When Extracellular Vesicles Go Viral: A Bird’s Eye View
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Abstract
The science of extracellular vesicles (EVs) is a rapidly growing field that spans multiple aspects of normal physiology and pathophysiology. EVs play a critical role in most basic biological processes of cell-cell communications under normal conditions and in disease. EVs have “gone viral” not only in terms of research popularity, but also in our realization that they exhibit an elaborate crosstalk with viruses, particularly with the enveloped ones, which are also extracellular vesicles that are released by cells as a part of their virulence cycle yet are replicative. Here, we highlight some of the complexities underlying EV-virus crosstalk and pathways and provide our insights on key challenges from the viewpoint of EV biology.
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References
1. Lecoq H. [Discovery of the first virus, the tobacco mosaic virus: 1892 or 1898?]. C R Acad Sci III. 2001;324(10):929-33. doi: 10.1016/s0764-4469(01)01368-3. PubMed PMID: 11570281.
2. Welsh JA, Goberdhan DCI, O’Driscoll L, Buzas EI, Blenkiron C, Bussolati B, Cai H, Di Vizio D, Driedonks TAP, Erdbrugger U, Falcon-Perez JM, Fu QL, Hill AF, Lenassi M, Lim SK, Mahoney MG, Mohanty S, Moller A, Nieuwland R, Ochiya T, Sahoo S, Torrecilhas AC, Zheng L, Zijlstra A, Abuelreich S, Bagabas R, Bergese P, Bridges EM, Brucale M, Burger D, Carney RP, Cocucci E, Crescitelli R, Hanser E, Harris AL, Haughey NJ, Hendrix A, Ivanov AR, Jovanovic-Talisman T, Kruh-Garcia NA, Ku’ulei-Lyn Faustino V, Kyburz D, Lasser C, Lennon KM, Lotvall J, Maddox AL, Martens-Uzunova ES, Mizenko RR, Newman LA, Ridolfi A, Rohde E, Rojalin T, Rowland A, Saftics A, Sandau US, Saugstad JA, Shekari F, Swift S, Ter-Ovanesyan D, Tosar JP, Useckaite Z, Valle F, Varga Z, van der Pol E, van Herwijnen MJC, Wauben MHM, Wehman AM, Williams S, Zendrini A, Zimmerman AJ, Consortium M, Thery C, Witwer KW. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J Extracell Vesicles. 2024;13(2):e12404. doi: 10.1002/jev2.12404. PubMed PMID: 38326288; PMCID: PMC10850029.
3. Chutipongtanate S, Morrow AL, Newburg DS. Human Milk Extracellular Vesicles: A Biological System with Clinical Implications. Cells. 2022;11(15). doi: 10.3390/cells11152345. PubMed PMID: 35954189; PMCID: PMC9367292.
4. Gallo DM, Fitzgerald W, Romero R, Gomez-Lopez N, Gudicha DW, Than NG, Bosco M, Chaiworapongsa T, Jung E, Meyyazhagan A, Suksai M, Gotsch F, Erez O, Tarca AL, Margolis L. Proteomic profile of extracellular vesicles in maternal plasma of women with fetal death. J Matern Fetal Neonatal Med. 2023;36(1):2177529. doi: 10.1080/14767058.2023.2177529. PubMed PMID: 36813269; PMCID: PMC10395052.
5. H US, Brotherton D, Inal J. Communication is key: extracellular vesicles as mediators of infection and defence during host-microbe interactions in animals and plants. FEMS Microbiol Rev. 2022;46(1). doi: 10.1093/femsre/fuab044. PubMed PMID: 34448857; PMCID: PMC8767456.
6. Biller SJ, Coe A, Arellano AA, Dooley K, Silvestri SM, Gong JS, Yeager EA, Becker JW, Chisholm SW. Environmental and Taxonomic Drivers of Bacterial Extracellular Vesicle Production in Marine Ecosystems. Appl Environ Microbiol. 2023;89(6):e0059423. doi: 10.1128/aem.00594-23. PubMed PMID: 37199672; PMCID: PMC10304870.
7. Lee JH. The complex role of extracellular vesicles in HIV infection. BMB Rep. 2023;56(6):335-40. doi: 10.5483/BMBRep.2023-0073. PubMed PMID: 37291055; PMCID: PMC10315562.
8. Hendrix A, Lippens L, Pinheiro C, Théry C, Martin-Jaular L, Lötvall J, Lässer C, Hill AF, Witwer KW. Extracellular vesicle analysis. Nature Reviews Methods Primers. 2023;3(1):56. doi: 10.1038/s43586-023-00240-z.
9. Fusco C, De Rosa G, Spatocco I, Vitiello E, Procaccini C, Frige C, Pellegrini V, La Grotta R, Furlan R, Matarese G, Prattichizzo F, de Candia P. Extracellular vesicles as human therapeutics: A scoping review of the literature. J Extracell Vesicles. 2024;13(5):e12433. doi: 10.1002/jev2.12433. PubMed PMID: 38738585; PMCID: PMC11089593.
10. Mohammadipoor A, Hershfield MR, Linsenbardt HR, Smith J, Mack J, Natesan S, Averitt DL, Stark TR, Sosanya NM. Biological function of Extracellular Vesicles (EVs): a review of the field. Mol Biol Rep. 2023;50(10):8639-51. doi: 10.1007/s11033-023-08624-w. PubMed PMID: 37535245.
11. Gilboa T, Ter-Ovanesyan D, Wang SC, Whiteman S, Kannarkat GT, Church GM, Chen-Plotkin AS, Walt DR. Measurement of alpha-synuclein as protein cargo in plasma extracellular vesicles. Proc Natl Acad Sci U S A. 2024;121(45):e2408949121. doi: 10.1073/pnas.2408949121. PubMed PMID: 39475636; PMCID: PMC11551346.
12. Rey-Cadilhac F, Rachenne F, Misse D, Pompon J. Viral Components Trafficking with(in) Extracellular Vesicles. Viruses. 2023;15(12). doi: 10.3390/v15122333. PubMed PMID: 38140574; PMCID: PMC10747788.
13. Moulin C, Crupi MJF, Ilkow CS, Bell JC, Boulton S. Extracellular Vesicles and Viruses: Two Intertwined Entities. Int J Mol Sci. 2023;24(2). doi: 10.3390/ijms24021036. PubMed PMID: 36674550; PMCID: PMC9861478.
14. Wazny L, Whiteside TL, Pietrowska M. Oncoviral Infections and Small Extracellular Vesicles. Viruses. 2024;16(8). doi: 10.3390/v16081291. PubMed PMID: 39205265; PMCID: PMC11359865.
15. Nolte-’t Hoen E, Cremer T, Gallo RC, Margolis LB. Extracellular vesicles and viruses: Are they close relatives? Proc Natl Acad Sci U S A. 2016;113(33):9155-61. doi: 10.1073/pnas.1605146113. PubMed PMID: 27432966; PMCID: PMC4995926.
16. Vucetic A, Lafleur A, Cote M, Kobasa D, Chan M, Alvarez F, Piccirillo C, Dong G, Olivier M. Extracellular vesicle storm during the course of Ebola virus infection in primates. Front Cell Infect Microbiol. 2023;13:1275277. doi: 10.3389/fcimb.2023.1275277. PubMed PMID: 38035334; PMCID: PMC10684970.
17. da Silva-Januario ME, da Costa CS, Tavares LA, Oliveira AK, Januario YC, de Carvalho AN, Cassiano MHA, Rodrigues RL, Miller ME, Palameta S, Arns CW, Arruda E, Paes Leme AF, daSilva LLP. HIV-1 Nef Changes the Proteome of T Cells Extracellular Vesicles Depleting IFITMs and Other Antiviral Factors. Mol Cell Proteomics. 2023;22(12):100676. doi: 10.1016/j.mcpro.2023.100676. PubMed PMID: 37940003; PMCID: PMC10746527.
18. Vanpouille C, Brichacek B, Pushkarsky T, Dubrovsky L, Fitzgerald W, Mukhamedova N, Garcia-Hernandez S, Matthies D, Popratiloff A, Sviridov D, Margolis L, Bukrinsky M. HIV-1 Nef is carried on the surface of extracellular vesicles. J Extracell Vesicles. 2024;13(7):e12478. doi: 10.1002/jev2.12478. PubMed PMID: 39016173; PMCID: PMC11252832.
19. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J, Plachy J, Stangassinger M, Erfle V, Schlondorff D. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000;6(7):769-75. doi: 10.1038/77498. PubMed PMID: 10888925.
20. Barclay RA, Mensah GA, Cowen M, DeMarino C, Kim Y, Pinto DO, Erickson J, Kashanchi F. Extracellular Vesicle Activation of Latent HIV-1 Is Driven by EV-Associated c-Src and Cellular SRC-1 via the PI3K/AKT/mTOR Pathway. Viruses. 2020;12(6). doi: 10.3390/v12060665. PubMed PMID: 32575590; PMCID: PMC7354524.
21. Yang L, Li J, Li S, Dang W, Xin S, Long S, Zhang W, Cao P, Lu J. Extracellular Vesicles Regulated by Viruses and Antiviral Strategies. Front Cell Dev Biol. 2021;9:722020. doi: 10.3389/fcell.2021.722020. PubMed PMID: 34746122; PMCID: PMC8566986.
22. Giannessi F, Aiello A, Franchi F, Percario ZA, Affabris E. The Role of Extracellular Vesicles as Allies of HIV, HCV and SARS Viruses. Viruses. 2020;12(5). doi: 10.3390/v12050571. PubMed PMID: 32456011; PMCID: PMC7291340.
23. O’Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020;21(10):585-606. doi: 10.1038/s41580-020-0251-y. PubMed PMID: 32457507; PMCID: PMC7249041.
24. Mata-Rocha M, Rodriguez-Hernandez RM, Chavez-Olmos P, Garrido E, Robles-Vazquez C, Aguilar-Ruiz S, Torres-Aguilar H, Gonzalez-Torres C, Gaytan-Cervantes J, Mejia-Arangure JM, Romero-Tlalolini MLA. Presence of HPV DNA in extracellular vesicles from HeLa cells and cervical samples. Enferm Infecc Microbiol Clin (Engl Ed). 2020;38(4):159-65. doi: 10.1016/j.eimc.2019.06.011. PubMed PMID: 31395428.
25. Martins ST, Alves LR. Extracellular Vesicles in Viral Infections: Two Sides of the Same Coin? Front Cell Infect Microbiol. 2020;10:593170. doi: 10.3389/fcimb.2020.593170. PubMed PMID: 33335862; PMCID: PMC7736630.
26. Kim Y, Mensah GA, Al Sharif S, Pinto DO, Branscome H, Yelamanchili SV, Cowen M, Erickson J, Khatkar P, Mahieux R, Kashanchi F. Extracellular Vesicles from Infected Cells Are Released Prior to Virion Release. Cells. 2021;10(4). doi: 10.3390/cells10040781. PubMed PMID: 33916140; PMCID: PMC8066806.
27. Buzas EI. The roles of extracellular vesicles in the immune system. Nat Rev Immunol. 2023;23(4):236-50. doi: 10.1038/s41577-022-00763-8. PubMed PMID: 35927511; PMCID: PMC9361922.
28. Papadakos SP, Arvanitakis K, Stergiou IE, Vallilas C, Sougioultzis S, Germanidis G, Theocharis S. Interplay of Extracellular Vesicles and TLR4 Signaling in Hepatocellular Carcinoma Pathophysiology and Therapeutics. Pharmaceutics. 2023;15(10). doi: 10.3390/pharmaceutics15102460. PubMed PMID: 37896221; PMCID: PMC10610499.
29. Gross R, Ressin H, von Maltitz P, Albers D, Schneider L, Bley H, Hoffmann M, Cortese M, Gupta D, Deniz M, Choi JY, Jansen J, Preusser C, Seehafer K, Pohlmann S, Voelker DR, Goffinet C, Pogge-von Strandmann E, Bunz U, Bartenschlager R, El Andaloussi S, Sparrer KMJ, Herker E, Becker S, Kirchhoff F, Munch J, Muller JA. Phosphatidylserine-exposing extracellular vesicles in body fluids are an innate defence against apoptotic mimicry viral pathogens. Nat Microbiol. 2024;9(4):905-21. doi: 10.1038/s41564-024-01637-6. PubMed PMID: 38528146; PMCID: PMC10994849.
30. Margolis L. Extracellular vesicles block viral entryways. Nat Microbiol. 2024;9(4):882-3. doi: 10.1038/s41564-024-01651-8. PubMed PMID: 38528149.
31. Delorme-Axford E, Donker RB, Mouillet JF, Chu T, Bayer A, Ouyang Y, Wang T, Stolz DB, Sarkar SN, Morelli AE, Sadovsky Y, Coyne CB. Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci U S A. 2013;110(29):12048-53. doi: 10.1073/pnas.1304718110. PubMed PMID: 23818581; PMCID: PMC3718097.
32. Mouillet JF, Ouyang Y, Bayer A, Coyne CB, Sadovsky Y. The role of trophoblastic microRNAs in placental viral infection. Int J Dev Biol. 2014;58(2-4):281-9. doi: 10.1387/ijdb.130349ys. PubMed PMID: 25023694; PMCID: PMC4377297.
33. Nahui Palomino RA, Vanpouille C, Laghi L, Parolin C, Melikov K, Backlund P, Vitali B, Margolis L. Extracellular vesicles from symbiotic vaginal lactobacilli inhibit HIV-1 infection of human tissues. Nat Commun. 2019;10(1):5656. doi: 10.1038/s41467-019-13468-9. PubMed PMID: 31827089; PMCID: PMC6906448.
34. Dilsiz N. A comprehensive review on recent advances in exosome isolation and characterization: Toward clinical applications. Transl Oncol. 2024;50:102121. doi: 10.1016/j.tranon.2024.102121. PubMed PMID: 39278189; PMCID: PMC11418158.
35. Khanabdali R, Mandrekar M, Grygiel R, Vo PA, Palma C, Nikseresht S, Barton S, Shojaee M, Bhuiyan S, Asari K, Belzer S, Ansari K, Coward JI, Perrin L, Hooper J, Guanzon D, Lai A, Salomon C, Kershner K, Newton C, Horejsh D, Rice G. High-throughput surface epitope immunoaffinity isolation of extracellular vesicles and downstream analysis. Biol Methods Protoc. 2024;9(1):bpae032. doi: 10.1093/biomethods/bpae032. PubMed PMID: 39070184; PMCID: PMC11272960.
36. Normak K, Papp M, Ullmann M, Paganini C, Manno M, Bongiovanni A, Bergese P, Arosio P. Multiparametric Orthogonal Characterization of Extracellular Vesicles by Liquid Chromatography Combined with In-Line Light Scattering and Fluorescence Detection. Anal Chem. 2023;95(33):12443-51. doi: 10.1021/acs.analchem.3c02108. PubMed PMID: 37556360; PMCID: PMC10448444.
37. Bian J, Gobalasingham N, Purchel A, Lin J. The Power of Field-Flow Fractionation in Characterization of Nanoparticles in Drug Delivery. Molecules. 2023;28(10). doi: 10.3390/molecules28104169. PubMed PMID: 37241911; PMCID: PMC10224342.
38. Strohle G, Gan J, Li H. Affinity-based isolation of extracellular vesicles and the effects on downstream molecular analysis. Anal Bioanal Chem. 2022;414(24):7051-67. doi: 10.1007/s00216-022-04178-1. PubMed PMID: 35732746.
39. Noble JM, Roberts LM, Vidavsky N, Chiou AE, Fischbach C, Paszek MJ, Estroff LA, Kourkoutis LF. Direct comparison of optical and electron microscopy methods for structural characterization of extracellular vesicles. J Struct Biol. 2020;210(1):107474. doi: 10.1016/j.jsb.2020.107474. PubMed PMID: 32032755; PMCID: PMC7067680.
40. Cho S, Yi J, Kwon Y, Kang H, Han C, Park J. Multifluorescence Single Extracellular Vesicle Analysis by Time-Sequential Illumination and Tracking. ACS Nano. 2021;15(7):11753-61. doi: 10.1021/acsnano.1c02556. PubMed PMID: 34181396.
41. Welsh JA, van der Pol E, Bettin BA, Carter DRF, Hendrix A, Lenassi M, Langlois MA, Llorente A, van de Nes AS, Nieuwland R, Tang V, Wang L, Witwer KW, Jones JC. Towards defining reference materials for measuring extracellular vesicle refractive index, epitope abundance, size and concentration. J Extracell Vesicles. 2020;9(1):1816641. doi: 10.1080/20013078.2020.1816641. PubMed PMID: 33062218; PMCID: PMC7534292.
42. Johnsen KB, Gudbergsson JM, Andresen TL, Simonsen JB. What is the blood concentration of extracellular vesicles? Implications for the use of extracellular vesicles as blood-borne biomarkers of cancer. Biochim Biophys Acta Rev Cancer. 2019;1871(1):109-16. doi: 10.1016/j.bbcan.2018.11.006. PubMed PMID: 30528756.
43. Hatton IA, Galbraith ED, Merleau NSC, Miettinen TP, Smith BM, Shander JA. The human cell count and size distribution. Proc Natl Acad Sci U S A. 2023;120(39):e2303077120. doi: 10.1073/pnas.2303077120. PubMed PMID: 37722043; PMCID: PMC10523466.
44. Auber M, Svenningsen P. An estimate of extracellular vesicle secretion rates of human blood cells. J Extracell Biol. 2022;1(6):e46. doi: 10.1002/jex2.46. PubMed PMID: 38938292; PMCID: PMC11080926.
45. Fordjour FK, Guo C, Ai Y, Daaboul GG, Gould SJ. A shared, stochastic pathway mediates exosome protein budding along plasma and endosome membranes. J Biol Chem. 2022;298(10):102394. doi: 10.1016/j.jbc.2022.102394. PubMed PMID: 35988652; PMCID: PMC9512851.
46. Van Delen M, Derdelinckx J, Wouters K, Nelissen I, Cools N. A systematic review and meta-analysis of clinical trials assessing safety and efficacy of human extracellular vesicle-based therapy. J Extracell Vesicles. 2024;13(7):e12458. doi: 10.1002/jev2.12458. PubMed PMID: 38958077; PMCID: PMC11220457.
47. Jeppesen DK, Zhang Q, Franklin JL, Coffey RJ. Extracellular vesicles and nanoparticles: emerging complexities. Trends Cell Biol. 2023;33(8):667-81. doi: 10.1016/j.tcb.2023.01.002. PubMed PMID: 36737375; PMCID: PMC10363204.
48. Zhang Q, Jeppesen DK, Higginbotham JN, Franklin JL, Coffey RJ. Comprehensive isolation of extracellular vesicles and nanoparticles. Nat Protoc. 2023;18(5):1462-87. doi: 10.1038/s41596-023-00811-0. PubMed PMID: 36914899; PMCID: PMC10445291.
49. Lozano-Andres E, Enciso-Martinez A, Gijsbers A, Ridolfi A, Van Niel G, Libregts S, Pinheiro C, van Herwijnen MJC, Hendrix A, Brucale M, Valle F, Peters PJ, Otto C, Arkesteijn GJA, Wauben MHM. Physical association of low density lipoprotein particles and extracellular vesicles unveiled by single particle analysis. J Extracell Vesicles. 2023;12(11):e12376. doi: 10.1002/jev2.12376. PubMed PMID: 37942918; PMCID: PMC10634195.
50. Rak J, Strzadala L. Heterogeneity of Extracellular Vesicles and Particles: Molecular Voxels in the Blood Borne “Hologram” of Organ Function, Disfunction and Cancer. Arch Immunol Ther Exp (Warsz). 2023;71(1):5. doi: 10.1007/s00005-023-00671-2. PubMed PMID: 36729313.
51. Zhang Q, Jeppesen DK, Higginbotham JN, Graves-Deal R, Trinh VQ, Ramirez MA, Sohn Y, Neininger AC, Taneja N, McKinley ET, Niitsu H, Cao Z, Evans R, Glass SE, Ray KC, Fissell WH, Hill S, Rose KL, Huh WJ, Washington MK, Ayers GD, Burnette DT, Sharma S, Rome LH, Franklin JL, Lee YA, Liu Q, Coffey RJ. Supermeres are functional extracellular nanoparticles replete with disease biomarkers and therapeutic targets. Nat Cell Biol. 2021;23(12):1240-54. doi: 10.1038/s41556-021-00805-8. PubMed PMID: 34887515; PMCID: PMC8656144.
52. Chou CY, Chiang PC, Li CC, Chang JW, Lu PH, Hsu WF, Chang LC, Hsu JL, Wu MS, Wo AM. Improving the Purity of Extracellular Vesicles by Removal of Lipoproteins from Size Exclusion Chromatography- and Ultracentrifugation-Processed Samples Using Glycosaminoglycan-Functionalized Magnetic Beads. ACS Appl Mater Interfaces. 2024;16(34):44386-98. doi: 10.1021/acsami.4c03869. PubMed PMID: 39149774; PMCID: PMC11367580.
53. Brennan K, Martin K, FitzGerald SP, O’Sullivan J, Wu Y, Blanco A, Richardson C, Mc Gee MM. A comparison of methods for the isolation and separation of extracellular vesicles from protein and lipid particles in human serum. Sci Rep. 2020;10(1):1039. doi: 10.1038/s41598-020-57497-7. PubMed PMID: 31974468; PMCID: PMC6978318.
54. Zaborowski MP, Balaj L, Breakefield XO, Lai CP. Extracellular Vesicles: Composition, Biological Relevance, and Methods of Study. Bioscience. 2015;65(8):783-97. doi: 10.1093/biosci/biv084. PubMed PMID: 26955082; PMCID: PMC4776721.
55. Winzer R, Nguyen DH, Schoppmeier F, Cortesi F, Gagliani N, Tolosa E. Purinergic enzymes on extracellular vesicles: immune modulation on the go. Front Immunol. 2024;15:1362996. doi: 10.3389/fimmu.2024.1362996. PubMed PMID: 38426088; PMCID: PMC10902224.
56. Toth EA, Turiak L, Visnovitz T, Cserep C, Mazlo A, Sodar BW, Forsonits AI, Petovari G, Sebestyen A, Komlosi Z, Drahos L, Kittel A, Nagy G, Bacsi A, Denes A, Gho YS, Szabo-Taylor KE, Buzas EI. Formation of a protein corona on the surface of extracellular vesicles in blood plasma. J Extracell Vesicles. 2021;10(11):e12140. doi: 10.1002/jev2.12140. PubMed PMID: 34520123; PMCID: PMC8439280.
57. Wolf M, Poupardin RW, Ebner-Peking P, Andrade AC, Blochl C, Obermayer A, Gomes FG, Vari B, Maeding N, Eminger E, Binder HM, Raninger AM, Hochmann S, Brachtl G, Spittler A, Heuser T, Ofir R, Huber CG, Aberman Z, Schallmoser K, Volk HD, Strunk D. A functional corona around extracellular vesicles enhances angiogenesis, skin regeneration and immunomodulation. J Extracell Vesicles. 2022;11(4):e12207. doi: 10.1002/jev2.12207. PubMed PMID: 35398993; PMCID: PMC8994701.
58. Musico A, Zenatelli R, Romano M, Zendrini A, Alacqua S, Tassoni S, Paolini L, Urbinati C, Rusnati M, Bergese P, Pomarico G, Radeghieri A. Surface functionalization of extracellular vesicle nanoparticles with antibodies: a first study on the protein corona “variable”. Nanoscale Adv. 2023;5(18):4703-17. doi: 10.1039/d3na00280b. PubMed PMID: 37705771; PMCID: PMC10496878.
59. Cocozza F, Martin-Jaular L, Lippens L, Di Cicco A, Arribas YA, Ansart N, Dingli F, Richard M, Merle L, Jouve San Roman M, Poullet P, Loew D, Levy D, Hendrix A, Kassiotis G, Joliot A, Tkach M, Thery C. Extracellular vesicles and co-isolated endogenous retroviruses from murine cancer cells differentially affect dendritic cells. EMBO J. 2023;42(24):e113590. doi: 10.15252/embj.2023113590. PubMed PMID: 38073509; PMCID: PMC10711651.
60. Ezzat K, Pernemalm M, Palsson S, Roberts TC, Jarver P, Dondalska A, Bestas B, Sobkowiak MJ, Levanen B, Skold M, Thompson EA, Saher O, Kari OK, Lajunen T, Sverremark Ekstrom E, Nilsson C, Ishchenko Y, Malm T, Wood MJA, Power UF, Masich S, Linden A, Sandberg JK, Lehtio J, Spetz AL, El Andaloussi S. The viral protein corona directs viral pathogenesis and amyloid aggregation. Nat Commun. 2019;10(1):2331. doi: 10.1038/s41467-019-10192-2. PubMed PMID: 31133680; PMCID: PMC6536551.
61. Raposo G, Stahl PD. Extracellular vesicles - on the cusp of a new language in the biological sciences. Extracell Vesicles Circ Nucl Acids. 2023;4(2):240-54. doi: 10.20517/evcna.2023.18. PubMed PMID: 38288044; PMCID: PMC10824536.
62. Nahui Palomino RA, Vanpouille C, Costantini PE, Margolis L. Microbiota-host communications: Bacterial extracellular vesicles as a common language. PLoS Pathog. 2021;17(5):e1009508. doi: 10.1371/journal.ppat.1009508. PubMed PMID: 33984071; PMCID: PMC8118305.
63. Kaur S, Elkahloun AG, Arakelyan A, Young L, Myers TG, Otaizo-Carrasquero F, Wu W, Margolis L, Roberts DD. CD63, MHC class 1, and CD47 identify subsets of extracellular vesicles containing distinct populations of noncoding RNAs. Sci Rep. 2018;8(1):2577. doi: 10.1038/s41598-018-20936-7. PubMed PMID: 29416092; PMCID: PMC5803193.
64. Jahnke K, Staufer O. Membranes on the move: The functional role of the extracellular vesicle membrane for contact-dependent cellular signalling. J Extracell Vesicles. 2024;13(4):e12436. doi: 10.1002/jev2.12436. PubMed PMID: 38649339; PMCID: PMC11035383.
65. Bonsergent E, Grisard E, Buchrieser J, Schwartz O, Thery C, Lavieu G. Quantitative characterization of extracellular vesicle uptake and content delivery within mammalian cells. Nat Commun. 2021;12(1):1864. doi: 10.1038/s41467-021-22126-y. PubMed PMID: 33767144; PMCID: PMC7994380.
66. Ginini L, Billan S, Fridman E, Gil Z. Insight into Extracellular Vesicle-Cell Communication: From Cell Recognition to Intracellular Fate. Cells. 2022;11(9). doi: 10.3390/cells11091375. PubMed PMID: 35563681; PMCID: PMC9101098.
67. Somiya M, Kuroda S. Real-Time Luminescence Assay for Cytoplasmic Cargo Delivery of Extracellular Vesicles. Anal Chem. 2021;93(13):5612-20. doi: 10.1021/acs.analchem.1c00339. PubMed PMID: 33759512.
68. Somiya M, Kuroda S. Reporter gene assay for membrane fusion of extracellular vesicles. J Extracell Vesicles. 2021;10(13):e12171. doi: 10.1002/jev2.12171. PubMed PMID: 34807503; PMCID: PMC8607979.
69. van Dongen HM, Masoumi N, Witwer KW, Pegtel DM. Extracellular Vesicles Exploit Viral Entry Routes for Cargo Delivery. Microbiol Mol Biol Rev. 2016;80(2):369-86. doi: 10.1128/MMBR.00063-15. PubMed PMID: 26935137; PMCID: PMC4867369.
70. van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213-28. doi: 10.1038/nrm.2017.125. PubMed PMID: 29339798.
71. Vietri M, Radulovic M, Stenmark H. The many functions of ESCRTs. Nat Rev Mol Cell Biol. 2020;21(1):25-42. doi: 10.1038/s41580-019-0177-4. PubMed PMID: 31705132.
72. van Niel G, Carter DRF, Clayton A, Lambert DW, Raposo G, Vader P. Challenges and directions in studying cell-cell communication by extracellular vesicles. Nat Rev Mol Cell Biol. 2022;23(5):369-82. doi: 10.1038/s41580-022-00460-3. PubMed PMID: 35260831.
73. Matsui T, Osaki F, Hiragi S, Sakamaki Y, Fukuda M. ALIX and ceramide differentially control polarized small extracellular vesicle release from epithelial cells. EMBO Rep. 2021;22(5):e51475. doi: 10.15252/embr.202051475. PubMed PMID: 33724661; PMCID: PMC8097368.
74. Yun JW, Barzegar M, Boyer CJ, Minagar A, Couraud PO, Alexander JS. Brain Endothelial Cells Release Apical and Basolateral Microparticles in Response to Inflammatory Cytokine Stimulation: Relevance to Neuroinflammatory Stress? Front Immunol. 2019;10:1455. doi: 10.3389/fimmu.2019.01455. PubMed PMID: 31316509; PMCID: PMC6610500.
75. Davies BA, Morton LO, Jefferson JR, Rozeveld CN, Doskey LC, LaRusso NF, Katzmann DJ. Polarized human cholangiocytes release distinct populations of apical and basolateral small extracellular vesicles. Mol Biol Cell. 2020;31(22):2463-74. doi: 10.1091/mbc.E19-03-0133. PubMed PMID: 32845745; PMCID: PMC7851850.
76. Colombo F, Casella G, Podini P, Finardi A, Racchetti G, Norton EG, Cocucci E, Furlan R. Polarized cells display asymmetric release of extracellular vesicles. Traffic. 2021;22(4):98-110. doi: 10.1111/tra.12775. PubMed PMID: 33314523.
77. Wang X, Wilkinson R, Kildey K, Ungerer JPJ, Hill MM, Shah AK, Mohamed A, Dutt M, Molendijk J, Healy H, Kassianos AJ. Molecular and functional profiling of apical versus basolateral small extracellular vesicles derived from primary human proximal tubular epithelial cells under inflammatory conditions. J Extracell Vesicles. 2021;10(4):e12064. doi: 10.1002/jev2.12064. PubMed PMID: 33643548; PMCID: PMC7886702.
78. Richens JH, Dmitrieva M, Zenner HL, Muschalik N, Butler R, Glashauser J, Camelo C, Luschnig S, Munro S, Rittscher J, St Johnston D. Tracking exocytic vesicle movements reveals the spatial control of secretion in epithelial cells. bioRxiv. 2024. doi: 10.1101/2024.01.25.577201.
79. Saint-Pol J, Gosselet F, Duban-Deweer S, Pottiez G, Karamanos Y. Targeting and Crossing the Blood-Brain Barrier with Extracellular Vesicles. Cells. 2020;9(4). doi: 10.3390/cells9040851. PubMed PMID: 32244730; PMCID: PMC7226770.
80. Li H, Pinilla-Macua I, Ouyang Y, Sadovsky E, Kajiwara K, Sorkin A, Sadovsky Y. Internalization of trophoblastic small extracellular vesicles and detection of their miRNA cargo in P-bodies. J Extracell Vesicles. 2020;9(1):1812261. doi: 10.1080/20013078.2020.1812261. PubMed PMID: 32944196; PMCID: PMC7480505.
81. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sanchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980. doi: 10.1038/ncomms3980. PubMed PMID: 24356509; PMCID: PMC3905700.
82. Liu XM, Ma L, Schekman R. Selective sorting of microRNAs into exosomes by phase-separated YBX1 condensates. Elife. 2021;10. doi: 10.7554/eLife.71982. PubMed PMID: 34766549; PMCID: PMC8612733.
83. Lucotti S, Kenific CM, Zhang H, Lyden D. Extracellular vesicles and particles impact the systemic landscape of cancer. EMBO J. 2022;41(18):e109288. doi: 10.15252/embj.2021109288. PubMed PMID: 36052513; PMCID: PMC9475536.
84. Zhu X, Lin X, Hu L, Wang L, Zhu Q. Harnessing crosstalk between extracellular vesicles and viruses for disease diagnostics and therapeutics. Extracell Vesicles Circ Nucl Acids. 2024;5(3):358-70. doi: 10.20517/evcna.2024.30. PubMed PMID: 39697627; PMCID: PMC11648403.
85. Nemeth K, Kestecher BM, Ghosal S, Bodnar BR, Kittel A, Hambalko S, Kovacshazi C, Giricz Z, Ferdinandy P, Osteikoetxea X, Burkhardt R, Buzas EI, Orso E. Therapeutic and pharmacological applications of extracellular vesicles and lipoproteins. Br J Pharmacol. 2024;181(23):4733-49. doi: 10.1111/bph.17336. PubMed PMID: 39491825.
86. Dooley K, McConnell RE, Xu K, Lewis ND, Haupt S, Youniss MR, Martin S, Sia CL, McCoy C, Moniz RJ, Burenkova O, Sanchez-Salazar J, Jang SC, Choi B, Harrison RA, Houde D, Burzyn D, Leng C, Kirwin K, Ross NL, Finn JD, Gaidukov L, Economides KD, Estes S, Thornton JE, Kulman JD, Sathyanarayanan S, Williams DE. A versatile platform for generating engineered extracellular vesicles with defined therapeutic properties. Mol Ther. 2021;29(5):1729-43. doi: 10.1016/j.ymthe.2021.01.020. PubMed PMID: 33484965; PMCID: PMC8116569.
87. Manno M, Bongiovanni A, Margolis L, Bergese P, Arosio P. The physico-chemical landscape of extracellular vesicles. Nature Reviews Bioengineering. 2024;3(1):68-82. doi: 10.1038/s44222-024-00255-5.