The Yin and the Yang of extracellular vesicles during viral infections

Biomedical Journal - Trang 100659 - 2023
Charlène Martin1, Gaëtan Ligat1, Cécile E. Malnou1
1Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), Université de Toulouse, INSERM, CNRS, UPS, Toulouse, France

Tài liệu tham khảo

van Niel, 2018, Shedding light on the cell biology of extracellular vesicles, Nat Rev Mol Cell Biol, 19, 213, 10.1038/nrm.2017.125 Théry, 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, J Extracell Vesicles, 7, 10.1080/20013078.2018.1535750 van Niel, 2022, Challenges and directions in studying cell–cell communication by extracellular vesicles, Nat Rev Mol Cell Biol, 23, 369, 10.1038/s41580-022-00460-3 Moulin, 2023, Extracellular vesicles and viruses: two intertwined entities, Int J Mol Sci, 24, 1036, 10.3390/ijms24021036 Martins, 2020, Extracellular vesicles in viral infections: two sides of the same coin?, Front Cell Infect Microbiol, 10, 593170, 10.3389/fcimb.2020.593170 Nolte-‘t Hoen, 2016, Extracellular vesicles and viruses: are they close relatives?, Proc Natl Acad Sci U S A, 113, 9155, 10.1073/pnas.1605146113 Votteler, 2013, Virus budding and the ESCRT pathway, Cell Host Microbe, 14, 10.1016/j.chom.2013.08.012 Schmidt, 2012, The ESCRT machinery, Curr Biol, 22, R116, 10.1016/j.cub.2012.01.028 Pfitzner, 2020, An ESCRT-III polymerization sequence drives membrane deformation and fission, Cell, 182, 1140, 10.1016/j.cell.2020.07.021 Chung, 2008, NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains, J Virol, 82, 4884, 10.1128/JVI.02667-07 Carpp, 2011, Interaction between the yellow fever virus nonstructural protein NS3 and the host protein Alix contributes to the release of infectious particles, Microb Infect, 13, 85, 10.1016/j.micinf.2010.10.010 Pattanakitsakul, 2010, Association of alix with late endosomal lysobisphosphatidic acid is important for dengue virus infection in human endothelial cells, J Proteome Res, 9, 4640, 10.1021/pr100357f Tabata, 2016, Unique requirement for ESCRT factors in flavivirus particle formation on the endoplasmic reticulum, Cell Rep, 16, 2339, 10.1016/j.celrep.2016.07.068 Tran, 2022, Roles of ESCRT proteins ALIX and CHMP4A and their interplay with interferon-stimulated gene 15 during tick-borne flavivirus infection, J Virol, 96, 10.1128/JVI.01624-21 Ray, 2019, Angiomotin-like 1 links paramyxovirus M proteins to NEDD4 family ubiquitin ligases, Viruses, 11, 128, 10.3390/v11020128 Sadeghipour, 2017, Herpesviruses hijack host exosomes for viral pathogenesis, Semin Cell Dev Biol, 67, 91, 10.1016/j.semcdb.2017.03.005 Crump, 2007, Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4, J Virol, 81, 7380, 10.1128/JVI.00222-07 Calistri, 2007, Intracellular trafficking and maturation of herpes simplex virus type 1 gB and virus egress require functional biogenesis of multivesicular bodies, J Virol, 81, 11468, 10.1128/JVI.01364-07 Kharkwal, 2014, Blocking ESCRT-mediated envelopment inhibits microtubule-dependent trafficking of alphaherpesviruses in vitro, J Virol, 88, 14467, 10.1128/JVI.02777-14 Tandon, 2009, Human cytomegalovirus exploits ESCRT machinery in the process of virion maturation, J Virol, 83, 10797, 10.1128/JVI.01093-09 Feng, 2013, A pathogenic picornavirus acquires an envelope by hijacking cellular membranes, Nature, 496, 367, 10.1038/nature12029 Nagashima, 2014, Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies, J Gen Virol, 95, 2166, 10.1099/vir.0.066910-0 Gu, 2020, Exosomes cloak the virion to transmit Enterovirus 71 non-lytically, Virulence, 11, 32, 10.1080/21505594.2019.1705022 Bukong, 2014, Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90, PLoS Pathog, 10, 10.1371/journal.ppat.1004424 Celma, 2009, A viral nonstructural protein regulates bluetongue virus trafficking and release, J Virol, 83, 6806, 10.1128/JVI.00263-09 Barajas, 2009, A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus, PLoS Pathog, 5, 10.1371/journal.ppat.1000705 Barajas, 2014, Noncanonical role for the host Vps4 AAA+ ATPase ESCRT protein in the formation of Tomato bushy stunt virus replicase, PLoS Pathog, 10, 10.1371/journal.ppat.1004087 Stieler, 2014, Involvement of ESCRT-II in hepatitis B virus morphogenesis, PLoS One, 9, 10.1371/journal.pone.0091279 Inoue, 2019, Small interfering RNA screening for the small GTPase Rab proteins identifies Rab5B as a major regulator of hepatitis B virus production, J Virol, 93, 10.1128/JVI.00621-19 Chen, 2015, Supporting role for GTPase Rab27a in hepatitis C virus RNA replication through a novel miR-122-mediated effect, PLoS Pathog, 11, 10.1371/journal.ppat.1005116 Rowe, 2008, Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells, Virology, 382, 239, 10.1016/j.virol.2008.09.021 Utley, 2008, Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2, Proc Natl Acad Sci USA, 105, 10209, 10.1073/pnas.0712144105 Bruce, 2010, The Rab11 pathway is required for influenza A virus budding and filament formation, J Virol, 84, 5848, 10.1128/JVI.00307-10 Chambers, 2010, Trafficking of Sendai virus nucleocapsids is mediated by intracellular vesicles, PLoS One, 5, 10.1371/journal.pone.0010994 Baietti, 2012, Syndecan–syntenin–ALIX regulates the biogenesis of exosomes, Nat Cell Biol, 14, 677, 10.1038/ncb2502 Nkosi, 2020, Epstein-barr virus LMP1 promotes syntenin-1- and hrs-induced extracellular vesicle formation for its own secretion to increase cell proliferation and migration, mBio, 11, 10.1128/mBio.00589-20 Ahsan, 2016, Presence of viral RNA and proteins in exosomes from cellular clones resistant to Rift Valley fever virus infection, Front Microbiol, 7, 10.3389/fmicb.2016.00139 Mori, 2008, Human herpesvirus-6 induces MVB formation, and virus egress occurs by an exosomal release pathway, Traffic, 9, 1728, 10.1111/j.1600-0854.2008.00796.x Chen, 2015, Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses, Cell, 160, 619, 10.1016/j.cell.2015.01.032 Robinson, 2014, Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers, PLoS Pathog, 10, 10.1371/journal.ppat.1004045 Bello-Morales, 2020, Isolation/analysis of extracellular microvesicles from HSV-1-Infected cells, Methods Mol Biol, 2060, 305, 10.1007/978-1-4939-9814-2_17 Caruso, 2018, Apoptotic cell-derived extracellular vesicles: more than just debris, Front Immunol, 9, 10.3389/fimmu.2018.01486 Krejbich-Trotot, 2011, Chikungunya virus mobilizes the apoptotic machinery to invade host cell defenses, Faseb J, 25, 314, 10.1096/fj.10-164178 Helle, 2020, Intercellular transmission of naked viruses through extracellular vesicles: focus on polyomaviruses, Viruses, 12, 1086, 10.3390/v12101086 Fu, 2023, Exosomes mediate Coxsackievirus B3 transmission and expand the viral tropism, PLoS Pathog, 19, 10.1371/journal.ppat.1011090 van der Grein, 2022, The encephalomyocarditis virus Leader promotes the release of virions inside extracellular vesicles via the induction of secretory autophagy, Nat Commun, 13, 3625, 10.1038/s41467-022-31181-y Reyes-Ruiz, 2019, Isolation and characterization of exosomes released from mosquito cells infected with dengue virus, Virus Res, 266, 1, 10.1016/j.virusres.2019.03.015 van der Grein, 2018, Intricate relationships between naked viruses and extracellular vesicles in the crosstalk between pathogen and host, Semin Immunopathol, 40, 491, 10.1007/s00281-018-0678-9 Santiana, 2018, Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission, Cell Host Microbe, 24, 208, 10.1016/j.chom.2018.07.006 Zhang, 2021, Emerging pathogenic unit of vesicle-cloaked murine norovirus clusters is resistant to environmental stresses and UV254 disinfection, Environ Sci Technol, 55, 6197, 10.1021/acs.est.1c01763 Handala, 2020, BK polyomavirus hijacks extracellular vesicles for en bloc transmission, J Virol, 94, 10.1128/JVI.01834-19 Altan-Bonnet, 2019, Extracellular vesicles: vehicles of en bloc viral transmission, Virus Res, 265, 143, 10.1016/j.virusres.2019.03.023 Andino, 2015, Viral quasispecies, Virology, 479–480, 46, 10.1016/j.virol.2015.03.022 Segredo-Otero, 2019, The effect of genetic complementation on the fitness and diversity of viruses spreading as collective infectious units, Virus Res, 267, 41, 10.1016/j.virusres.2019.05.005 O'Hara, 2020, JC Virus infected choroid plexus epithelial cells produce extracellular vesicles that infect glial cells independently of the virus attachment receptor, PLoS Pathog, 16 Altan-Bonnet, 2017, Lipid tales of viral replication and transmission, Trends Cell Biol, 27, 201, 10.1016/j.tcb.2016.09.011 Zhang, 2019, Exosomes-mediated transmission of foot-and-mouth disease virus in vivo and in vitro, Vet Microbiol, 233, 164, 10.1016/j.vetmic.2019.04.030 Wang, 2018, Exosomes mediate intercellular transmission of porcine reproductive and respiratory Syndrome virus, J Virol, 92 Berry, 2022, Proviral role of human respiratory epithelial cell-derived small extracellular vesicles in SARS-CoV-2 infection, J Extracell Vesicles, 11, 10.1002/jev2.12269 Mack, 2000, Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection, Nat Med, 6, 769, 10.1038/77498 Pinto, 2019, HTLV-1 extracellular vesicles promote cell-to-cell contact, Front Microbiol, 10, 2147, 10.3389/fmicb.2019.02147 Bergamelli, 2021, Human cytomegalovirus infection changes the pattern of surface markers of small extracellular vesicles isolated from first trimester placental long-term histocultures, Front Cell Dev Biol, 9, 689122, 10.3389/fcell.2021.689122 Bergamelli, 2022, Human cytomegalovirus modifies placental small extracellular vesicle composition to enhance infection of fetal neural cells in vitro, Viruses, 14, 2030, 10.3390/v14092030 Lenassi, 2010, HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells, Traffic, 11, 110, 10.1111/j.1600-0854.2009.01006.x Vora, 2018, Arthropod EVs mediate dengue virus transmission through interaction with a tetraspanin domain containing glycoprotein Tsp29Fb, Proc Natl Acad Sci U S A, 115, E6604, 10.1073/pnas.1720125115 Liu, 2014, Exosome-associated hepatitis C virus in cell cultures and patient plasma, Biochem Biophys Res Commun, 455, 218, 10.1016/j.bbrc.2014.10.146 Fu, 2017, Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection, PLoS Pathog, 13, 10.1371/journal.ppat.1006611 Zhou, 2019, Exosomes carry microRNAs into neighboring cells to promote diffusive infection of Newcastle disease virus, Viruses, 11, 527, 10.3390/v11060527 Yeh, 2023, The anti-immune dengue subgenomic flaviviral RNA is present in vesicles in mosquito saliva and is associated with increased infectivity, PLoS Pathog, 19, 10.1371/journal.ppat.1011224 Shi, 2019, Exosomal interferon-induced Transmembrane protein 2 transmitted to dendritic cells inhibits interferon alpha pathway activation and blocks anti-hepatitis B virus efficacy of exogenous interferon alpha, Hepatology, 69, 2396, 10.1002/hep.30548 Niazy, 2017, Misdirection of endosomal trafficking mediated by herpes simplex virus-encoded glycoprotein B, Faseb J, 31, 1650, 10.1096/fj.201600521R Turner, 2020, The host exosome pathway underpins biogenesis of the human cytomegalovirus virion, Elife, 9, 10.7554/eLife.58288 Yang, 2017, Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction, Cell Mol Immunol, 14, 465, 10.1038/cmi.2016.24 Pleet, 2019, Extracellular vesicles and Ebola virus: a new mechanism of immune evasion, Viruses, 11, 410, 10.3390/v11050410 Mukhamedova, 2019, Exosomes containing HIV protein Nef reorganize lipid rafts potentiating inflammatory response in bystander cells, PLoS Pathog, 15, 10.1371/journal.ppat.1007907 Sadri Nahand, 2020, Pathogenic role of exosomes and microRNAs in HPV-mediated inflammation and cervical cancer: a review, Int J Cancer, 146, 305, 10.1002/ijc.32688 Sur, 2022, Circulatory exosomes from COVID-19 patients trigger NLRP3 inflammasome in endothelial cells, mBio, 13, 10.1128/mbio.00951-22 Li, 2022, Effects of exosomal viral components on the tumor microenvironment, Cancers, 14, 3552, 10.3390/cancers14143552 Giannessi, 2020, The role of extracellular vesicles as allies of HIV, HCV and SARS viruses, Viruses, 12, 571, 10.3390/v12050571 Ouattara, 2018, Seminal exosomes and HIV-1 transmission, Andrologia, 50, 10.1111/and.13220 Malnou, 2018, Imprinted MicroRNA gene clusters in the evolution, development, and functions of mammalian placenta, Front Genet, 9, 706, 10.3389/fgene.2018.00706 Martin, 2022, Placental extracellular vesicles in maternal-fetal communication during pregnancy, Biochem Soc Trans, 50, 1785, 10.1042/BST20220734 Delorme-Axford, 2013, Human placental trophoblasts confer viral resistance to recipient cells, Proc Natl Acad Sci U S A, 110, 12048, 10.1073/pnas.1304718110 Bayer, 2018, Chromosome 19 microRNAs exert antiviral activity independent from type III interferon signaling, Placenta, 61, 33, 10.1016/j.placenta.2017.11.004 Hamilton, 2021, A placental specific miRNA miR-517a-3p exerts anti-human cytomegalovirus activity, Placenta, 112, 62, 10.1016/j.placenta.2021.06.013 Wickramage, 2023, SINE RNA of the imprinted miRNA clusters mediates constitutive type III interferon expression and antiviral protection in hemochorial placentas, Cell Host Microbe, 31, 1185, 10.1016/j.chom.2023.05.018 Baglio, 2016, Sensing of latent EBV infection through exosomal transfer of 5’pppRNA, Proc Natl Acad Sci U S A, 113, E587, 10.1073/pnas.1518130113 Liu, 2019, Exosome-delivered and Y RNA-derived small RNA suppresses influenza virus replication, J Biomed Sci, 26, 58, 10.1186/s12929-019-0553-6 Wang, 2019, Exosome-mediated delivery of inducible miR-423-5p enhances resistance of MRC-5 cells to Rabies virus infection, Int J Mol Sci, 20, 1537, 10.3390/ijms20071537 Gentili, 2015, Transmission of innate immune signaling by packaging of cGAMP in viral particles, Science, 349, 1232, 10.1126/science.aab3628 Deschamps, 2018, Extracellular vesicles released by herpes simplex virus 1-infected cells block virus replication in recipient cells in a STING-dependent manner, J Virol, 92, 10.1128/JVI.01102-18 Yao, 2018, Exosomes exploit the virus entry machinery and pathway to transmit alpha interferon-induced antiviral activity, J Virol, 92, 15788, 10.1128/JVI.01578-18 Wrensch, 2019, Interferon-induced Transmembrane proteins mediate viral evasion in acute and chronic hepatitis C virus infection, Hepatology, 70, 1506, 10.1002/hep.30699 Zhu, 2015, IFITM3-containing exosome as a novel mediator for anti-viral response in dengue virus infection, Cell Microbiol, 17, 105, 10.1111/cmi.12339 Bedford, 2020, Airway exosomes released during influenza virus infection serve as a key component of the antiviral innate immune response, Front Immunol, 11, 887, 10.3389/fimmu.2020.00887 Chahar, 2018, Respiratory syncytial virus infection changes cargo composition of exosome released from airway epithelial cells, Sci Rep, 8, 387, 10.1038/s41598-017-18672-5 Velandia-Romero, 2020, Extracellular vesicles of U937 macrophage cell line infected with DENV-2 induce activation in endothelial cells EA.hy926, PLoS One, 15, 10.1371/journal.pone.0227030 Kouwaki, 2016, Extracellular vesicles including exosomes regulate innate immune responses to hepatitis B virus infection, Front Immunol, 7, 335, 10.3389/fimmu.2016.00335 Lindenbergh, 2018, Antigen presentation by extracellular vesicles from professional antigen-presenting cells, Annu Rev Immunol, 36, 435, 10.1146/annurev-immunol-041015-055700 Zhao, 2023, Extracellular vesicles from Zika virus-infected cells display viral E protein that binds ZIKV-neutralizing antibodies to prevent infection enhancement, EMBO J, 42, 10.15252/embj.2022112096