Harnessing crosstalk between extracellular vesicles and viruses for disease diagnostics and therapeutics

Xinxi Zhu , Xiuhui Lin , Liang Hu , Liangxing Wang , Qingfu Zhu

Extracellular Vesicles and Circulating Nucleic Acids ›› 2024, Vol. 5 ›› Issue (3) : 358 -70.

PDF
Extracellular Vesicles and Circulating Nucleic Acids ›› 2024, Vol. 5 ›› Issue (3) :358 -70. DOI: 10.20517/evcna.2024.30
Review

Harnessing crosstalk between extracellular vesicles and viruses for disease diagnostics and therapeutics

Author information +
History +
PDF

Abstract

Extracellular vesicles (EVs) are increasingly acknowledged as important mediators of intercellular communication, closely related to the occurrence and development of a variety of diseases. Numerous studies have demonstrated that EVs play a multifaceted role in the infection process of viral diseases, elucidating their ability to both facilitate viral spread and inhibit infection progression. These versatile entities not only enhance infection rates and widen the scope of viral infection through the transmission of entire viruses or viral genomes, but also trigger antiviral responses and prompt cytokine secretion near the infection site, thereby fortifying the host's defense mechanisms and safeguarding neighboring cells against infection. This complicated crosstalk between EVs and viral infections prompts a deeper exploration into their roles in potential clinical applications. In this review, we aim to encapsulate the recent advances in understanding the intricate interplay between viruses and EVs, shedding light on the mechanisms underlying this vesicle-to-virion crosstalk. Furthermore, we underscore the significance of harnessing this knowledge for diagnostic and therapeutic functions in combating viral diseases.

Keywords

Extracellular vesicle / exosome / virus / viral infection / diagnostics / therapeutics

Cite this article

Download citation ▾
Xinxi Zhu, Xiuhui Lin, Liang Hu, Liangxing Wang, Qingfu Zhu. Harnessing crosstalk between extracellular vesicles and viruses for disease diagnostics and therapeutics. Extracellular Vesicles and Circulating Nucleic Acids, 2024, 5(3): 358-70 DOI:10.20517/evcna.2024.30

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles.Nat Rev Mol Cell Biol2018;19:213-28

[2]

Zhu Q,Yang Q.Recent technical advances to study metabolomics of extracellular vesicles.Microchem J2021;171:106816

[3]

Ruan S,He M.Light-induced high-efficient cellular production of immune functional extracellular vesicles.J Extracell Vesicles2022;11:e12194 PMCID:PMC8886920

[4]

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 Biol2022;23:369-82

[5]

Debnath K,Rivera A,Shin JW.Extracellular vesicle-matrix interactions.Nat Rev Mater2023;8:390-402 PMCID:PMC10919209

[6]

Yang R,Xia K,Zhu Q.A pH-Mediated highly selective system enabling simultaneous analysis of circulating rnas carried by extracellular vesicles and lipoproteins.Anal Chem2023;95:18803-13

[7]

Zhu Q,Li HP.Robust acute pancreatitis identification and diagnosis: RAPIDx.ACS Nano2023;17:8564-74

[8]

Zhu Q,Zhao Z.Microfluidic engineering of exosomes: editing cellular messages for precision therapeutics.Lab Chip2018;18:1690-703 PMCID:PMC5997967

[9]

Zhu Q,Deng C.The genetic source tracking of human urinary exosomes.Proc Natl Acad Sci U S A2021;118 PMCID:PMC8639375

[10]

Hendrix A,Pinheiro C.Extracellular vesicle analysis.Nat Rev Methods Primers2023;3

[11]

Dixson AC,Di Vizio D.Context-specific regulation of extracellular vesicle biogenesis and cargo selection.Nat Rev Mol Cell Biol2023;24:454-76 PMCID:PMC10330318

[12]

DeLong JP,Al-Ameeli ZT.Towards an integrative view of virus phenotypes.Nat Rev Microbiol2022;20:83-94

[13]

Koonin EV,Krupovic M.The logic of virus evolution.Cell Host Microbe2022;30:917-29

[14]

Kerviel A,Altan-Bonnet N.A new infectious unit: extracellular vesicles carrying virus populations.Annu Rev Cell Dev Biol2021;37:171-97

[15]

Schatz D,Saltvedt MR,Feldmesser E.Ecological significance of extracellular vesicles in modulating host-virus interactions during algal blooms.ISME J2021;15:3714-21 PMCID:PMC8630046

[16]

Peng Y,Li Y,Luan Y.Exosome and virus infection.Front Immunol2023;14:1154217 PMCID:PMC10098074

[17]

Deng L,Wang X.Syntenin regulates hepatitis C virus sensitivity to neutralizing antibody by promoting E2 secretion through exosomes.J Hepatol2019;71:52-61

[18]

Liao TL,Hsieh SL.Hepatitis C virus-induced exosomal microRNAs and toll-like receptor 7 polymorphism regulate B-cell activating factor.mBio2021;12:e0276421 PMCID:PMC8561394

[19]

Kouwaki T,Daito T.Extracellular Vesicles Including Exosomes Regulate Innate Immune Responses to Hepatitis B Virus Infection.Front Immunol2016;7:335 PMCID:PMC5005343

[20]

González-López O,Hu F.Redundant late domain functions of tandem VP2 YPX(3)L motifs in nonlytic cellular egress of quasi-enveloped hepatitis A virus.J Virol2018;92 PMCID:PMC6232465

[21]

Jiang W,Deng L.Hepatitis A virus structural protein pX interacts with ALIX and promotes the secretion of virions and foreign proteins through exosome-like vesicles.J Extracell Vesicles2020;9:1716513 PMCID:PMC7006762

[22]

Ding Q,Capuccino JM.Hepatitis E virus ORF3 is a functional ion channel required for release of infectious particles.Proc Natl Acad Sci U S A2017;114:1147-52 PMCID:PMC5293053

[23]

Mukhamedova N,Dragoljevic D.Exosomes containing HIV protein Nef reorganize lipid rafts potentiating inflammatory response in bystander cells.PLoS Pathog2019;15:e1007907 PMCID:PMC6657916

[24]

Pleet ML,DeMarino C.Ebola virus VP40 Modulates cell cycle and biogenesis of extracellular vesicles.J Infect Dis2018;218:S365-87 PMCID:PMC6249571

[25]

Fu Y,Zhang F.Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection.PLoS Pathog2017;13:e1006611 PMCID:PMC5614653

[26]

Fu Y.Exosomes mediate Coxsackievirus B3 transmission and expand the viral tropism.PLoS Pathog2023;19:e1011090 PMCID:PMC9888687

[27]

Ding T,Zhu X.Exosomes mediate the antibody-resistant intercellular transmission of porcine epidemic diarrhea virus.Vet Microbiol2023;284:109834

[28]

Wang J,Zhao G.Exosome-mediated delivery of inducible miR-423-5p enhances resistance of MRC-5 cells to rabies virus infection.Int J Mol Sci2019;20:1537 PMCID:PMC6479321

[29]

Li J,Liu Y.Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity.Nat Immunol2013;14:793-803

[30]

Yao Z,Li X.Exosomes exploit the virus entry machinery and pathway to transmit alpha interferon-induced antiviral activity.J Virol2018;92 PMCID:PMC6258946

[31]

Zhao F,Liu N.Extracellular vesicles from Zika virus-infected cells display viral E protein that binds ZIKV-neutralizing antibodies to prevent infection enhancement.EMBO J2023;42:e112096 PMCID:PMC10015360

[32]

Wakim LM.Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection.Nature2011;471:629-32 PMCID:PMC3423191

[33]

Chen YH,Hagemeijer MC.Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses.Cell2015;160:619-30 PMCID:PMC6704014

[34]

Santiana M,Ho BA.Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission.Cell Host Microbe2018;24:208-220.e8 PMCID:PMC6226266

[35]

O'Hara BA,Gee GV,Atwood WJ.JC Virus infected choroid plexus epithelial cells produce extracellular vesicles that infect glial cells independently of the virus attachment receptor.PLoS Pathog2020;16:e1008371 PMCID:PMC7075641

[36]

Herrmann IK,Fuhrmann G.Extracellular vesicles as a next-generation drug delivery platform.Nat Nanotechnol2021;16:748-59

[37]

Feng Z,McKnight KL.A pathogenic picornavirus acquires an envelope by hijacking cellular membranes.Nature2013;496:367-71 PMCID:PMC3631468

[38]

Bukong TN,Kodys K,Szabo G.Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90.PLoS Pathog2014;10:e1004424 PMCID:PMC4183590

[39]

Schatz D,Malitsky S,Feldmesser E.Communication via extracellular vesicles enhances viral infection of a cosmopolitan alga.Nat Microbiol2017;2:1485-92

[40]

Yang Y,Hou Z,Tian Z.Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction.Cell Mol Immunol2017;14:465-75 PMCID:PMC5423088

[41]

Li X,Liang Y.Extracellular vesicle-encapsulated adeno-associated viruses for therapeutic gene delivery to the heart.Circulation2023;148:405-25

[42]

Wang J,Liu C.Exosomes released from rabies virus-infected cells may be involved in the infection process.Virol Sin2019;34:59-65 PMCID:PMC6420551

[43]

Kalluri R.The biology, function, and biomedical applications of exosomes.Science2020;367 PMCID:PMC7717626

[44]

Dreux M,Boyd B.Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity.Cell Host Microbe2012;12:558-70 PMCID:PMC3479672

[45]

McKnight KL,González-López O,Chen X.Protein composition of the hepatitis A virus quasi-envelope.Proc Natl Acad Sci U S A2017;114:6587-92 PMCID:PMC5488923

[46]

Nkwe DO,Burden JJ,Marsh M.The intracellular plasma membrane-connected compartment in the assembly of HIV-1 in human macrophages.BMC Biol2016;14:50 PMCID:PMC4919869

[47]

Mackman N,Antoniak S.Tissue factor expression, extracellular vesicles, and thrombosis after infection with the respiratory viruses influenza A virus and coronavirus.J Thromb Haemost2021;19:2652-8 PMCID:PMC9770926

[48]

Wang Z,He H.Nonenveloped avian reoviruses released with small extracellular vesicles are highly infectious.Viruses2023;15:1610 PMCID:PMC10384003

[49]

Martins ST.Extracellular vesicles in viral infections: two sides of the same coin?.Front Cell Infect Microbiol2020;10:593170 PMCID:PMC7736630

[50]

Lindenbergh MFS.Antigen presentation by extracellular vesicles from professional antigen-presenting cells.Annu Rev Immunol2018;36:435-59

[51]

Kwon Y,Srivastava S.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 Ther2020;11:514 PMCID:PMC7703503

[52]

Wu Z,Tian C,Jiang L.Exploiting sound for emerging applications of extracellular vesicles.Nano Res2024;17:462-75 PMCID:PMC11073796

[53]

Zhu Q,Huang L.Identification and detection of plasma extracellular vesicles-derived biomarkers for esophageal squamous cell carcinoma diagnosis.Biosens Bioelectron2023;225:115088

[54]

He N,Zhong C.Nano pom-poms prepared exosomes enable highly specific cancer biomarker detection.Commun Biol2022;5:660 PMCID:PMC9253007

[55]

Yan H,Cheng S.Advances in analytical technologies for extracellular vesicles.Anal Chem2021;93:4739-74

[56]

Tian Y,Hu Y.Quality and efficiency assessment of six extracellular vesicle isolation methods by nano-flow cytometry.J Extracell Vesicles2020;9:1697028 PMCID:PMC6896440

[57]

McNamara RP.Modern techniques for the isolation of extracellular vesicles and viruses.J Neuroimmune Pharmacol2020;15:459-72 PMCID:PMC7065924

[58]

McNamara RP,Bailey A.Extracellular vesicles from Kaposi Sarcoma-associated herpesvirus lymphoma induce long-term endothelial cell reprogramming.PLoS Pathog2019;15:e1007536 PMCID:PMC6361468

[59]

McNamara RP,Myers TA.Nef secretion into extracellular vesicles or exosomes is conserved across human and simian immunodeficiency viruses.mBio2018;9 PMCID:PMC5801467

[60]

Barclay RA,Mensah G.An Omics Approach to extracellular vesicles from HIV-1 infected cells.Cells2019;8:787 PMCID:PMC6724219

[61]

Jung S,Shein M.Efficient and reproducible depletion of hepatitis B virus from plasma derived extracellular vesicles.J Extracell Vesicles2020;10:e12040 PMCID:PMC7754750

[62]

Dogrammatzis C,Deighan C.Diverse populations of extracellular vesicles with opposite functions during herpes simplex virus 1 infection.J Virol2021;95 PMCID:PMC8094966

[63]

Lee Y,Beretov J,Graham P.Recent advances of small extracellular vesicle biomarkers in breast cancer diagnosis and prognosis.Mol Cancer2023;22:33 PMCID:PMC9933347

[64]

Yu W,Roberts D.Exosome-based liquid biopsies in cancer: opportunities and challenges.Ann Oncol2021;32:466-77 PMCID:PMC8268076

[65]

Yang Q,Hu L.An integrative microfluidic device for isolation and ultrasensitive detection of lung cancer-specific exosomes from patient urine.Biosens Bioelectron2020;163:112290

[66]

Wang S,Zhu X,Sun L.Separation of high-purity plasma extracellular vesicles for investigating proteomic signatures in diabetic retinopathy.J Chromatogr A2024;1718:464700

[67]

Hoen E, Cremer T, Gallo RC, Margolis LB. Extracellular vesicles and viruses: Are they close relatives?.Proc Natl Acad Sci U S A2016;113:9155-61 PMCID:PMC4995926

[68]

Jia X,Megger DA.Label-free proteomic analysis of exosomes derived from inducible hepatitis B virus-replicating HepAD38 cell line.Mol Cell Proteomics2017;16:S144-60 PMCID:PMC5393393

[69]

Kaddour H,Lyu Y.HIV-infection and cocaine use regulate semen extracellular vesicles proteome and miRNAome in a manner that mediates strategic monocyte haptotaxis governed by miR-128 network.Cell Mol Life Sci2021;79:5 PMCID:PMC9134786

[70]

Hu Y,Di H.Noninvasive diagnosis of nasopharyngeal carcinoma based on phenotypic profiling of viral and tumor markers on plasma extracellular vesicles.Anal Chem2022;94:9740-9

[71]

Rosell A,von Meijenfeldt F.Patients with COVID-19 have elevated levels of circulating extracellular vesicle tissue factor activity that is associated with severity and mortality-brief report.Arterioscler Thromb Vasc Biol2021;41:878-82

[72]

Balbi C,Bolis S.Circulating extracellular vesicles are endowed with enhanced procoagulant activity in SARS-CoV-2 infection.EBioMedicine2021;67:103369 PMCID:PMC8104913

[73]

Matsuura K,Schechterly C.Circulating let-7 levels in plasma and extracellular vesicles correlate with hepatic fibrosis progression in chronic hepatitis C.Hepatology2016;64:732-45 PMCID:PMC4992455

[74]

Chavda VP,Bezbaruah R.Unveiling the promise: Exosomes as game‐changers in anti‐infective therapy.Exploration

[75]

Tsai SJ,Cacciottolo M.Exosome-mediated mRNA delivery in vivo is safe and can be used to induce SARS-CoV-2 immunity.J Biol Chem2021;297:101266 PMCID:PMC8483990

[76]

Jesus S,Cruz MT.Exosomes as adjuvants for the recombinant hepatitis B antigen: First report.Eur J Pharm Biopharm2018;133:1-11

[77]

Fu Y.Tagged extracellular vesicles with the RBD of the viral spike protein for delivery of antiviral agents against SARS-COV-2 infection.J Control Release2021;335:584-95 PMCID:PMC8172277

[78]

Wang Z,Zhu D.Exosomes decorated with a recombinant SARS-CoV-2 receptor-binding domain as an inhalable COVID-19 vaccine.Nat Biomed Eng2022;6:791-805 PMCID:PMC10782831

[79]

Pei W,Zhu X.Multitargeted Immunomodulatory therapy for viral myocarditis by engineered extracellular vesicles.ACS Nano2024;18:2782-99

[80]

Narayanan A,Das R.Exosomes derived from HIV-1-infected cells contain trans-activation response element RNA.J Biol Chem2013;288:20014-33 PMCID:PMC3707700

[81]

Montaner-Tarbes S,Tarancón V.Targeted-pig trial on safety and immunogenicity of serum-derived extracellular vesicles enriched fractions obtained from Porcine Respiratory and Reproductive virus infections.Sci Rep2018;8:17487 PMCID:PMC6269534

[82]

Gu W,Cai S.Extracellular vesicles incorporating retrovirus-like capsids for the enhanced packaging and systemic delivery of mRNA into neurons.Nat Biomed Eng2024;8:415-26

[83]

Abbott TR,Liu Y.Development of CRISPR as an antiviral strategy to combat SARS-CoV-2 and influenza.Cell2020;181:865-876.e12 PMCID:PMC7189862

[84]

Ahmadi SE,Shahriyary F.Viral vectors and extracellular vesicles: innate delivery systems utilized in CRISPR/Cas-mediated cancer therapy.Cancer Gene Ther2023;30:936-54 PMCID:PMC9971689

[85]

Ilahibaks NF,de Jong OG.Extracellular vesicle-mediated delivery of CRISPR/Cas9 ribonucleoprotein complex targeting proprotein convertase subtilisin-kexin type 9 (Pcsk9) in primary mouse hepatocytes.J Extracell Vesicles2024;13:e12389 PMCID:PMC10774704

[86]

Whitley JA.Engineering extracellular vesicles to deliver CRISPR ribonucleoprotein for gene editing.J Extracell Vesicles2023;12:e12343 PMCID:PMC10507228

[87]

Wan Y,Chen R.Engineered extracellular vesicles efficiently deliver CRISPR-Cas9 ribonucleoprotein (RNP) to inhibit herpes simplex virus1 infection in vitro and in vivo.Acta Pharm Sin B2024;14:1362-79 PMCID:PMC10934336

[88]

Qian X,Fang S.Exosomal microRNAs derived from umbilical mesenchymal stem cells inhibit hepatitis C virus infection.Stem Cells Transl Med2016;5:1190-203 PMCID:PMC4996444

[89]

Welch JL,Schlievert PM,Okeoma CM.Semen exosomes promote transcriptional silencing of HIV-1 by disrupting NF-κB/Sp1/Tat circuitry.J Virol2018;92 PMCID:PMC6189507

[90]

Welch JL,Margolick JB.Effect of prolonged freezing of semen on exosome recovery and biologic activity.Sci Rep2017;7:45034 PMCID:PMC5364471

[91]

Delorme-Axford E,Mouillet JF.Human placental trophoblasts confer viral resistance to recipient cells.Proc Natl Acad Sci U S A2013;110:12048-53 PMCID:PMC3718097

[92]

Teng Y,Zhang X.Plant-derived exosomal microRNAs inhibit lung inflammation induced by exosomes SARS-CoV-2 Nsp12.Mol Ther2021;29:2424-40

[93]

Drayman N,Vistain L.HSV-1 single-cell analysis reveals the activation of anti-viral and developmental programs in distinct sub-populations.Elife2019;8 PMCID:PMC6570482

AI Summary AI Mindmap
PDF

70

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/