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Abstract

Viral egress and transmission have long been described to take place through single free virus particles. However, viruses can also shed into the environment and transmit as populations clustered inside extracellular vesicles (EVs), a process we had first called vesicle-mediated en bloc transmission. These membrane-cloaked virus clusters can originate from a variety of cellular organelles including autophagosomes, plasma membrane, and multivesicular bodies. Their viral cargo can be multiples of nonenveloped or enveloped virus particles or even naked infectious genomes, but egress is always nonlytic, with the cell remaining intact. Here we put forth the thesis that EV-cloaked viral clusters are a distinct form of infectious unit as compared to free single viruses (nonenveloped or enveloped) or even free virus aggregates. We discuss how efficient and prevalent these infectious EVs are in the context of virus-associated diseases and highlight the importance of their proper detection and disinfection for public health.

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2021-10-06
2024-04-16
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Literature Cited

  1. Aguilera ER, Erickson AK, Jesudhasan PR, Robinson CM, Pfeiffer JK. 2017. Plaques formed by mutagenized viral populations have elevated coinfection frequencies. mBio 8:2e02020-16
    [Google Scholar]
  2. Akuma P, Okagu OD, Udenigwe CC. 2019. Naturally occurring exosome vesicles as potential delivery vehicle for bioactive compounds. Front. Sustain. Food Syst. 3:e00023
    [Google Scholar]
  3. Altan-Bonnet N. 2017. Lipid tales of viral replication and transmission. Trends Cell Biol 27:3201–13
    [Google Scholar]
  4. Altan-Bonnet N, Chen Y-H. 2015. Intercellular transmission of viral populations with vesicles. J. Virol. 89:2412242–44
    [Google Scholar]
  5. Altan-Bonnet N, Perales C, Domingo E 2019. Extracellular vesicles: vehicles of en bloc viral transmission. Virus Res 265:143–49
    [Google Scholar]
  6. Amara A, Mercer J 2015. Viral apoptotic mimicry. Nat. Rev. Microbiol. 13:8461–69
    [Google Scholar]
  7. Andreu-Moreno I, Sanjuán R 2018. Collective infection of cells by viral aggregates promotes early viral proliferation and reveals a cellular-level Allee effect. Curr. Biol. 28:203212–19.e4
    [Google Scholar]
  8. Ashley J, Cordy B, Lucia D, Fradkin LG, Budnik V, Thomson T. 2018. Retrovirus-like Gag protein Arc1 binds RNA and traffics across synaptic boutons. Cell 172:1262–74.e11
    [Google Scholar]
  9. Ashraf Malik M, Ishtiyaq Ali Mirza J, Umar M, Manzoor S 2019. CD81+ exosomes play a pivotal role in the establishment of hepatitis C persistent infection and contribute toward the progression of hepatocellular carcinoma. Viral Immunol 32:10453–62
    [Google Scholar]
  10. Badierah RA, Uversky VN, Redwan EM. 2020. Dancing with Trojan horses: an interplay between the extracellular vesicles and viruses. J. Biomol. Struct. Dyn. https://doi.org/10.1080/07391102.2020.1756409
    [Crossref] [Google Scholar]
  11. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G et al. 2012. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14:7677–85
    [Google Scholar]
  12. Balaj L, Lessard R, Dai L, Cho Y-J, Pomeroy SL et al. 2011. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2:180
    [Google Scholar]
  13. Beaton AR, Rodriguez J, Reddy YK, Roy P 2002. The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. PNAS 99:2013154–59
    [Google Scholar]
  14. Bello-Morales R, López-Guerrero JA. 2018. Extracellular vesicles in herpes viral spread and immune evasion. Front. Microbiol. 9:e02572
    [Google Scholar]
  15. Bello-Morales R, Praena B, de la Nuez C, Rejas MT, Guerra M et al. 2018. Role of microvesicles in the spread of herpes simplex virus 1 in oligodendrocytic cells. J. Virol. 92:10e00088-18
    [Google Scholar]
  16. Bello-Morales R, Ripa I, López-Guerrero JA. 2020. Extracellular vesicles in viral spread and antiviral response. Viruses 12:6623
    [Google Scholar]
  17. Bird SW, Maynard ND, Covert MW, Kirkegaard K 2014. Nonlytic viral spread enhanced by autophagy components. PNAS 111:3613081–86
    [Google Scholar]
  18. Birge RB, Boeltz S, Kumar S, Carlson J, Wanderley J et al. 2016. Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer. Cell Death Differ 23:6962–78
    [Google Scholar]
  19. Blachere FM, Lindsley WG, McMillen CM, Beezhold DH, Fisher EM et al. 2018. Assessment of influenza virus exposure and recovery from contaminated surgical masks and N95 respirators. J. Virol. Methods 260:98–106
    [Google Scholar]
  20. Blackwell JH, Wool S, Kosikowski FV. 1981. Vesicular exocytosis of foot-and-mouth disease virus from mammary gland secretory epithelium of infected cows. J. Gen. Virol. 56:1207–12
    [Google Scholar]
  21. Bou J-V, Geller R, Sanjuán R. 2019. Membrane-associated enteroviruses undergo intercellular transmission as pools of sibling viral genomes. Cell Rep 29:3714–23.e4
    [Google Scholar]
  22. Boukouris S, Mathivanan S. 2015. Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteom. Clin. Appl. 9:3–4358–67
    [Google Scholar]
  23. Bukong TN, Momen-Heravi F, Kodys K, Bala S, Szabo G. 2014. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLOS Pathogens 10:10e1004424
    [Google Scholar]
  24. Cai S, Luo B, Jiang P, Zhou X, Lan F et al. 2018. Immuno-modified superparamagnetic nanoparticles via host–guest interactions for high-purity capture and mild release of exosomes. Nanoscale 10:2914280–89
    [Google Scholar]
  25. Cannon JL, Aydin A, Mann AN, Bolton SL, Zhao T, Doyle MP. 2012. Efficacy of a levulinic acid plus sodium dodecyl sulfate–based sanitizer on inactivation of human norovirus surrogates. J. Food Prot. 75:81532–35
    [Google Scholar]
  26. Cao B, Parnell LA, Diamond MS, Mysorekar IU. 2017. Inhibition of autophagy limits vertical transmission of Zika virus in pregnant mice. J. Exp. Med. 214:82303–13
    [Google Scholar]
  27. Caobi A, Nair M, Raymond AD. 2020. Extracellular vesicles in the pathogenesis of viral infections in humans. Viruses 12:101200
    [Google Scholar]
  28. Carocci M, Bakkali-Kassimi L. 2012. The encephalomyocarditis virus. Virulence 3:4351–67
    [Google Scholar]
  29. Caruso S, Poon IKH. 2018. Apoptotic cell-derived extracellular vesicles: more than just debris. Front. Immunol. 9:1486
    [Google Scholar]
  30. CDC (Centers Dis. Control Prev.) 2020. Global immunization. US Department of Health and Human Services https://www.cdc.gov/polio/
    [Google Scholar]
  31. Charrin S, Jouannet S, Boucheix C, Rubinstein E. 2014. Tetraspanins at a glance. J. Cell Sci. 127:173641–48
    [Google Scholar]
  32. Chen Y-H, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:4619–30
    [Google Scholar]
  33. Cheung LS, Sahloul S, Orozaliev A, Song Y-A 2018. Rapid detection and trapping of extracellular vesicles by electrokinetic concentration for liquid biopsy on chip. Micromachines 9:6306
    [Google Scholar]
  34. Cocucci E, Racchetti G, Meldolesi J. 2009. Shedding microvesicles: artefacts no more. Trends Cell Biol 19:243–51
    [Google Scholar]
  35. Colombo M, Moita C, van Niel G, Kowal J, Vigneron J et al. 2013. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126:245553–65
    [Google Scholar]
  36. Combes GB, Varner DD, Schroeder F, Burghardt RC, Blanchard TL. 2000. Effect of cholesterol on the motility and plasma membrane integrity of frozen equine spermatozoa after thawing. J. Reprod. Fertil. Suppl.56127–32
    [Google Scholar]
  37. Cornick S, Kumar M, Moreau F, Gaisano H, Chadee K. 2019. VAMP8-mediated MUC2 mucin exocytosis from colonic goblet cells maintains innate intestinal homeostasis. Nat. Commun. 10:4306
    [Google Scholar]
  38. Corona Velazquez A, Corona AK, Klein KA, Jackson WT 2018. Poliovirus induces autophagic signaling independent of the ULK1 complex. Autophagy 14:71201–13
    [Google Scholar]
  39. Cortez V, Boyd DF, Crawford JC, Sharp B, Livingston B et al. 2020. Astrovirus infects actively secreting goblet cells and alters the gut mucus barrier. Nat. Commun. 11:2097
    [Google Scholar]
  40. Cortez V, Meliopoulos VA, Karlsson EA, Hargest V, Johnson C, Schultz-Cherry S. 2017. Astrovirus biology and pathogenesis. Annu. Rev. Virol 4:327–48
    [Google Scholar]
  41. Cuevas JM, Durán-Moreno M, Sanjuán R. 2017. Multi-virion infectious units arise from free viral particles in an enveloped virus. Nat. Microbiol. 2:17078
    [Google Scholar]
  42. Darnell MER, Subbarao K, Feinstone SM, Taylor DR. 2004. Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV. J. Virol. Methods 121:185–91
    [Google Scholar]
  43. Das A, Hirai-Yuki A, González-López O, Rhein B, Moller-Tank S et al. 2017. TIM1 (HAVCR1) is not essential for cellular entry of either quasi-enveloped or naked hepatitis A virions. mBio 8:5e00969-17
    [Google Scholar]
  44. Das A, Maury W, Lemon SM 2019. TIM1 (HAVCR1): an essential “receptor” or an “accessory attachment factor” for hepatitis A virus?. J. Virol. 93:11e01793-18
    [Google Scholar]
  45. de Toledo Martins S, Alves LR 2020. Extracellular vesicles in viral infections: two sides of the same coin?. Front. Cell Infect. Microbiol 10:e593170
    [Google Scholar]
  46. del Rocío Banos-Lara M, Méndez E 2010. Role of individual caspases induced by astrovirus on the processing of its structural protein and its release from the cell through a non-lytic mechanism. Virology 401:2322–32
    [Google Scholar]
  47. Deschamps T, Kalamvoki M. 2018. Extracellular vesicles released by herpes simplex virus 1-infected cells block virus replication in recipient cells in a STING-dependent manner. J. Virol. 92:18e01102-18
    [Google Scholar]
  48. Ding Q, Heller B, Capuccino JMV, Song B, Nimgaonkar I et al. 2017. Hepatitis E virus ORF3 is a functional ion channel required for release of infectious particles. PNAS 114:51147–52
    [Google Scholar]
  49. Domingo E, Holland JJ. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151–78
    [Google Scholar]
  50. Dulbecco R, Vogt M. 1953. Some problems of animal virology as studied by the plaque technique. Cold Spring Harb. Symp. Quant. Biol. 18:273–79
    [Google Scholar]
  51. Erickson AK, Jesudhasan PR, Mayer MJ, Narbad A, Winter SE, Pfeiffer JK. 2018. Bacteria facilitate enteric virus co-infection of mammalian cells and promote genetic recombination. Cell Host Microbe 23:177–88.e5
    [Google Scholar]
  52. EPA (Environ. Prot. Agency) 2021. Drinking water. US Environmental Protection Agency. https://www.epa.ie/our-services/compliance–enforcement/drinking-water/
    [Google Scholar]
  53. Erlendsson S, Morado DR, Cullen HB, Feschotte C, Shepherd JD, Briggs JAG. 2020. Structures of virus-like capsids formed by the Drosophila neuronal Arc proteins. Nat. Neurosci. 23:2172–75
    [Google Scholar]
  54. Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:7445367–71
    [Google Scholar]
  55. Feng Z, Hirai-Yuki A, McKnight KL, Lemon SM. 2014. Naked viruses that aren't always naked: quasi-enveloped agents of acute hepatitis. Annu. Rev. Virol. 1:539–60
    [Google Scholar]
  56. Feng Z, Li Y, McKnight KL, Hensley L, Lanford RE et al. 2015. Human pDCs preferentially sense enveloped hepatitis A virions. J. Clin. Invest. 125:1169–76
    [Google Scholar]
  57. Friedrich R, Block S, Alizadehheidari M, Heider S, Fritzsche J et al. 2017. A nano flow cytometer for single lipid vesicle analysis. Lab Chip 17:5830–41
    [Google Scholar]
  58. Gardiner C, Vizio DD, Sahoo S, Théry C, Witwer KW et al. 2016. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J. Extracell. Vesicles 5:32945
    [Google Scholar]
  59. Ge Q, Zhou Y, Lu J, Bai Y, Xie X, Lu Z. 2014. miRNA in plasma exosome is stable under different storage conditions. Molecules 19:21568–75
    [Google Scholar]
  60. Giannecchini S. 2020. Evidence of the mechanism by which polyomaviruses exploit the extracellular vesicle delivery system during infection. Viruses 12:6585
    [Google Scholar]
  61. González-López O, Rivera-Serrano EE, Hu F, Hensley L, McKnight KL et al. 2018. Redundant late domain functions of tandem VP2 YPX3L motifs in nonlytic cellular egress of quasi-enveloped hepatitis A virus. J. Virol. 92:23e01308-18
    [Google Scholar]
  62. Gouttenoire J, Pollán A, Abrami L, Oechslin N, Mauron J et al. 2018. Palmitoylation mediates membrane association of hepatitis E virus ORF3 protein and is required for infectious particle secretion. PLOS Pathog 14:12e1007471
    [Google Scholar]
  63. Gu J, Wu J, Fang D, Qiu Y, Zou X et al. 2019. Exosomes cloak the virion to transmit Enterovirus 71 non-lytically. Virulence 11:132–38
    [Google Scholar]
  64. Handala L, Blanchard E, Raynal P-I, Roingeard P, Morel V et al. 2020. BK polyomavirus hijacks extracellular vesicles for en bloc transmission. J. Virol. 94:6e01834-19
    [Google Scholar]
  65. Harder T, Scheiffele P, Verkade P, Simons K. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:4929–42
    [Google Scholar]
  66. Helle F, Handala L, Bentz M, Duverlie G, Brochot E. 2020. Intercellular transmission of naked viruses through extracellular vesicles: focus on polyomaviruses. Viruses 12:101086
    [Google Scholar]
  67. Hsu N-Y, Ilnytska O, Belov G, Santiana M, Chen Y-H et al. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:5799–811
    [Google Scholar]
  68. Huang S-C, Chang C-L, Wang P-S, Tsai Y, Liu H-S. 2009. Enterovirus 71-induced autophagy detected in vitro and in vivo promotes viral replication. J. Med. Virol. 81:71241–52
    [Google Scholar]
  69. Hurley JH. 2008. ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20:14–11
    [Google Scholar]
  70. Hyatt AD, Zhao Y, Roy P. 1993. Release of bluetongue virus-like particles from insect cells is mediated by BTV nonstructural protein NS3/NS3A. Virology 193:2592–603
    [Google Scholar]
  71. Ilnytska O, Santiana M, Hsu N-Y, Du W-L, Chen Y-H et al. 2013. Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication. Cell Host Microbe 14:3281–93
    [Google Scholar]
  72. Irion U, St Johnston D 2007. Bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445:7127554–58
    [Google Scholar]
  73. Jackson WT, Giddings TH, Taylor MP, Mulinyawe S, Rabinovitch M et al. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLOS Biol 3:50030156
    [Google Scholar]
  74. Jemielity S, Wang JJ, Chan YK, Ahmed AA, Li W et al. 2013. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLOS Pathog 9:3e1003232
    [Google Scholar]
  75. Jiang W, Ma P, Deng L, Liu Z, Wang X et al. 2020. Hepatitis A virus structural protein pX interacts with ALIX and promotes the secretion of virions and foreign proteins through exosome-like vesicles. J. Extracell. Vesicles 9:11716513
    [Google Scholar]
  76. Kalamvoki M, Du T, Roizman B 2014. Cells infected with herpes simplex virus 1 export to uninfected cells exosomes containing STING, viral mRNAs, and microRNAs. PNAS 111:46E4991–96
    [Google Scholar]
  77. Kalra H, Adda CG, Liem M, Ang C-S, Mechler A et al. 2013. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics 13:223354–64
    [Google Scholar]
  78. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P et al. 2012. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLOS Biol 10:12e1001450
    [Google Scholar]
  79. Keerthikumar S, Chisanga D, Ariyaratne D, Al Saffar H, Anand S et al. 2016. ExoCarta: a web-based compendium of exosomal cargo. J. Mol. Biol. 428:4688–92
    [Google Scholar]
  80. Kim D-K, Lee J, Kim SR, Choi D-S, Yoon YJ et al. 2015. EVpedia: a community web portal for extracellular vesicles research. Bioinformatics 31:6933–39
    [Google Scholar]
  81. Kim JG, Yousef AE, Dave S 1999. Application of ozone for enhancing the microbiological safety and quality of foods: a review. J. Food Prot. 62:91071–87
    [Google Scholar]
  82. Kirkegaard K, Jackson WT. 2005. Topology of double-membraned vesicles and the opportunity for non-lytic release of cytoplasm. Autophagy 1:3182–84
    [Google Scholar]
  83. Kowal J, Arras G, Colombo M, Jouve M, Morath JP et al. 2016. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. PNAS 113:8E968–77
    [Google Scholar]
  84. Kumeda N, Ogawa Y, Akimoto Y, Kawakami H, Tsujimoto M, Yanoshita R. 2017. Characterization of membrane integrity and morphological stability of human salivary exosomes. Biol. Pharm. Bull. 40:81183–91
    [Google Scholar]
  85. Labadie T, Roy P. 2020. A non-enveloped arbovirus released in lysosome-derived extracellular vesicles induces super-infection exclusion. PLOS Pathog 16:10e1009015
    [Google Scholar]
  86. Labadie T, Sullivan E, Roy P 2020. Multiple routes of bluetongue virus egress. . Microorganisms 8:7965
    [Google Scholar]
  87. Lässer C, Alikhani VS, Ekström K, Eldh M, Paredes PT et al. 2011. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J. Transl. Med. 9:9
    [Google Scholar]
  88. Liangsupree T, Multia E, Riekkola M-L. 2021. Modern isolation and separation techniques for extracellular vesicles. J. Chromatogr. A 1636:461773
    [Google Scholar]
  89. Lindenbach BD, Rice CM. 2013. The ins and outs of hepatitis C virus entry and assembly. Nat. Rev. Microbiol. 11:10688–700
    [Google Scholar]
  90. Longatti A, Boyd B, Chisari FV. 2015. Virion-independent transfer of replication-competent hepatitis C virus RNA between permissive cells. J. Virol. 89:52956–61
    [Google Scholar]
  91. McKnight KL, Xie L, González-López O, Rivera-Serrano EE, Chen X, Lemon SM 2017. Protein composition of the hepatitis A virus quasi-envelope. PNAS 114:256587–92
    [Google Scholar]
  92. McNamara RP, Dittmer DP. 2020a. Extracellular vesicles in virus infection and pathogenesis. Curr. Opin. Virol. 44:129–38
    [Google Scholar]
  93. McNamara RP, Dittmer DP. 2020b. Modern techniques for the isolation of extracellular vesicles and viruses. J. Neuroimmune Pharmacol. 15:3459–72
    [Google Scholar]
  94. Melentijevic I, Toth ML, Arnold ML, Guasp RJ, Harinath G et al. 2017. C. elegans neurons jettison protein aggregates and mitochondria under neurotoxic stress. Nature 542:7641367–71
    [Google Scholar]
  95. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:5363–74
    [Google Scholar]
  96. Minciacchi VR, Spinelli C, Reis-Sobreiro M, Cavallini L, You S et al. 2017. MYC mediates large oncosome-induced fibroblast reprogramming in prostate cancer. Cancer Res 77:92306–17
    [Google Scholar]
  97. Moens U, Krumbholz A, Ehlers B, Zell R, Johne R et al. 2017. Biology, evolution, and medical importance of polyomaviruses: an update. Infect. Genet. Evol. 54:18–38
    [Google Scholar]
  98. Mohamud Y, Shi J, Qu J, Poon T, Xue YC et al. 2018. Enteroviral infection inhibits autophagic flux via disruption of the SNARE complex to enhance viral replication. Cell Rep 22:123292–303
    [Google Scholar]
  99. Mohl B-P, Kerviel A, Labadie T, Matsuo E, Roy P. 2020. Differential localization of structural and non-structural proteins during the bluetongue virus replication cycle. Viruses 12:3343
    [Google Scholar]
  100. Moller-Tank S, Maury W 2014. Phosphatidylserine receptors: enhancers of enveloped virus entry and infection. Virology 468–470:565–80
    [Google Scholar]
  101. Montaner-Tarbes S, Borrás FE, Montoya M, Fraile L, del Portillo HA. 2016. Serum-derived exosomes from non-viremic animals previously exposed to the porcine respiratory and reproductive virus contain antigenic viral proteins. Veterinary Res 47:59
    [Google Scholar]
  102. Montaner-Tarbes S, Novell E, Tarancón V, Borrás FE, Montoya M et al. 2018. Targeted-pig trial on safety and immunogenicity of serum-derived extracellular vesicles enriched fractions obtained from Porcine Respiratory and Reproductive virus infections. Sci. Rep. 8:17487
    [Google Scholar]
  103. Morales-Kastresana A, Musich TA, Welsh JA, Telford W, Demberg T et al. 2019. High-fidelity detection and sorting of nanoscale vesicles in viral disease and cancer. J. Extracell. Vesicles 8:11597603
    [Google Scholar]
  104. Morizono K, Chen ISY. 2014. Role of phosphatidylserine receptors in enveloped virus infection. J. Virol. 88:84275–90
    [Google Scholar]
  105. Morozov VA, Lagaye S. 2018. Hepatitis C virus: morphogenesis, infection and therapy. World J. Hepatol. 10:2186–212
    [Google Scholar]
  106. Morris-Love J, Gee GV, O'Hara BA, Assetta B, Atkinson AL et al. 2019. JC polyomavirus uses extracellular vesicles to infect target cells. mBio 10:2e00379-19
    [Google Scholar]
  107. Mothes W, Sherer NM, Jin J, Zhong P 2010. Virus cell-to-cell transmission. J. Virol. 84:178360–68
    [Google Scholar]
  108. Mulcahy LA, Pink RC, Carter DRF. 2014. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles 3:124641
    [Google Scholar]
  109. Mutsafi Y, Altan-Bonnet N. 2018. Enterovirus transmission by secretory autophagy. Viruses 10:3139
    [Google Scholar]
  110. Nagashima S, Jirintai S, Takahashi M, Kobayashi T, Tanggis et al. 2014. Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J. Gen. Virol. 95:102166–75
    [Google Scholar]
  111. Nagashima S, Takahashi M, Jirintai S, Tanaka T, Nishizawa T et al. 2011a. Tumour susceptibility gene 101 and the vacuolar protein sorting pathway are required for the release of hepatitis E virions. J. Gen. Virol. 92:122838–48
    [Google Scholar]
  112. Nagashima S, Takahashi M, Jirintai S, Tanaka T, Yamada K et al. 2011b. A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J. Gen. Virol. 92:2269–78
    [Google Scholar]
  113. Nakai W, Yoshida T, Diez D, Miyatake Y, Nishibu T et al. 2016. A novel affinity-based method for the isolation of highly purified extracellular vesicles. Sci. Rep. 6:33935
    [Google Scholar]
  114. Nieto-Torres JL, Leidal AM, Debnath J, Hansen M. 2021. Beyond autophagy: the expanding roles of ATG8 proteins. Trends Biochem. Sci 46:867286
    [Google Scholar]
  115. Nieuwland R, Falcón-Pérez JM, Théry C, Witwer KW. 2020. Rigor and standardization of extracellular vesicle research: paving the road towards robustness. J. Extracell. Vesicles 10:2e12037
    [Google Scholar]
  116. O'Hara BA, Morris-Love J, Gee GV, Haley SA, Atwood WJ. 2020. JC virus infected choroid plexus epithelial cells produce extracellular vesicles that infect glial cells independently of the virus attachment receptor. PLOS Pathog 16:3e1008371
    [Google Scholar]
  117. Orchard RC, Wilen CB, Doench JG, Baldridge MT, McCune BT et al. 2016. Discovery of a proteinaceous cellular receptor for a norovirus. Science 353:6302933–36
    [Google Scholar]
  118. Osteikoetxea X, Sódar B, Németh A, Szabó-Taylor K, Pálóczi K et al. 2015. Differential detergent sensitivity of extracellular vesicle subpopulations. Org. Biomol. Chem. 13:389775–82
    [Google Scholar]
  119. Panou M-M, Prescott EL, Hurdiss DL, Swinscoe G, Hollinshead M et al. 2018. Agnoprotein is an essential egress factor during BK polyomavirus infection. Int. J. Mol. Sci. 19:3902
    [Google Scholar]
  120. Papahadjopoulos D, Jacobson K, Nir S, Isac T. 1973. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim. Biophys. Acta 311:3330–48
    [Google Scholar]
  121. Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV et al. 2018. The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell 172:1–2275–88.e18
    [Google Scholar]
  122. Pegtel DM, Gould SJ. 2019. Exosomes. Annu. Rev. Biochem. 88:487–514
    [Google Scholar]
  123. Pelletier JPR, Transue S, Snyder EL. 2006. Pathogen inactivation techniques. Best Pract. Res. Clin. Haematol. 19:1205–42
    [Google Scholar]
  124. Perez-Hernandez D, Gutiérrez-Vázquez C, Jorge I, López-Martín S, Ursa A et al. 2013. The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J. Biol. Chem. 288:1711649–61
    [Google Scholar]
  125. Pieters BCH, Arntz OJ, Bennink MB, Broeren MGA, van Caam APM et al. 2015. Commercial cow milk contains physically stable extracellular vesicles expressing immunoregulatory TGF-β. PLOS ONE 10:3e0121123
    [Google Scholar]
  126. Pileri E, Mateu E. 2016. Review on the transmission porcine reproductive and respiratory syndrome virus between pigs and farms and impact on vaccination. Veterinary Res 47:108
    [Google Scholar]
  127. Ponpuak M, Mandell M, Kimura T, Chauhan S, Cleyrat C, Deretic V 2015. Secretory autophagy. Curr. Opin. Cell Biol 35:106–16
    [Google Scholar]
  128. Raab-Traub N, Dittmer DP. 2017. Viral effects on the content and function of extracellular vesicles. Nat. Rev. Microbiol. 15:9559–72
    [Google Scholar]
  129. Rachmadi AT, Kitajima M, Kato T, Kato H, Okabe S, Sano D. 2020. Required chlorination doses to fulfill the credit value for disinfection of enteric viruses in water: a critical review. Environ. Sci. Technol. 54:42068–77
    [Google Scholar]
  130. Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q et al. 2013. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. PNAS 110:3213109–13
    [Google Scholar]
  131. Reyes-Ruiz JM, Osuna-Ramos JF, De Jesús-González LA, Hurtado-Monzón AM, Farfan-Morales CN et al. 2019. Isolation and characterization of exosomes released from mosquito cells infected with dengue virus. Virus Res 266:1–14
    [Google Scholar]
  132. Reyes-Ruiz JM, Osuna-Ramos JF, De Jesús-González LA, Palacios-Rápalo SN, Cordero-Rivera CD et al. 2020. The regulation of flavivirus infection by hijacking exosome-mediated cell–cell communication: new insights on virus–host interactions. Viruses 12:7765
    [Google Scholar]
  133. Richards AL, Jackson WT. 2012. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLOS Pathog 8:11e1003046
    [Google Scholar]
  134. Rivera-Serrano EE, González-López O, Das A, Lemon SM 2019. Cellular entry and uncoating of naked and quasi-enveloped human hepatoviruses. eLife 8:e43983
    [Google Scholar]
  135. Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. 2014. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog 10:4e1004045
    [Google Scholar]
  136. Rothlin CV, Carrera-Silva EA, Bosurgi L, Ghosh S. 2015. TAM receptor signaling in immune homeostasis. Annu. Rev. Immunol. 33:1355–91
    [Google Scholar]
  137. Royo F, Théry C, Falcón-Pérez JM, Nieuwland R, Witwer KW. 2020. Methods for separation and characterization of extracellular vesicles: results of a worldwide survey performed by the ISEV rigor and standardization subcommittee. Cells 9:91955
    [Google Scholar]
  138. Sadeghipour S, Mathias RA. 2017. Herpesviruses hijack host exosomes for viral pathogenesis. Semin. Cell Dev. Biol. 67:91–100
    [Google Scholar]
  139. Sanjuán R. 2018. Collective properties of viral infectivity. Curr. Opin. Virol. 33:1–6
    [Google Scholar]
  140. Santiana M, Altan-Bonnet N. 2019. Insane in the membrane: glial extracellular vesicles transmit polyomaviruses. mBio 10:3e01024-19
    [Google Scholar]
  141. Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. 2018. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 24:2208–20.e8
    [Google Scholar]
  142. Saribas AS, Coric P, Bouaziz S, Safak M. 2019. Expression of novel proteins by polyomaviruses and recent advances in the structural and functional features of agnoprotein of JC virus, BK virus, and simian virus 40. J. Cell Physiol. 234:68295–315
    [Google Scholar]
  143. Schaefer L. 2014. Complexity of danger: the diverse nature of damage-associated molecular patterns. J. Biol. Chem. 289:5135237–45
    [Google Scholar]
  144. Schlegel A, Giddings TH, Ladinsky MS, Kirkegaard K. 1996. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 70:106576–88
    [Google Scholar]
  145. Shi Y, He X, Zhu G, Tu H, Liu Z et al. 2015. Coxsackievirus A16 elicits incomplete autophagy involving the mTOR and ERK pathways. PLOS ONE 10:4e0122109
    [Google Scholar]
  146. Shirogane Y, Watanabe S, Yanagi Y. 2019. Cooperation between different variants: a unique potential for virus evolution. Virus Res 264:68–73
    [Google Scholar]
  147. Silvas JA, Popov VL, Paulucci-Holthauzen A, Aguilar PV. 2016. Extracellular vesicles mediate receptor-independent transmission of novel tick-borne bunyavirus. J. Virol. 90:2873–86
    [Google Scholar]
  148. Silverman AI, Boehm AB. 2020. Systematic review and meta-analysis of the persistence and disinfection of human coronaviruses and their viral surrogates in water and wastewater. Environ. Sci. Technol. Lett. 7:8544–53
    [Google Scholar]
  149. Sin J, McIntyre L, Stotland A, Feuer R, Gottlieb RA. 2017. Coxsackievirus B escapes the infected cell in ejected mitophagosomes. J. Virol. 91:24e01347-17
    [Google Scholar]
  150. Skotland T, Hessvik NP, Sandvig K, Llorente A. 2019. Exosomal lipid composition and the role of ether lipids and phosphoinositides in exosome biology. J. Lipid Res. 60:19–18
    [Google Scholar]
  151. Skotland T, Sagini K, Sandvig K, Llorente A. 2020. An emerging focus on lipids in extracellular vesicles. Adv. Drug Deliv. Rev. 159:308–21
    [Google Scholar]
  152. Skotland T, Sandvig K, Llorente A. 2017. Lipids in exosomes: current knowledge and the way forward. Prog. Lipid Res. 66:30–41
    [Google Scholar]
  153. Slack J, Arif BM. 2007. The baculoviruses occlusion-derived virus: virion structure and function. Adv. Virus Res. 69:99–165
    [Google Scholar]
  154. Sokolova V, Ludwig A-K, Hornung S, Rotan O, Horn PA et al. 2011. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf. B Biointerfaces 87:1146–50
    [Google Scholar]
  155. Souza Arantes T, Lima Rodrigues RA, dos Santos Silva LK, Pereira Oliveira G, de Souza HL et al. 2016. The large Marseillevirus explores different entry pathways by forming giant infectious vesicles. J. Virol. 90:115246–55
    [Google Scholar]
  156. Stiefel P, Schmidt FI, Dörig P, Behr P, Zambelli T et al. 2012. Cooperative vaccinia infection demonstrated at the single-cell level using FluidFM. Nano Lett 12:84219–27
    [Google Scholar]
  157. Tamai K, Tanaka N, Nakano T, Kakazu E, Kondo Y et al. 2010. Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem. Biophys. Res. Commun. 399:3384–90
    [Google Scholar]
  158. Tavano S, Heisenberg C-P. 2019. Migrasomes take center stage. Nat. Cell Biol. 21:8918–20
    [Google Scholar]
  159. Théry C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9:8581–93
    [Google Scholar]
  160. Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD et al. 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 7:11535750
    [Google Scholar]
  161. Too IHK, Yeo H, Sessions OM, Yan B, Libau EA et al. 2016. Enterovirus 71 infection of motor neuron-like NSC-34 cells undergoes a non-lytic exit pathway. Sci. Rep. 6:36983
    [Google Scholar]
  162. Urbanelli L, Buratta S, Tancini B, Sagini K, Delo F et al. 2019. The role of extracellular vesicles in viral infection and transmission. Vaccines 7:3102
    [Google Scholar]
  163. Uygur B, Melikov K, Arakelyan A, Margolis LB, Chernomordik LV. 2019. Syncytin 1 dependent horizontal transfer of marker genes from retrovirally transduced cells. Sci. Rep. 9:17637
    [Google Scholar]
  164. van der Grein SG, Defourny KAY, Rabouw HH, Galiveti CR, Langereis MA et al. 2019. Picornavirus infection induces temporal release of multiple extracellular vesicle subsets that differ in molecular composition and infectious potential. PLOS Pathog 15:2e1007594
    [Google Scholar]
  165. Van Deun J, Mestdagh P, Agostinis P, Akay Ö, Anand S et al. 2017. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat. Methods 14:3228–32
    [Google Scholar]
  166. van Dongen HM, Masoumi N, Witwer KW, Pegtel DM. 2016. Extracellular vesicles exploit viral entry routes for cargo delivery. Microbiol. Mol. Biol. Rev. 80:2369–86
    [Google Scholar]
  167. van Niel G, D'Angelo G, Raposo G 2018. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19:4213–28
    [Google Scholar]
  168. Vargas A, Zhou S, Éthier-Chiasson M, Flipo D, Lafond J et al. 2014. Syncytin proteins incorporated in placenta exosomes are important for cell uptake and show variation in abundance in serum exosomes from patients with preeclampsia. FASEB J 28:83703–19
    [Google Scholar]
  169. Vignuzzi M, López CB. 2019. Defective viral genomes are key drivers of the virus–host interaction. Nat. Microbiol. 4:71075–87
    [Google Scholar]
  170. Vitallé J, Terrén I, Orrantia A, Zenarruzabeitia O, Borrego F. 2019. CD300 receptor family in viral infections. Eur. J. Immunol. 49:3364–74
    [Google Scholar]
  171. Vora A, Zhou W, Londono-Renteria B, Woodson M, Sherman MB et al. 2018. Arthropod EVs mediate dengue virus transmission through interaction with a tetraspanin domain containing glycoprotein Tsp29Fb. PNAS 115:28E6604–13
    [Google Scholar]
  172. Wang T, Fang L, Zhao F, Wang D, Xiao S 2018. Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J. Virol. 92:4e01734-17
    [Google Scholar]
  173. Welch SR, Davies KA, Buczkowski H, Hettiarachchi N, Green N et al. 2020. Analysis of inactivation of SARS-CoV-2 by specimen transport media, nucleic acid extraction reagents, detergents, and fixatives. J. Clin. Microbiol. 58:11e01713-20
    [Google Scholar]
  174. WHO (World Health Org.) 2021. Poliomyelitis (polio). World Health Organization. https://www.who.int/health-topics/poliomyelitis
    [Google Scholar]
  175. Wirblich C, Bhattacharya B, Roy P. 2006. Nonstructural protein 3 of bluetongue virus assists virus release by recruiting ESCRT-I protein Tsg101. J. Virol. 80:1460–73
    [Google Scholar]
  176. Yin X, Ambardekar C, Lu Y, Feng Z. 2016. Distinct entry mechanisms for nonenveloped and quasi-enveloped hepatitis E viruses. J. Virol. 90:84232–42
    [Google Scholar]
  177. Zaritsky LA, Bedsaul JR, Zoon KC. 2015. Virus multiplicity of infection affects type I interferon subtype induction profiles and interferon-stimulated genes. J. Virol. 89:2211534–48
    [Google Scholar]
  178. Zhang K, Xu S, Shi X, Xu G, Shen C et al. 2019. Exosomes-mediated transmission of foot-and-mouth disease virus in vivo and in vitro. Veterinary Microbiol 233:164–73
    [Google Scholar]
  179. Zhang M, Ghosh S, Kumar M, Santiana M, Bleck KEC et al. 2021. Emerging pathogenic unit of vesicle-cloaked murine norovirus clusters is resistant to environmental stresses and UV254 disinfection. Environ. Sci. Technol. 55:96197–205
    [Google Scholar]
  180. Zhang W, Wu J, Ward MD, Yang S, Chuang Y-A et al. 2015. Structural basis of Arc binding to synaptic proteins: implications for cognitive disease. Neuron 86:2490–500
    [Google Scholar]
  181. Zhou W, Woodson M, Neupane B, Bai F, Sherman MB et al. 2018. Exosomes serve as novel modes of tick-borne flavivirus transmission from arthropod to human cells and facilitates dissemination of viral RNA and proteins to the vertebrate neuronal cells. PLOS Pathog 14:e1006764
    [Google Scholar]
  182. Zhou W, Woodson M, Sherman MB, Neelakanta G, Sultana H. 2019. Exosomes mediate Zika virus transmission through SMPD3 neutral sphingomyelinase in cortical neurons. Emerg. Microbes Infections 8:1307–26
    [Google Scholar]
  183. Zhu X, He Z, Yuan J, Wen W, Huang X et al. 2015. IFITM3-containing exosome as a novel mediator for anti-viral response in dengue virus infection. Cell. Microbiol. 17:1105–18
    [Google Scholar]
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