Exosomes in the life cycle of viruses and the pathogenesis of viral infections
- 作者: Kushch A.A.1, Ivanov A.V.2
-
隶属关系:
- National Research Center for Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya of the Ministry of Health of the Russian Federation
- Institute of Molecular Biology named after V.A. Engelhardt of Russian Academy of Sciences
- 期: 卷 68, 编号 3 (2023)
- 页面: 181-197
- 栏目: REVIEWS
- URL: https://ogarev-online.ru/0507-4088/article/view/132631
- DOI: https://doi.org/10.36233/0507-4088-173
- EDN: https://elibrary.ru/uablap
- ID: 132631
如何引用文章
详细
Exosomes are extracellular vesicles of endosomal origin, with a bilayer membrane, 30–160 nm in diameter. Exosomes are released from cells of different origins and are detected in various body fluids. They contain nucleic acids, proteins, lipids, metabolites and can transfer the contents to recipient cells. Exosome biogenesis involves cellular proteins of the Rab GTPase family and the ESCRT system, which regulate budding, vesicle transport, molecule sorting, membrane fusion, formation of multivesicular bodies and exosome secretion. Exosomes are released from cells infected with viruses and may contain viral DNA and RNA, as well as mRNA, microRNA, other types of RNA, proteins and virions. Exosomes are capable of transferring viral components into uninfected cells of various organs and tissues. This review analyzes the impact of exosomes on the life cycle of widespread viruses that cause serious human diseases: human immunodeficiency virus (HIV-1), hepatitis B virus, hepatitis C virus, SARS-CoV-2. Viruses are able to enter cells by endocytosis, use molecular and cellular pathways involving Rab and ESCRT proteins to release exosomes and spread viral infections. It has been shown that exosomes can have multidirectional effects on the pathogenesis of viral infections, suppressing or enhancing the course of diseases. Exosomes can potentially be used in noninvasive diagnostics as biomarkers of the stage of infection, and exosomes loaded with biomolecules and drugs - as therapeutic agents. Genetically modified exosomes are promising candidates for new antiviral vaccines.
作者简介
Alla Kushch
National Research Center for Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya of the Ministry of Health of the Russian Federation
编辑信件的主要联系方式.
Email: vitallku@mail.ru
ORCID iD: 0000-0002-3396-5533
SPIN 代码: 6964-1715
Dr. Sci. (Biology), Professor, Leading Researcher
俄罗斯联邦, 123098, MoscowAlexandr Ivanov
Institute of Molecular Biology named after V.A. Engelhardt of Russian Academy of Sciences
Email: aivanov@yandex.ru
ORCID iD: 0000-0002-5659-9679
SPIN 代码: 5776-5496
Dr. Sci. Biol., Chief Researcher, head of the laboratory of biochemistry of viral infections; deputy director for scientific work
俄罗斯联邦, 119991, Moscow参考
- Harding C., Heuser J., Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 1983; 97(2): 329–39. https://doi.org/10.1083/jcb.97.2.329
- Pan B.T., Johnstone R.M. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983; 33(3): 967–78. https://doi.org/10.1016/0092-8674(83)90040-5
- Harding C.V., Heuser J.E., Stahl P.D. Exosomes: looking back three decades and into the future. J. Cell Biol. 2013; 200(4): 367–71. https://doi.org/10.1083/jcb.201212113
- Johnstone R.M., Adam M., Hammond J.R., Orr L., Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 1987; 262(19): 9412–20.
- Xie S., Zhang Q., Jiang L. Current knowledge on exosome biogenesis, cargo-sorting mechanism and therapeutic implications. Membranes (Basel). 2022; 12(5): 498. https://doi.org/10.3390/membranes12050498
- Kowal J., Arras G., Colombo M., Jouve M., Morath J.P., Primdal-Bengtson B., et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl Acad. Sci. USA. 2016; 113(8): E968–77. https://doi.org/10.1073/pnas.1521230113
- Wang S., Zhang K., Tan S., Xin J., Yuan Q., Xu H., et al. Circular RNAs in body fluids as cancer biomarkers: the new frontier of liquid biopsies. Mol. Cancer. 2021; 20(1): 13. https://doi.org/10.1186/s12943-020-01298-z
- Kalluri R., LeBleu V.S. The biology, function, and biomedical applications of exosomes. Science. 2020; 367(6478): eaau6977. https://doi.org/10.1126/science.aau6977
- Zeng Y., Qiu Y., Jiang W., Shen J., Yao X., He X., et al. Biological features of extracellular vesicles and challenges. Front. Cell Dev. Biol. 2022; 10: 816698. https://doi.org/10.3389/fcell.2022.816698
- Todd K.V., Tripp R.A. Exosome-mediated human norovirus infection. PLoS One. 2020; 15(8): e0237044. https://doi.org/10.1371/journal.pone.0237044
- Kowalczyk A., Wrzecińska M., Czerniawska-Piątkowska E., Kupczyński R. Exosomes – spectacular role in reproduction. Biomed. Pharmacother. 2022; 148: 112752. https://doi.org/10.1016/j.biopha.2022.112752
- Lee I., Choi Y., Shin D.U., Kwon M., Kim S., Jung H., et al. Small extracellular vesicles as a new class of medicines. Pharmaceutics. 2023; 15(2): 325. https://doi.org/10.3390/pharmaceutics15020325
- Picca A., Guerra F., Calvani R., Coelho-Junior H.J., Bucci C., Marzetti E. Circulating extracellular vesicles: friends and foes in neurodegeneration. Neural. Regen. Res. 2022; 17(3): 534–42. https://doi.org/10.4103/1673-5374.320972
- Liu F., Vermesh O., Mani V., Ge T.J., Madsen S.J., Sabour A., et al. The exosome total isolation chip. ACS Nano. 2017; 11(11): 10712–23. https://doi.org/10.1021/acsnano.7b04878
- Zhang H., Lyden D. Asymmetric-flow field-flow fractionation technology for exomere and small extracellular vesicle separation and characterization. Nat. Protoc. 2019; 14(4): 1027–53. https://doi.org/10.1038/s41596-019-0126-x
- Kang Y.T., Kim Y.J., Bu J., Cho Y.H., Han S.W., Moon B.I. High-purity capture and release of circulating exosomes using an exosome-specific dual-patterned immunofiltration (ExoDIF) device. Nanoscale. 2017; 9(36): 13495–505. https://doi.org/10.1039/c7nr04557c
- Pathan M., Fonseka P., Chitti S.V., Kang T., Sanwlani R., Van Deun J., et al. Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic. Acids. Res. 2019; 47(D1): D516–9. https://doi.org/10.1093/nar/gky1029
- Sidhom K., Obi P.O., Saleem A. A review of exosomal isolation methods: is size exclusion chromatography the best option? Int. J. Mol. Sci. 2020; 21(18): 6466. https://doi.org/10.3390/ijms21186466
- van der Pol E., Sturk A., van Leeuwen T., Nieuwland R., Coumans F. Standardization of extracellular vesicle measurements by flow cytometry through vesicle diameter approximation. J. Thromb. Haemost. 2018; 16(6): 1236–45. https://doi.org/10.1111/jth.14009
- Théry C., Witwer K.W., Aikawa E., Alcaraz M.J., Anderson J.D., Andriantsitohaina R., et al. 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. J. Extracell. Vesicles. 2018; 7(1): 1535750. https://doi.org/10.1080/20013078.2018
- Mulligan R.J., Yap C.C., Winckler B. Endosomal transport to lysosomes and the trans-Golgi network in neurons and other cells: visualizing maturational flux. Methods Mol. Biol. 2023; 2557: 595–618. https://doi.org/10.1007/978-1-0716-2639-9_36
- Krylova S.V., Feng D. The machinery of exosomes: biogenesis, release, and uptake. Int. J. Mol. Sci. 2023; 24(2): 1337. https://doi.org/10.3390/ijms24021337
- Homma Y., Hiragi S., Fukuda M. Rab family of small GTPases: an updated view on their regulation and functions. FEBS J. 2021; 288(1): 36–55. https://doi.org/10.1111/febs.15453
- Liu G., Yin X.M. The role of extracellular vesicles in liver pathogenesis. Am. J. Pathol. 2022; 192(10): 1358–67. https://doi.org/10.1016/j.ajpath.2022.06.007
- Scourfield E.J., Martin-Serrano J. Growing functions of the ESCRT machinery in cell biology and viral replication. Biochem. Soc. Trans. 2017; 45(3): 613–34. https://doi.org/10.1042/BST20160479
- Lin C.Y., Urbina A.N., Wang W.H., Thitithanyanont A., Wang S.F. Virus hijacks host proteins and machinery for assembly and budding, with HIV-1 as an example. Viruses. 2022; 14(7): 1528. https://doi.org/10.3390/v14071528
- Johnson D.S., Bleck M., Simon S.M. Timing of ESCRT-III protein recruitment and membrane scission during HIV-1 assembly. Elife. 2018; 7: e36221. https://doi.org/10.7554/eLife.36221
- Hoffman H.K., Fernandez M.V., Groves N.S., Freed E.O., van Engelenburg S.B. Genomic tagging of endogenous human ESCRT-I complex preserves ESCRT-mediated membrane-remodeling functions. J. Biol. Chem. 2019; 294(44): 16266–81. https://doi.org/10.1074/jbc.RA119.009372
- Meusser B., Purfuerst B., Luft F.C. HIV-1 Gag release from yeast reveals ESCRT interaction with the Gag N-terminal protein region. J. Biol. Chem. 2020; 295(52): 17950–72. https://doi.org/10.1074/jbc.RA120.014710
- Hadpech S., Moonmuang S., Chupradit K., Yasamut U., Tayapiwatana C. Updating on roles of HIV intrinsic factors: a review of their antiviral mechanisms and emerging functions. Intervirology. 2022; 65(2): 67–79. https://doi.org/10.1159/000519241
- Gerber P.P., Cabrini M., Jancic C., Paoletti L., Banchio C., von Bilderling C., et al. Rab27a controls HIV-1 assembly by regulating plasma membrane levels of phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 2015; 209(3): 435–52. https://doi.org/10.1083/jcb.201409082
- Teow S.Y., Nordin A.C., Ali S.A., Khoo A.S. Exosomes in human immunodeficiency virus type I pathogenesis: threat or opportunity? Adv. Virol. 2016; 2016: 9852494. https://doi.org/10.1155/2016/9852494
- Chiozzini C., Arenaccio C., Olivetta E., Anticoli S., Manfredi F., Ferrantelli F., et al. Trans-dissemination of exosomes from HIV-1-infected cells fosters both HIV-1 trans-infection in resting CD4+ T lymphocytes and reactivation of the HIV-1 reservoir. Arch. Virol. 2017; 162(9): 2565–77. https://doi.org/10.1007/s00705-017-3391-4
- Hayes C.N., Zhang Y., Makokha G.N., Hasan M.Z., Omokoko M.D., Chayama K. Early events in hepatitis B virus infection: From the cell surface to the nucleus. J. Gastroenterol. Hepatol. 2016; 31(2): 302–9. https://doi.org/10.1111/jgh.13175
- Lin Y., Wu C., Wang X., Kemper T., Squire A., Gunzer M., et al. Hepatitis B virus is degraded by autophagosome-lysosome fusion mediated by Rab7 and related components. Protein Cell. 2019; 10(1): 60–6. https://doi.org/10.1007/s13238-018-0555-2
- Chou S.F., Tsai M.L., Huang J.Y., Chang Y.S., Shih C. The dual role of an ESCRT-0 component HGS in HBV transcription and naked capsid secretion. PLoS Pathog. 2015; 11(10): e1005123. https://doi.org/10.1371/journal.ppat.1005123
- Prange R. Hepatitis B virus movement through the hepatocyte: An update. Biol. Cell. 2022; 114(12): 325–48. https://doi.org/10.1111/boc.202200060
- Wu Q., Glitscher M., Tonnemacher S., Schollmeier A., Raupach J., Zahn T., et al. Presence of intact hepatitis B virions in exosomes. Cell Mol. Gastroenterol. Hepatol. 2023; 15(1): 237–59. https://doi.org/10.1016/j.jcmgh.2022.09.012
- van der Ree M.H., Jansen L., Kruize Z., van Nuenen A.C., van Dort K.A., Takkenberg R.B., et al. Plasma MicroRNA levels are associated with hepatitis B e antigen status and treatment response in chronic hepatitis B patients. J. Infect. Dis. 2017; 215(9): 1421–9. https://doi.org/10.1093/infdis/jix140
- Wang D., Huang T., Ren T., Liu Q., Zhou Z., Ge L., et al. Identification of blood exosomal miRNA-1246, miRNA-150-5p, miRNA-5787 and miRNA-8069 as sensitive biomarkers for hepatitis B virus infection. Clin. Lab. 2022; 68(2). https://doi.org/10.7754/Clin.Lab.2021.210415
- Ninomiya M., Inoue J., Krueger E.W., Chen J., Cao H., Masamune A., et al. The exosome-associated tetraspanin CD63 contributes to the efficient assembly and infectivity of the hepatitis B virus. Hepatol. Commun. 2021; 5(7): 1238–51. https://doi.org/10.1002/hep4.1709
- Kakizaki M., Yamamoto Y., Yabuta S., Kurosaki N., Kagawa T., Kotani A. The immunological function of extracellular vesicles in hepatitis B virus-infected hepatocytes. PLoS One. 2018; 13(12): e0205886. https://doi.org/10.1371/journal.pone.0205886
- Wang C., Liu J., Yan Y., Tan Y. Role of exosomes in chronic liver disease development and their potential clinical applications. J. Immunol. Res. 2022; 2022: 1695802. https://doi.org/10.1155/2022/1695802
- Bunz M., Ritter M., Schindler M. HCV egress – unconventional secretion of assembled viral particles. Trends Microbiol. 2022; 30(4): 364–78. https://doi.org/10.1016/j.tim.2021.08.005
- Kulhanek K.R., Roose J.P., Rubio I. Regulation of the small GTPase Ras and its relevance to human disease. Methods. Mol. Biol. 2021; 2262: 19–43. https://doi.org/10.1007/978-1-0716-1190-6_2
- Elgner F., Hildt E., Bender D. Relevance of Rab proteins for the life cycle of hepatitis C virus. Front. Cell Dev. Biol. 2018; 6: 166. https://doi.org/10.3389/fcell.2018.00166
- Ahmed I., Akram Z., Iqbal H.M.N., Munn A.L. The regulation of Endosomal Sorting Complex Required for Transport and accessory proteins in multivesicular body sorting and enveloped viral budding – an overview. Int. J. Biol. Macromol. 2019; 127: 1–11. https://doi.org/10.1016/j.ijbiomac.2019.01.015
- Corless L., Crump C.M., Griffin S.D., Harris M. Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles. J. Gen. Virol. 2010; 91(Pt. 2): 362–72. https://doi.org/10.1099/vir.0.017285-0
- Li C., Gao Z., Cui Z., Liu Z., Bian Y., Sun H., et al. Deubiquitylation of Rab35 by USP32 promotes the transmission of imatinib resistance by enhancing exosome secretion in gastrointestinal stromal tumours. Oncogene. 2023; 42(12): 894–910. https://doi.org/10.1038/s41388-023-02600-1
- Kumar S., Barouch-Bentov R., Xiao F., Schor S., Pu S., Biquand E., et al. MARCH8 ubiquitinates the hepatitis C virus nonstructural 2 protein and mediates viral envelopment. Cell Rep. 2019; 26(7): 1800–14.e5. https://doi.org/10.1016/j.celrep.2019.01.075
- Tamai K., Shiina M., Tanaka N., Nakano T., Yamamoto A., Kondo Y., et al. Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. Virology. 2012; 422(2): 377–85. https://doi.org/10.1016/j.virol.2011.11.009
- Tamai K., Tanaka N., Nakano T., Kakazu E., Kondo Y., Inoue J., et al. Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem. Biophys. Res. Commun. 2010; 399(3): 384–90. https://doi.org/10.1016/j.bbrc.2010.07.083
- Barouch-Bentov R., Neveu G., Xiao F., Beer M., Bekerman E., Schor S., et al. Hepatitis C virus proteins interact with the Endosomal Sorting Complex Required for Transport (ESCRT) machinery via ubiquitination to facilitate viral envelopment. mBio. 2016; 7(6): e01456-16. https://doi.org/10.1128/mBio.01456-16
- Younossi Z., Tacke F., Arrese M., Chander Sharma B., Mostafa I., Bugianesi E., et al. Global perspectives on nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology. 2019; 69(6): 2672–82. https://doi.org/10.1002/hep.30251
- Newman L.A., Muller K., Rowland A. Circulating cell-specific extracellular vesicles as biomarkers for the diagnosis and monitoring of chronic liver diseases. Cell Mol. Life Sci. 2022; 79(5): 232. https://doi.org/10.1007/s00018-022-04256-8
- Li J., Liu H., Mauer A.S., Lucien F., Raiter A., Bandla H., et al. Characterization of cellular sources and circulating levels of extracellular vesicles in a dietary murine model of nonalcoholic steatohepatitis. Hepatol. Commun. 2019; 3(9): 1235–49. https://doi.org/10.1002/hep4.1404
- Shah R., Patel T., Freedman J.E. Circulating extracellular vesicles in human disease. N. Engl. J. Med. 2018; 379(10): 958–66. https://doi.org/10.1056/NEJMra1704286
- Ramakrishnaiah V., Thumann C., Fofana I., Habersetzer F., Pan Q., de Ruiter P.E., et al. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. Proc. Natl Acad. Sci. USA. 2013; 110(32): 13109–13. https://doi.org/10.1073/pnas.1221899110
- Bukong T.N., Momen-Heravi F., Kodys K., Bala S., Szabo G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 2014; 10(10): e1004424. https://doi.org/10.1371/journal.ppat.1004424
- Dreux M., Garaigorta U., Boyd B., Décembre E., Chung J., Whitten-Bauer C., et al. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host. Microbe. 2012; 12(4): 558–70. https://doi.org/10.1016/j.chom.2012.08.010
- Zhang S., Kodys K., Babcock G.J., Szabo G. CD81/CD9 tetraspanins aid plasmacytoid dendritic cells in recognition of hepatitis C virus-infected cells and induction of interferon-alpha. Hepatology. 2013; 58(3): 940–9. https://doi.org/10.1002/hep.25827
- Conde-Vancells J., Rodriguez-Suarez E., Embade N., Gil D., Matthiesen R., Valle M., et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome. Res. 2008; 7(12): 5157–66. https://doi.org/10.1021/pr8004887
- Properzi F., Logozzi M., Fais S. Exosomes: the future of biomarkers in medicine. Biomark. Med. 2013; 7(5): 769–78. https://doi.org/10.2217/bmm.13.63
- Szabo G., Momen-Heravi F. Extracellular vesicles in liver disease and potential as biomarkers and therapeutic targets. Nat. Rev. Gastroenterol. Hepatol. 2017; 14(8): 455–66. https://doi.org/10.1038/nrgastro.2017.71
- Borrelli D.A., Yankson K., Shukla N., Vilanilam G., Ticer T., Wolfram J. Extracellular vesicle therapeutics for liver disease. J. Control. Release. 2018; 273: 86–98. https://doi.org/10.1016/j.jconrel.2018.01.022
- Lin D., Reddy V., Osman H., Lopez A., Koksal A.R., Rhadhi S.M., et al. Additional inhibition of Wnt/β-catenin signaling by metformin in DAA treatments as a novel therapeutic strategy for HCV-Infected patients. Cells. 2021; 10(4): 790. https://doi.org/10.3390/cells10040790
- McVey M.J., Kuebler W.M. Extracellular vesicles: biomarkers and regulators of vascular function during extracorporeal circulation. Oncotarget. 2018; 9(98): 37229–51. https://doi.org/10.18632/oncotarget.26433
- Fendl B., Weiss R., Eichhorn T., Linsberger I., Afonyushkin T., Puhm F., et al. Extracellular vesicles are associated with C-reactive protein in sepsis. Sci. Rep. 2021; 11(1): 6996. https://doi.org/10.1038/s41598-021-86489-4
- U.S. National Library of Medicine. Available at: https://clinicaltrials.gov/
- Feng Y., Wang A.T., Jia H.H., Zhao M., Yu H. A brief analysis of mesenchymal stem cells as biological drugs for the treatment of Acute-on-Chronic Liver Failure (ACLF): safety and potency. Curr. Stem. Cell Res. Ther. 2020; 15(3): 202–10. https://doi.org/10.2174/1574888X15666200101124317
- Qian X., Xu C., Fang S., Zhao P., Wang Y., Liu H., et al. Exosomal microRNAs derived from umbilical mesenchymal stem cells inhibit hepatitis C virus infection. Stem. Cells Transl. Med. 2016; 5(9): 1190–203. https://doi.org/10.5966/sctm.2015-0348
- Khatun M., Ray R.B. Mechanisms underlying hepatitis C virus-associated hepatic fibrosis. Cells. 2019; 8(10): 1249. https://doi.org/10.3390/cells8101249
- Devhare P.B., Sasaki R., Shrivastava S., Di Bisceglie A.M., Ray R., Ray R.B. Exosome-mediated intercellular communication between hepatitis C virus-infected hepatocytes and hepatic stellate cells. J. Virol. 2017; 91(6): e02225-16. https://doi.org/10.1128/JVI.02225-16
- Kim J.H., Lee C.H., Lee S.W. Exosomal transmission of microRNA from HCV replicating cells stimulates transdifferentiation in hepatic stellate cells. Mol. Ther. Nucleic. Acids. 2019; 14: 483–97. https://doi.org/10.1016/j.omtn.2019.01.006
- Bruno S., Pasquino C., Herrera Sanchez M.B., Tapparo M., Figliolini F., Grange C., et al. HLSC-derived extracellular vesicles attenuate liver fibrosis and inflammation in a murine model of non-alcoholic steatohepatitis. Mol. Ther. 2020; 28(2): 479–89. https://doi.org/10.1016/j.ymthe.2019.10.016
- Chiabotto G., Ceccotti E., Tapparo M., Camussi G., Bruno S. Human liver stem cell-derived extracellular vesicles target hepatic stellate cells and attenuate their pro-fibrotic phenotype. Front. Cell Dev. Biol. 2021; 9: 777462. https://doi.org/10.3389/fcell.2021.777462
- Rong X., Liu J., Yao X., Jiang T., Wang Y., Xie F. Human bone marrow mesenchymal stem cells-derived exosomes alleviate liver fibrosis through the Wnt/β-catenin pathway. Stem. Cell Res. Ther. 2019; 10(1): 98. https://doi.org/10.1186/s13287-019-1204-2
- Kim J., Lee C., Shin Y., Wang S., Han J., Kim M., et al. sEVs from tonsil-derived mesenchymal stromal cells alleviate activation of hepatic stellate cells and liver fibrosis through miR-486-5p. Mol. Ther. 2021; 29(4): 1471–86. https://doi.org/10.1016/j.ymthe.2020.12.025
- Du Z., Wu T., Liu L., Luo B., Wei C. Extracellular vesicles-derived miR-150-5p secreted by adipose-derived mesenchymal stem cells inhibits CXCL1 expression to attenuate hepatic fibrosis. J. Cell Mol. Med. 2021; 25(2): 701–15. https://doi.org/10.1111/jcmm.16119
- Chen L., Chen R., Kemper S., Cong M., You H., Brigstock D.R. Therapeutic effects of serum extracellular vesicles in liver fibrosis. J. Extracell. Vesicles. 2018; 7(1): 1461505. https://doi.org/10.1080/20013078.2018.1461505
- Bruno S., Chiabotto G., Camussi G. Extracellular vesicles: a therapeutic option for liver fibrosis. Int. J. Mol. Sci. 2020; 21(12): 4255. https://doi.org/10.3390/ijms21124255
- Hwang S., Yang Y.M. Exosomal microRNAs as diagnostic and therapeutic biomarkers in non-malignant liver diseases. Arch. Pharm. Res. 2021; 44(6): 574–87. https://doi.org/10.1007/s12272-021-01338-2
- Zhou Y., Wang X., Sun L., Zhou L., Ma T.C., Song L., et al. Toll-like receptor 3-activated macrophages confer anti-HCV activity to hepatocytes through exosomes. FASEB J. 2016; 30(12): 4132–40. https://doi.org/10.1096/fj.201600696R
- Fasbender F., Widera A., Hengstler J.G., Watzl C. Natural killer cells and liver fibrosis. Front. Immunol. 2016; 7: 19. https://doi.org/10.3389/fimmu.2016.00019
- Neviani P., Wise P.M., Murtadha M., Liu C.W., Wu C.H., Jong A.Y., et al. Natural killer-derived exosomal miR-186 inhibits neuroblastoma growth and immune escape mechanisms. Cancer Res. 2019; 79(6): 1151–64. https://doi.org/10.1158/0008-5472.CAN-18-0779
- Wang L., Wang Y., Quan J. Exosomes derived from natural killer cells inhibit hepatic stellate cell activation and liver fibrosis. Hum. Cell. 2020; 33(3): 582–9. https://doi.org/10.1007/s13577-020-00371-5
- Target Scan Human. Whitehead Institute for Biomedical Research. Available at: http://www.targetscan.org
- Wang L., Wang Y., Quan J. Exosomal miR-223 derived from natural killer cells inhibits hepatic stellate cell activation by suppressing autophagy. Mol. Med. 2020; 26(1): 81. https://doi.org/10.1186/s10020-020-00207-w
- Ye H.L., Zhang J.W., Chen X.Z., Wu P.B., Chen L., Zhang G. Ursodeoxycholic acid alleviates experimental liver fibrosis involving inhibition of autophagy. Life Sci. 2020; 242: 117175. https://doi.org/10.1016/j.lfs.2019.117175
- Zhang Y., Hua L., Lin C., Yuan M., Xu W., Raj D.A., et al. Pien-Tze-Huang alleviates CCl4-induced liver fibrosis through the inhibition of HSC autophagy and the TGF-β1/Smad2 pathway. Front. Pharmacol. 2022; 13: 937484. https://doi.org/10.3389/fphar.2022.937484
- Avalos P.N., Forsthoefel D.J. An emerging frontier in intercellular communication: extracellular vesicles in regeneration. Front. Cell Dev. Biol. 2022; 10: 849905. https://doi.org/10.3389/fcell.2022.849905
- Verweij F.J., Revenu C., Arras G., Dingli F., et al. Live tracking of inter-organ communication by endogenous exosomes in vivo. Dev. Cell. 2019; 48(4): 573–89.e4. https://doi.org/10.1016/j.devcel.2019.01.004
- Matsumoto A., Takahashi Y., Nishikawa M., Sano K., Morishita M., Charoenviriyakul C., et al. Role of phosphatidylserine-derived negative surface charges in the recognition and uptake of intravenously injected B16BL6-derived exosomes by macrophages. J. Pharm. Sci. 2017; 106(1): 168–75. https://doi.org/10.1016/j.xphs.2016.07.022
- Wu R., Fan X., Wang Y., Shen M., Zheng Y., Zhao S., et al. Mesenchymal stem cell-derived extracellular vesicles in liver immunity and therapy. Front. Immunol. 2022; 13: 833878. https://doi.org/10.3389/fimmu.2022.833878
- Schorey J.S., Harding C.V. Extracellular vesicles and infectious diseases: new complexity to an old story. J. Clin. Invest. 2016; 126(4): 1181–9. https://doi.org/10.1172/JCI81132
- Yao Z., Qiao Y., Li X., Chen J., Ding J., Bai L., et al. Exosomes exploit the virus entry machinery and pathway to transmit alpha interferon-induced antiviral activity. J. Virol. 2018; 92(24): e01578-18. https://doi.org/10.1128/JVI.01578-18
- Hassanpour M., Rezaie J., Nouri M., Panahi Y. The role of extracellular vesicles in COVID-19 virus infection. Infect. Genet. Evol. 2020; 85: 104422. https://doi.org/10.1016/j.meegid.2020.104422
- Earnest J.T., Hantak M.P., Li K., McCray P.B. Jr., Perlman S., Gallagher T. The tetraspanin CD9 facilitates MERS-coronavirus entry by scaffolding host cell receptors and proteases. PLoS Pathog. 2017; 13(7): e1006546. https://doi.org/10.1371/journal.ppat.1006546
- Barberis E., Vanella V.V., Falasca M., Caneapero V., Cappellano G., Raineri D., et al. Circulating exosomes are strongly involved in SARS-CoV-2 infection. Front. Mol. Biosci. 2021; 8: 632290. https://doi.org/10.3389/fmolb.2021.632290
- Bansal S., Perincheri S., Fleming T., Poulson C., Tiffany B., Bremner R.M., et al. Cutting edge: circulating exosomes with COVID spike protein are induced by BNT162b2 (Pfizer-BioNTech) vaccination prior to development of antibodies: a novel mechanism for immune activation by mRNA vaccines. J. Immunol. 2021; 207(10): 2405–10. https://doi.org/10.4049/jimmunol.2100637
- Sur S., Khatun M., Steele R., Isbell T.S., Ray R., Ray R.B. Exosomes from COVID-19 patients carry tenascin-C and fibrinogen-β in triggering inflammatory signals in cells of distant organ. Int. J. Mol. Sci. 2021; 22(6): 3184. https://doi.org/10.3390/ijms22063184
- Mills J.T., Schwenzer A., Marsh E.K., Edwards M.R., Sabroe I., Midwood K.S., et al. Airway epithelial cells generate pro-inflammatory tenascin-C and small extracellular vesicles in response to TLR3 stimuli and rhinovirus infection. Front. Immunol. 2019; 10: 1987. https://doi.org/10.3389/fimmu.2019.01987
- Gupta A., Madhavan M.V., Sehgal K., Nair N., Mahajan S., Sehrawat T.S., et al. Extrapulmonary manifestations of COVID-19. Nat. Med. 2020; 26(7): 1017–32. https://doi.org/10.1038/s41591-020-0968-3
- Kwon Y., Nukala S.B., Srivastava S., Miyamoto H., Ismail N.I., Jousma J., et al. Detection of viral RNA fragments in human iPSC cardiomyocytes following treatment with extracellular vesicles from SARS-CoV-2 coding sequence overexpressing lung epithelial cells. Stem. Cell Res. Ther. 2020; 11(1): 514. https://doi.org/10.1186/s13287-020-02033-7
- Wang J., Chen S., Bihl J. Exosome-mediated transfer of ACE2 (Angiotensin-Converting Enzyme 2) from endothelial progenitor cells promotes survival and function of endothelial cell. Oxid. Med. Cell Longev. 2020; 2020: 4213541. https://doi.org/10.1155/2020/4213541
- Cocozza F., Névo N., Piovesana E., Lahaye X., Buchrieser J., Schwartz O., et al. Extracellular vesicles containing ACE2 efficiently prevent infection by SARS-CoV-2 Spike protein-containing virus. J. Extracell. Vesicles. 2020; 10(2): e12050. https://doi.org/10.1002/jev2.12050
- El-Shennawy L., Hoffmann A.D., Dashzeveg N.K., McAndrews K.M., Mehl P.J., Cornish D., et al. Circulating ACE2-expressing extracellular vesicles block broad strains of SARS-CoV-2. Nat. Commun. 2022; 13(1): 405. https://doi.org/10.1038/s41467-021-27893-2
- Ching K.L., de Vries M., Gago J., Dancel-Manning K., Sall J., Rice W.J., et al. ACE2-containing defensosomes serve as decoys to inhibit SARS-CoV-2 infection. PLoS Biol. 2022; 20(9): e3001754. https://doi.org/10.1371/journal.pbio.3001754
- Song J.W., Lam S.M., Fan X., Cao W.J., Wang S.Y., Tian H., et al. Omics-driven systems interrogation of metabolic dysregulation in COVID-19 pathogenesis. Cell Metab. 2020; 32(2): 188–202.e5. https://doi.org/10.1016/j.cmet.2020.06.016
- Shenoy G.N., Loyall J., Berenson C.S., Kelleher R.J. Jr., Iyer V., Balu-Iyer S.V., et al. Sialic acid-dependent inhibition of T cells by exosomal ganglioside GD3 in ovarian tumor microenvironments. J. Immunol. 2018; 201(12): 3750–8. https://doi.org/10.4049/jimmunol.1801041
- Schnaar R.L. The biology of gangliosides. Adv. Carbohydr. Chem. Biochem. 2019; 76: 113–48. https://doi.org/10.1016/bs.accb.2018.09.002
- Fantini J., Chahinian H., Yahi N. Leveraging coronavirus binding to gangliosides for innovative vaccine and therapeutic strategies against COVID-19. Biochem. Biophys. Res. Commun. 2021; 538: 132–6. https://doi.org/10.1016/j.bbrc.2020.10.015
- Hall M.W., Joshi I., Leal L., Ooi E.E. Immune immunomodulation in coronavirus disease 2019 (COVID-19): strategic considerations for personalized therapeutic intervention. Clin. Infect. Dis. 2022; 74(1): 144–8. https://doi.org/10.1093/cid/ciaa904
- Holnthoner W., Bonstingl C., Hromada C., Muehleder S., Zipperle J., Stojkovic S., et al. Endothelial cell-derived extracellular vesicles size-dependently exert procoagulant activity detected by thromboelastometry. Sci. Rep. 2017; 7(1): 3707. https://doi.org/10.1038/s41598-017-03159-0
- Balbi C., Burrello J., Bolis S., Lazzarini E., Biemmi V., Pianezzi E., et al. Circulating extracellular vesicles are endowed with enhanced procoagulant activity in SARS-CoV-2 infection. EBioMedicine. 2021; 67: 103369. https://doi.org/10.1016/j.ebiom.2021.103369
- Cappellano G., Raineri D., Rolla R., Giordano M., Puricelli C., Vilardo B., et al. Circulating platelet-derived extracellular vesicles are a hallmark of SARS-Cov-2 infection. Cells. 2021; 10(1): 85. https://doi.org/10.3390/cells10010085
- Tahyra A.S.C., Calado R.T., Almeida F. The role of extracellular vesicles in COVID-19 pathology. Cells. 2022; 11(16): 2496. https://doi.org/10.3390/cells11162496
- Yang C.W., Chen R.D., Zhu Q.R., Han S.J., Kuang M.J. Efficacy of umbilical cord mesenchymal stromal cells for COVID-19: A systematic review and meta-analysis. Front. Immunol. 2022; 13: 923286. https://doi.org/10.3389/fimmu.2022.923286
- Tan M.I., Alfarafisa N.M., Septiani P., Barlian A., Firmansyah M., Faizal A., et al. Potential cell-based and cell-free therapy for patients with COVID-19. Cells. 2022; 11(15): 2319. https://doi.org/10.3390/cells11152319
- Bari E., Ferrarotti I., Saracino L., Perteghella S., Torre M.L., Richeldi L., et al. Mesenchymal stromal cell secretome for post-COVID-19 pulmonary fibrosis: a new therapy to treat the long-term lung sequelae? Cells. 2021; 10(5): 1203. https://doi.org/10.3390/cells10051203
- Gardin C., Ferroni L., Chachques J.C., Zavan B. Could mesenchymal stem cell-derived exosomes be a therapeutic option for critically ill COVID-19 patients? J. Clin. Med. 2020; 9(9): 2762. https://doi.org/10.3390/jcm9092762
- Perets N., Hertz S., London M., Offen D. Intranasal administration of exosomes derived from mesenchymal stem cells ameliorates autistic-like behaviors of BTBR mice. Mol. Autism. 2018; 9: 57. https://doi.org/10.1186/s13229-018-0240-6
- Elahi F.M., Farwell D.G., Nolta J.A., Anderson J.D. Preclinical translation of exosomes derived from mesenchymal stem/stromal cells. Stem. Cells. 2020; 38(1): 15–21. https://doi.org/10.1002/stem.3061
- Allan D., Tieu A., Lalu M., Burger D. Mesenchymal stromal cell-derived extracellular vesicles for regenerative therapy and immune modulation: Progress and challenges toward clinical application. Stem. Cells Transl. Med. 2020; 9(1): 39–46. https://doi.org/10.1002/sctm.19-0114
- Dinh P.C., Paudel D., Brochu H., Popowski K.D., Gracieux M.C., Cores J., et al. Inhalation of lung spheroid cell secretome and exosomes promotes lung repair in pulmonary fibrosis. Nat. Commun. 2020; 11(1): 1064. https://doi.org/10.1038/s41467-020-14344-7
- Cocozza F., Névo N., Piovesana E., Lahaye X., Buchrieser J., Schwartz O., et al. Extracellular vesicles containing ACE2 efficiently prevent infection by SARS-CoV-2 Spike protein-containing virus. J. Extracell. Vesicles. 2020; 10(2): e12050. https://doi.org/10.1002/jev2.12050
- Inal J.M. Decoy ACE2-expressing extracellular vesicles that competitively bind SARS-CoV-2 as a possible COVID-19 therapy. Clin. Sci. (Lond). 2020; 134(12): 1301–4. https://doi.org/10.1042/CS20200623
- Askenase P.W. COVID-19 therapy with mesenchymal stromal cells (MSC) and convalescent plasma must consider exosome involvement: Do the exosomes in convalescent plasma antagonize the weak immune antibodies? J. Extracell. Vesicles. 2020; 10(1): e12004. https://doi.org/10.1002/jev2.12004
- Rezabakhsh A., Mahdipour M., Nourazarian A., Habibollahi P., Sokullu E., Avci Ç.B., et al. Application of exosomes for the alleviation of COVID-19-related pathologies. Cell Biochem. Funct. 2022; 40(5): 430–8. https://doi.org/10.1002/cbf.3720
- Sengupta V., Sengupta S., Lazo A., Woods P., Nolan A., Bremer N. Exosomes derived from bone marrow mesenchymal stem cells as treatment for severe COVID-19. Stem. Cells Dev. 2020; 29(12): 747–54. https://doi.org/10.1089/scd.2020.0080
- Kuate S., Cinatl J., Doerr H.W., Uberla K. Exosomal vaccines containing the S protein of the SARS coronavirus induce high levels of neutralizing antibodies. Virology. 2007; 362(1): 26–37. https://doi.org/10.1016/j.virol.2006.12.011
- Sharma K., Koirala A., Nicolopoulos K., Chiu C., Wood N., Britton P.N. Vaccines for COVID-19: Where do we stand in 2021? Paediatr. Respir. Rev. 2021; 39: 22–31. https://doi.org/10.1016/j.prrv.2021.07.001
- Wang Z., Popowski K.D., Zhu D., de Juan Abad B.L., Wang X., Liu M., et al. Exosomes decorated with a recombinant SARS-CoV-2 receptor-binding domain as an inhalable COVID-19 vaccine. Nat. Biomed. Eng. 2022; 6(7): 791–805. https://doi.org/10.1038/s41551-022-00902-5
- Altan-Bonnet N. Extracellular vesicles are the Trojan horses of viral infection. Curr. Opin. Microbiol. 2016; 32: 77–81. https://doi.org/10.1016/j.mib.2016.05.004
- Badierah R.A., Uversky V.N., Redwan E.M. Dancing with Trojan horses: an interplay between the extracellular vesicles and viruses. J. Biomol. Struct. Dyn. 2021; 39(8): 3034–60. https://doi.org/10.1080/07391102.2020.1756409
- Sun L., Wang X., Zhou Y., Zhou R.H., Ho W.Z., Li J.L. Exosomes contribute to the transmission of anti-HIV activity from TLR3-activated brain microvascular endothelial cells to macrophages. Antiviral. Res. 2016; 134: 167–71. https://doi.org/10.1016/j.antiviral.2016.07.013
- Welch J.L., Kaddour H., Schlievert P.M., Stapleton J.T., Okeoma C.M. Semen exosomes promote transcriptional silencing of HIV-1 by disrupting NF-κB/Sp1/Tat circuitry. J. Virol. 2018; 92(21): e00731-18. https://doi.org/10.1128/JVI.00731-18
- Chen J., Li C., Li R., Chen H., Chen D., Li W. Exosomes in HIV infection. Curr. Opin. HIV AIDS. 2021; 16(5): 262–70. https://doi.org/10.1097/COH.0000000000000694
- Abraham A., Krasnodembskaya A. Mesenchymal stem cell-derived extracellular vesicles for the treatment of acute respiratory distress syndrome. Stem. Cells. Transl. Med. 2020; 9(1): 28–38. https://doi.org/10.1002/sctm.19-0205
- Popowski K.D., Dinh P.C., George A., Lutz H., Cheng K. Exosome therapeutics for COVID-19 and respiratory viruses. View (Beijing). 2021; 2(3): 20200186. https://doi.org/10.1002/VIW.20200186
- Rangel-Ramírez V.V., González-Sánchez H.M., Lucio-García C. Exosomes: from biology to immunotherapy in infectious diseases. Infect. Dis. (Lond). 2023; 55(2): 79–107. https://doi.org/10.1080/23744235.2022.2149852
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