of Medicine University of Buenos Aires Buenos Aires Argentina
Department of Parasitology Faculty of Medicine Khon Kaen University Khon Kaen Thailand
Department of Public health and infectious diseases Sapienza University of Rome Rome Italy
ELKH SE Immune Proteogenomics Extracellular Vesicle Research Group Budapest Hungary
Faculty of Science University of South Bohemia České Budějovice Czech Republic
HCEMM SU Extracellular Vesicle Research Group Budapest Hungary
Institute for the Application of Nuclear Energy INEP University of Belgrade Belgrade Serbia
Instituto de Salud Carlos 3 National Center for Microbiology Majadahonda Madrid Spain
Leiden University Medical Center Parasitology Leiden The Netherlands
McGill University Institute of Parasitology Ste Anne de Bellevue Quebec Canada
Medical University of Vienna Institute of Specific Prophylaxis and Tropical Medicine Vienna Austria
Queen's University Belfast School of Biological Sciences Belfast Northern Ireland UK
Swiss Tropical and Public Health Institute Allschwil Switzerland
Universidad de la República Facultad de Medicina Departamento de Genetica Montevideo Uruguay
University of Basel Basel Switzerland
University of Pennsylvania School of Veterinary Medicine Pathobiology Philadelphia Pennsylvania USA
University of Zurich Institute of Parasitology Vetsuisse Faculty Zurich Switzerland
Wellcome Sanger Institute Parasites and Microbes Cambridge UK
Zobrazit více v PubMed
Allen, N. R. , Taylor‐Mew, A. R. , Wilkinson, T. J. , Huws, S. , Phillips, H. , Morphew, R. M. , & Brophy, P. M. (2021). Modulation of rumen microbes through extracellular vesicle released by the rumen fluke calicophoron daubneyi. Frontiers in Cellular and Infection Microbiology, 11, 263. 10.3389/FCIMB.2021.661830/BIBTEX PubMed DOI PMC
Bennett, A. P. S. , De La Torre‐Escudero, E. , Dermott, S. S. E. , Threadgold, L. T. , Hanna, R. E. B. , & Robinson, M. W. (2022). Fasciola hepatica gastrodermal cells selectively release extracellular vesicles via a novel atypical secretory mechanism. International Journal of Molecular Sciences, 23(10), 5525. 10.3390/ijms23105525 PubMed DOI PMC
Bishop, D. G. , & Work, E. (1965). An extracellular glycolipid produced by Escherichia coli grown under lysine‐limiting conditions. Biochemical Journal, 96(2), 567. 10.1042/BJ0960567 PubMed DOI PMC
Blaxter, M. , & Koutsovoulos, G. (2015). The evolution of parasitism in Nematoda. Parasitology, 142(S1), S26–S39. 10.1017/S0031182014000791 PubMed DOI PMC
Borup, A. , Boysen, A. T. , Ridolfi, A. , Brucale, M. , Valle, F. , Paolini, L. , Bergese, P. , & Nejsum, P. (2022). Comparison of separation methods for immunomodulatory extracellular vesicles from helminths. Journal of Extracellular Biology, 1(5), e41. 10.1002/JEX2.41 PubMed DOI PMC
Boysen, A. T. , Whitehead, B. , Stensballe, A. , Carnerup, A. , Nylander, T. , & Nejsum, P. (2020). Fluorescent labeling of helminth extracellular vesicles using an in vivo whole organism approach. Biomedicines, 8(7), 213. 10.3390/BIOMEDICINES8070213 PubMed DOI PMC
Buck, A. H. , Coakley, G. , Simbari, F. , McSorley, H. J. , Quintana, J. F. , Le Bihan, T. , Kumar, S. , Abreu‐Goodger, C. , Lear, M. , Harcus, Y. , Ceroni, A. , Babayan, S. A. , Blaxter, M. , Ivens, A. , & Maizels, R. M. (2014). Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature Communications, 5, 5488. 10.1038/NCOMMS6488 PubMed DOI PMC
Chaiyadet, S. , Sotillo, J. , Krueajampa, W. , Thongsen, S. , Brindley, P. J. , Sripa, B. , Loukas, A. , & Laha, T. (2019). Vaccination of hamsters with opisthorchis viverrini extracellular vesicles and vesicle‐derived recombinant tetraspanins induces antibodies that block vesicle uptake by cholangiocytes and reduce parasite burden after challenge infection. PLoS Neglected Tropical Diseases, 13(5), e0007450. 10.1371/journal.pntd.0007450 PubMed DOI PMC
Chaiyadet, S. , Sotillo, J. , Krueajampa, W. , Thongsen, S. , Smout, M. , Brindley, P. J. , Laha, T. , & Loukas, A. (2022). Silencing of opisthorchis viverrini tetraspanin gene expression results in reduced secretion of extracellular vesicles. Frontiers in Cellular and Infection Microbiology, 12, 75. 10.3389/FCIMB.2022.827521/BIBTEX PubMed DOI PMC
Cheng, Y. , Zeng, Q. , Han, Q. , & Xia, W. (2019). Effect of pH, temperature and freezing‐thawing on quantity changes and cellular uptake of exosomes. Protein and Cell, 10(4), 295–299. 10.1007/S13238-018-0529-4/FIGURES/2 PubMed DOI PMC
Chow, F. W. N. , Koutsovoulos, G. , Ovando‐Vázquez, C. , Neophytou, K. , Bermúdez‐Barrientos, J. R. , Laetsch, D. R. , Robertson, E. , Kumar, S. , Claycomb, J. M. , Blaxter, M. , Abreu‐Goodger, C. , & Buck, A. H. (2019). Secretion of an Argonaute protein by a parasitic nematode and the evolution of its siRNA guides. Nucleic Acids Research, 47(7), 3594–3606. 10.1093/nar/gkz142 PubMed DOI PMC
Coakley, G. , Maizels, R. M. , & Buck, A. H. (2015). Exosomes and other extracellular vesicles: The new communicators in parasite infections. In: Trends in parasitology (pp. 477–489). Trends Parasitol. 10.1016/j.pt.2015.06.009 PubMed DOI PMC
Coakley, G. , McCaskill, J. L. , Borger, J. G. , Simbari, F. , Robertson, E. , Millar, M. , Harcus, Y. , McSorley, H. J. , Maizels, R. M. , & Buck, A. H. (2017). Extracellular vesicles from a helminth parasite suppress macrophage activation and constitute an effective vaccine for protective immunity. Cell Reports, 19(8), 1545–1557. 10.1016/j.celrep.2017.05.001 PubMed DOI PMC
Coghlan, A. , Tyagi, R. , Cotton, J. A. , Holroyd, N. , Rosa, B. A. , Tsai, I. J. , Laetsch, D. R. , Beech, R. N. , Day, T. A. , Hallsworth‐Pepin, K. , Ke, H. M. , Kuo, T. H. , Lee, T. J. , Martin, J. , Maizels, R. M. , Mutowo, P. , Ozersky, P. , Parkinson, J. , Reid, A. J. , … Berriman, M. (2019). Comparative genomics of the major parasitic worms. Nature Genetics, 51(1), 163–174. 10.1038/s41588-018-0262-1 PubMed DOI PMC
Cucher, M. A. , Ancarola, M. E. , & Kamenetzky, L. (2021). The challenging world of extracellular RNAs of helminth parasites. Molecular Immunology, 134, 150–160. 10.1016/J.MOLIMM.2021.03.011 PubMed DOI
Cwiklinski, K. , Dalton, J. P. , Dufresne, P. J. , La Course, J. , Williams, D. J. L. , Hodgkinson, J. , & Paterson, S. (2015). The Fasciola hepatica genome: Gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biology, 16(1), 1–13. 10.1186/S13059-015-0632-2/FIGURES/6 PubMed DOI PMC
Davis, C. N. , Phillips, H. , Tomes, J. J. , Swain, M. T. , Wilkinson, T. J. , Brophy, P. M. , & Morphew, R. M. (2019). The importance of extracellular vesicle purification for downstream analysis: A comparison of differential centrifugation and size exclusion chromatography for helminth pathogens. PLoS Neglected Tropical Diseases, 13(2), e0007191. 10.1371/JOURNAL.PNTD.0007191 PubMed DOI PMC
De, S. N. (1959). Enterotoxicity of bacteria‐free culture‐filtrate of vibrio cholerae. Nature, 183(4674), 1533–1534. 10.1038/1831533a0 PubMed DOI
Drurey, C. , Coakley, G. , & Maizels, R. M. (2020). Extracellular vesicles: New targets for vaccines against helminth parasites. International Journal for Parasitology, 50(9), 623. 10.1016/J.IJPARA.2020.04.011 PubMed DOI PMC
Drurey, C. , & Maizels, R. M. (2021). Helminth extracellular vesicles: Interactions with the host immune system. Molecular Immunology, 137, 124–133. 10.1016/j.molimm.2021.06.017 PubMed DOI PMC
Eichenberger, R. M. , Ryan, S. , Jones, L. , Buitrago, G. , Polster, R. , de Oca, M. M. , Zuvelek, J. , Giacomin, P. R. , Dent, L. A. , Engwerda, C. R. , Field, M. A. , Sotillo, J. , & Loukas, A. (2018a). Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Frontiers in Immunology, 9, 850. 10.3389/fimmu.2018.00850 PubMed DOI PMC
Eichenberger, R. M. , Talukder, M. H. , Field, M. A. , Wangchuk, P. , Giacomin, P. , Loukas, A. , & Sotillo, J. (2018b). Characterization of Trichuris muris secreted proteins and extracellular vesicles provides new insights into host–parasite communication. Journal of Extracellular Vesicles, 7(1), 1428004. 10.1080/20013078.2018.1428004 PubMed DOI PMC
Flynn, R. A. , Pedram, K. , Malaker, S. A. , Batista, P. J. , Smith, B. A. H. , Johnson, A. G. , George, B. M. , Majzoub, K. , Villalta, P. W. , Carette, J. E. , & Bertozzi, C. R. (2021). Small RNAs are modified with N‐glycans and displayed on the surface of living cells. Cell, 184(12), 3109–3124.e22. 10.1016/J.CELL.2021.04.023 PubMed DOI PMC
Galiano, A. , Minguez, M. T. , Sánchez, C. M. , & Marcilla, A. (2020). Isolation and analysis of Fasciola hepatica extracellular vesicles. In: Methods in molecular biology (pp. 37–50). Humana. 10.1007/978-1-0716-0475-5_4 PubMed DOI
Gasan, T. A. , Kuipers, M. E. , Roberts, G. H. , Padalino, G. , Forde‐Thomas, J. E. , Wilson, S. , Wawrzyniak, J. , Tukahebwa, E. M. , Hoffmann, K. F. , & Chalmers, I. W. (2021). Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre‐acetabular glands of invading cercariae. PLoS Neglected Tropical Diseases, 15(11), e0009981. 10.1371/JOURNAL.PNTD.0009981 PubMed DOI PMC
Guidi, A. , Gimmelli, R. , Bresciani, A. , & Ruberti, G. (2020). Luminescence‐based, low‐ and medium‐throughput assays for drug screening in schistosoma mansoni larval stage. Methods in Molecular Biology (Clifton, N.J.), 2151, 219–227. 10.1007/978-1-0716-0635-3_18 PubMed DOI
Hoffmann, K. F. , Hokke, C. H. , Loukas, A. , & Buck, A. H. (2020). Helminth extracellular vesicles: Great balls of wonder. International Journal for Parasitology, 50(9), 621–622. 10.1016/J.IJPARA.2020.07.002 PubMed DOI
Jensen, W. A. (1965). The composition and ultrastructure of the nucellus in cotton. Journal of Ultrasructure Research, 13(1–2), 112–128. 10.1016/S0022-5320(65)80092-2 DOI
Johnstone, R. M. , Adam, M. , Hammond, J. R. , Orr, L. , & Turbide, C. (1987). Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). Journal of Biological Chemistry, 262(19), 9412–9420. 10.1016/S0021-9258(18)48095-7 PubMed DOI
Kim, K. M. , Abdelmohsen, K. , Mustapic, M. , Kapogiannis, D. , & Gorospe, M. (2017). RNA in extracellular vesicles. In: Wiley interdisciplinary reviews: RNA. NIH Public Access. 10.1002/wrna.1413 PubMed DOI PMC
Kuipers, M. E. , Hoen, E. N. M. N.‐‘t , van der Ham, A. J. , Ozir‐Fazalalikhan, A. , Nguyen, D. L. , de Korne, C. M. , Koning, R. I. , Tomes, J. J. , Hoffmann, K. F. , Smits, H. H. , & Hokke, C. H. (2020). DC‐SIGN mediated internalisation of glycosylated extracellular vesicles from Schistosoma mansoni increases activation of monocyte‐derived dendritic cells. Journal of Extracellular Vesicles, 9(1), 1753420. 10.1080/20013078.2020.1753420 PubMed DOI PMC
Kuipers, M. E. , Koning, R. I. , Bos, E. , Hokke, C. H. , Smits, H. H. , & Nolte‐’T Hoen, E. N. M. (2022). Optimized protocol for the isolation of extracellular vesicles from the parasitic worm schistosoma mansoni with improved purity, concentration, and yield. Journal of Immunology Research, 2022, 5473763. 10.1155/2022/5473763 PubMed DOI PMC
Leinonen, R. , Sugawara, H. , & Shumway, M. (2011). The sequence read archive. Nucleic Acids Research, 39, (Database issue), D19. 10.1093/NAR/GKQ1019 PubMed DOI PMC
Malkin, E. Z. , & Bratman, S. V. (2020). Bioactive DNA from extracellular vesicles and particles. In: Cell death and disease. Nature Publishing Group. 10.1038/s41419-020-02803-4 PubMed DOI PMC
Marcilla, A. , Trelis, M. , Cortés, A. , Sotillo, J. , & Cantalapiedra, F. (2012). Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS ONE, 7(9), 45974. 10.1371/journal.pone.0045974 PubMed DOI PMC
Mekonnen, G. , Tedla, B. , Pickering, D. , Becker, L. , Wang, L. , Zhan, B. , Bottazzi, M. , Loukas, A. , Sotillo, J. , & Pearson, M. (2020). Schistosoma haematobium extracellular vesicle proteins confer protection in a heterologous model of schistosomiasis. Vaccines, 8(3), 1–20. 10.3390/VACCINES8030416 PubMed DOI PMC
Mu, Y. , McManus, D. P. , Gordon, C. A. , & Cai, P. (2021). Parasitic helminth‐derived microRNAs and extracellular vesicle cargos as biomarkers for helminthic infections. Frontiers in Cellular and Infection Microbiology, 11, 581. 10.3389/FCIMB.2021.708952/BIBTEX PubMed DOI PMC
Murphy, A. , Cwiklinski, K. , Lalor, R. , O'connell, B. , Robinson, M. W. , Gerlach, J. , Joshi, L. , Kilcoyne, M. , Dalton, J. P. , & O'neill, S. M. (2020). Fasciola hepatica extracellular vesicles isolated from excretory‐secretory products using a gravity flow method modulate dendritic cell phenotype and activity. PLoS Neglected Tropical Diseases, 14(9), 1–25. 10.1371/journal.pntd.0008626 PubMed DOI PMC
Nguyen, L. T. , Zajíčková, M. , Mašátová, E. , Matoušková, P. , & Skálová, L. (2021). The ATP bioluminescence assay: A new application and optimization for viability testing in the parasitic nematode Haemonchus contortus. Veterinary Research, 52(1), 124. 10.1186/S13567-021-00980-4 PubMed DOI PMC
Nizamudeen, Z. A. , Xerri, R. , Parmenter, C. , Suain, K. , Markus, R. , Chakrabarti, L. , & Sottile, V. (2021). Low‐power sonication can alter extracellular vesicle size and properties. Cells, 10(9), 2413. 10.3390/CELLS10092413/S1 PubMed DOI PMC
Nowacki, F. C. , Swain, M. T. , Klychnikov, O. I. , Niazi, U. , Ivens, A. , Quintana, J. F. , Hensbergen, P. J. , Hokke, C. H. , Buck, A. H. , & Hoffmann, K. F. (2015). Protein and small non‐coding RNA‐enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. Journal of Extracellular Vesicles, 4(1), 28665. 10.3402/JEV.V4.28665 PubMed DOI PMC
Osteikoetxea, X. , Balogh, A. , Szabó‐Taylor, K. , Németh, A. , Szabó, T. G. , Pálóczi, K. , Sódar, B. , Kittel, Á. , György, B. , Pállinger, É. , Matkó, J. , & Buzás, E. I. (2015). Improved characterization of EV preparations based on protein to lipid ratio and lipid properties. PLoS ONE, 10(3), e0121184. 10.1371/JOURNAL.PONE.0121184 PubMed DOI PMC
Pathan, M. , Fonseka, P. , Chitti, S. V. , Kang, T. , Sanwlani, R. , Van Deun, J. , Hendrix, A. , & Mathivanan, S. (2019). Vesiclepedia 2019: A compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Research, 47(D1), D516–D519. 10.1093/NAR/GKY1029 PubMed DOI PMC
Peak, E. , Chalmers, I. W. , & Hoffmann, K. F. (2010). Development and validation of a quantitative, high‐throughput, fluorescent‐based bioassay to detect schistosoma viability. PLoS Neglected Tropical Diseases, 4(7), e759. 10.1371/JOURNAL.PNTD.0000759 PubMed DOI PMC
Perez‐Riverol, Y. , Csordas, A. , Bai, J. , Bernal‐Llinares, M. , Hewapathirana, S. , Kundu, D. J. , Inuganti, A. , Griss, J. , Mayer, G. , Eisenacher, M. , Pérez, E. , Uszkoreit, J. , Pfeuffer, J. , Sachsenberg, T. , Yilmaz, Ş. , Tiwary, S. , Cox, J. , Audain, E. , Walzer, M. , … Vizcaíno, J. A. (2019). The PRIDE database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Research, 47(D1), D442–D450. 10.1093/NAR/GKY1106 PubMed DOI PMC
Phumrattanaprapin, W. , Pearson, M. , Pickering, D. , Tedla, B. , Smout, M. , Chaiyadet, S. , Brindley, P. J. , Loukas, A. , & Laha, T. (2021). Monoclonal antibodies targeting an opisthorchis viverrini extracellular vesicle tetraspanin protect hamsters against challenge infection. Vaccines, 9(7), 740. 10.3390/vaccines9070740 PubMed DOI PMC
Ramirez, B. , Bickle, Q. , Yousif, F. , Fakorede, F. , Mouries, M. A. , & Nwaka, S. (2007). Schistosomes: Challenges in compound screening. Expert Opinion on Drug Discovery, 2(s1), S53–61. 10.1517/17460441.2.S1.S53 PubMed DOI
Ramirez, M. I. , & Marcilla, A. (2021). Pathogens and extracellular vesicles: New paths and challenges to understanding and treating diseases. Editorial opinion. Molecular Immunology, 139, 155–156. 10.1016/J.MOLIMM.2021.09.006 PubMed DOI
Raposo, G. , Nijman, H. W. , Stoorvogel, W. , Leijendekker, R. , Harding, C. V. , Melief, C. J. M. , & Geuze, H. J. (1996). B lymphocytes secrete antigen‐presenting vesicles. The Journal of Experimental Medicine, 183(3), 1161. 10.1084/JEM.183.3.1161 PubMed DOI PMC
Ridolfi, A. , Brucale, M. , Montis, C. , Caselli, L. , Paolini, L. , Borup, A. , Boysen, A. T. , Loria, F. , van Herwijnen, M. J. C. , Kleinjan, M. , Nejsum, P. , Zarovni, N. , Wauben, M. H. M. , Berti, D. , Bergese, P. , & Valle, F. (2020). AFM‐based high‐throughput nanomechanical screening of single extracellular vesicles. Analytical Chemistry, 92(15), 10274–10282. 10.1021/ACS.ANALCHEM.9B05716 PubMed DOI
Ryan, S. M. , Eichenberger, R. M. , Ruscher, R. , Giacomin, P. R. , & Loukas, A. (2020). Harnessing helminth‐driven immunoregulation in the search for novel therapeutic modalities. In: PLoS pathogens (p. e1008508). Public Library of Science. 10.1371/journal.ppat.1008508 PubMed DOI PMC
Sánchez‐López, C. , Trelis, M. , Bernal, D. , & Marcilla, A. (2021). Overview of the interaction of helminth extracellular vesicles with the host and their potential functions and biological applications. Molecular Immunology, 134, 228–235. 10.1016/J.MOLIMM.2021.03.020 PubMed DOI
Shears, R. , Bancroft, A. , Hughes, G. , Grencis, R. , & Thornton, D. (2018). Extracellular vesicles induce protective immunity against Trichuris muris. Parasite Immunology, 40(7), e12536. 10.1111/PIM.12536 PubMed DOI PMC
Shelke, G. V. , Lässer, C. , Gho, Y. S. , & Lötvall, J. (2014). Importance of exosome depletion protocols to eliminate functional and RNA‐containing extracellular vesicles from fetal bovine serum. Journal of Extracellular Vesicles, 3. 10.3402/JEV.V3.24783/SUPPL_FILE/ZJEV_A_11815515_SM0001.PDF PubMed DOI PMC
Sotillo, J. , Pearson, M. , Potriquet, J. , Becker, L. , Pickering, D. , Mulvenna, J. , & Loukas, A. (2016). Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates. International Journal for Parasitology, 46(1), 1–5. 10.1016/J.IJPARA.2015.09.002 PubMed DOI
Sotillo, J. , Robinson, M. W. , Kimber, M. J. , Cucher, M. , Ancarola, M. E. , Nejsum, P. , Marcilla, A. , Eichenberger, R. M. , & Tritten, L. (2020). The protein and microRNA cargo of extracellular vesicles from parasitic helminths – current status and research priorities. Int J Parasitol, 50(9), 635–645. 10.1016/j.ijpara.2020.04.010 PubMed DOI
Théry, C. , Witwer, K. W. , Aikawa, E. , Alcaraz, M. J. , Anderson, J. D. , Andriantsitohaina, R. , Antoniou, A. , Arab, T. , Archer, F. , Atkin‐Smith, G. K. , Ayre, D. C. , Bach, J.‐M. , Bachurski, D. , Baharvand, H. , Balaj, L. , Baldacchino, S. , Bauer, N. N. , Baxter, A. A. , Bebawy, M. , … Zuba‐Surma, E. K. (2018). 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. Journal of Extracellular Vesicles, 7(1), 1535750. 10.1080/20013078.2018.1535750 PubMed DOI PMC
de la Torre‐Escudero, E. , Gerlach, J. Q. , Bennett, A. P. S. , Cwiklinski, K. , Jewhurst, H. L. , Huson, K. M. , Joshi, L. , Kilcoyne, M. , O'Neill, S. , Dalton, J. P. , & Robinson, M. W. (2019). Surface molecules of extracellular vesicles secreted by the helminth pathogen Fasciola hepatica direct their internalisation by host cells. PLOS Neglected Tropical Diseases, 13(1), e0007087. 10.1371/JOURNAL.PNTD.0007087 PubMed DOI PMC
Tóth, E. , Turiák, L. , Visnovitz, T. , Cserép, C. , Mázló, A. , Sódar, B. W. , Försönits, A. I. , Petővári, G. , Sebestyén, A. , Komlósi, Z. , Drahos, L. , Kittel, Á. , Nagy, G. , Bácsi, A. , Dénes, Á. , Gho, Y. S. , Szabó‐Taylor, K. , & Buzás, E. I. (2021). Formation of a protein corona on the surface of extracellular vesicles in blood plasma. Journal of Extracellular Vesicles, 10(11), e12140. 10.1002/jev2.12140 PubMed DOI PMC
Trelis, M. , Galiano, A. , Bolado, A. , Toledo, R. , Marcilla, A. , & Bernal, D. (2016). Subcutaneous injection of exosomes reduces symptom severity and mortality induced by Echinostoma caproni infection in BALB/c mice. International Journal for Parasitology, 46(12), 799–808. 10.1016/J.IJPARA.2016.07.003 PubMed DOI
Van Deun, J. , Mestdagh, P. , Agostinis, P. , Akay, Ö. , Anand, S. , Anckaert, J. , Martinez, Z. A. , Baetens, T. , Beghein, E. , Bertier, L. , Berx, G. , Boere, J. , Boukouris, S. , Bremer, M. , Buschmann, D. , Byrd, J. B. , Casert, C. , Cheng, L. , Cmoch, A. , … Hendrix, A. (2017). EV‐TRACK: Transparent reporting and centralizing knowledge in extracellular vesicle research. Nature Methods, 14(3), 228–232. 10.1038/nmeth.4185 PubMed DOI
Viney, M. (2018). The genomic basis of nematode parasitism. In: Briefings in functional genomics. Brief Funct Genomics. 10.1093/BFGP/ELX010 PubMed DOI PMC
Visnovitz, T. , Osteikoetxea, X. , Sódar, B. W. , Mihály, J. , Lőrincz, P. , Vukman, K. V. , Tóth, E. Á. , Koncz, A. , Székács, I. , Horváth, R. , Varga, Z. , & Buzás, E. I. (2019). An improved 96 well plate format lipid quantification assay for standardisation of experiments with extracellular vesicles. Journal of Extracellular Vesicles, 8(1), 1565263. 10.1080/20013078.2019.1565263 PubMed DOI PMC
Watanabe, Y. , Aoki‐Kinoshita, K. F. , Ishihama, Y. , & Okuda, S. (2021). GlycoPOST realizes FAIR principles for glycomics mass spectrometry data. Nucleic Acids Research, 49(D1), D1523–D1528. 10.1093/NAR/GKAA1012 PubMed DOI PMC
Welsh, J. A. , van der Pol, E. , Bettin, B. A. , Carter, D. R. F. , Hendrix, A. , Lenassi, M. , Langlois, M. A. , Llorente, A. , van de Nes, A. S. , Nieuwland, R. , Tang, V. , Wang, L. , Witwer, K. W. , & Jones, J. C. (2020). Towards defining reference materials for measuring extracellular vesicle refractive index, epitope abundance, size and concentration. Journal of Extracellular Vesicles, 9(1), 1816641. 10.1080/20013078.2020.1816641 PubMed DOI PMC
Webber, J. , & Clayton, A. (2013). How pure are your vesicles? J Extracell Vesicles. Journal of Extracellular Vesicles, 2(1), 10.3402/jev.v2i0.19861 PubMed DOI PMC
White, R. , Kumar, S. , Chow, F. , Robertson, E. , Hayes, K. , Grencis, R. , Duque‐Correa, M. , & Buck, A. (2020). Extracellular vesicles from Heligmosomoides bakeri and Trichuris muris contain distinct microRNA families and small RNAs that could underpin different functions in the host. International Journal for Parasitology, 50(9), 719–729. 10.1016/J.IJPARA.2020.06.002 PubMed DOI PMC
WHO . (2020). Ending the neglect to attain the Sustainable Development Goals. WHO (World Health Organization), 2. https://www.who.int/publications/i/item/9789240010352
Wititkornkul, B. , Hulme, B. J. , Tomes, J. J. , Allen, N. R. , Davis, C. N. , Davey, S. D. , Cookson, A. R. , Phillips, H. C. , Hegarty, M. J. , Swain, M. T. , Brophy, P. M. , Wonfor, R. E. , & Morphew, R. M. (2021). Evidence of immune modulators in the secretome of the equine tapeworm anoplocephala perfoliata. Pathogens, 10(7), 912. 10.3390/PATHOGENS10070912/S1 PubMed DOI PMC
Woith, E. , Fuhrmann, G. , & Melzig, M. F. (2019). Extracellular vesicles—connecting kingdoms. In: International journal of molecular sciences. MDPI AG. 10.3390/ijms20225695 PubMed DOI PMC
Zitvogel, L. , Regnault, A. , Lozier, A. , Wolfers, J. , Flament, C. , Tenza, D. , Ricciardi‐Castagnoli, P. , Raposo, G. , & Amigorena, S. (1998). Eradication of established murine tumors using a novel cell‐free vaccine: Dendritic cell‐derived exosomes. Nature Medicine, 4(5), 594–600. 10.1038/NM0598-594 PubMed DOI