Extracellular vesicles originating from autophagy mediate an antibody-resistant spread of classical swine fever virus in cell culture

References

• Lindenbach BD, Murray CL, Thiel HJ. Flaviviridae. In: Knipe DM, Howley PM, Cohen JI, et al., editors. Field’s virology. vol. 2. 6th ed. Philadelphia (PA): Lippincott Williams & Wilkins; 2013. p. 712–746.
   Google Scholar
• Tu C, Lu Z, Li H, et al. Phylogenetic comparison of classical swine fever virus in China. Virus Res. 2001;81(1–2):29–37.
   PubMed Web of Science ®Google Scholar
• Lefkowitz EJ, Dempsey DM, Hendrickson RC, et al. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 2018;46:D708–D717.
   PubMed Web of Science ®Google Scholar
• Thiel HJ, Stark R, Weiland E, et al. Hog cholera virus: molecular composition of virions from a pestivirus. J Virol. 1991;65(9):4705–4712.
   PubMed Web of Science ®Google Scholar
• Coronado L, Bohórquez JA, Muñoz-González S, et al. Investigation of chronic and persistent classical swine fever infections under field conditions and their impact on vaccine efficacy. BMC Vet Res. 2019;15(1):247.
   PubMedGoogle Scholar
• Zhong P, Agosto LM, Munro JB, et al. Cell-to-cell transmission of viruses. Curr Opin Virol. 2013;3(1):44–50.
   PubMed Web of Science ®Google Scholar
• Mothes W, Sherer NM, Jin J, et al. Virus cell-to-cell transmission. J Virol. 2010;84(17):8360–8368.
   PubMed Web of Science ®Google Scholar
• Chen YH, Du W, Hagemeijer MC, et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell. 2015;160(4):619–630.
   PubMed Web of Science ®Google Scholar
• Aydin H, Cook JD, Lee JE. Crystal structures of beta- and gammaretrovirus fusion proteins reveal a role for electrostatic stapling in viral entry. J Virol. 2014;88(1):143–153.
   PubMed Web of Science ®Google Scholar
• Bose S, Song AS, Jardetzky TS, et al. Fusion activation through attachment protein stalk domains indicates a conserved core mechanism of paramyxovirus entry into cells. J Virol. 2014;88(8):3925–3941.
   PubMed Web of Science ®Google Scholar
• Johnson DC, Huber MT. Directed egress of animal viruses promotes cell-to-cell spread. J Virol. 2002;76(1):1–8.
   PubMed Web of Science ®Google Scholar
• Maas S, Breakefield XO, Weaver AM. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 2017;27(3):172–188.
   PubMed Web of Science ®Google Scholar
• Pant S, Hilton H, Burczynski ME. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem Pharmacol. 2012;83(11):1484–1494.
   PubMed Web of Science ®Google Scholar
• Wang T, Fang L, Zhao F, et al. Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J Virol. 2018;92:e01734–17.
   PubMed Web of Science ®Google Scholar
• Yang Y, Han Q, Hou Z, et al. Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction. Cell Mol Immunol. 2017;14(5):465–475.
   PubMed Web of Science ®Google Scholar
• Pei J, Zhao M, Ye Z, et al. Autophagy enhances the replication of classical swine fever virus in vitro. Autophagy. 2014;10(1):93–110.
   PubMed Web of Science ®Google Scholar
• Lin J, Wang C, Liang W, et al. Rab1A is required for assembly of classical swine fever virus particle. Virology. 2018;514:18–29.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy. 2007;3(3):181–206.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Noda T, Yoshimori T, et al. A protein conjugation system essential for autophagy. Nature. 1998;395(6700):395–398.
   PubMed Web of Science ®Google Scholar
• Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122(6):927–939.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
   PubMed Web of Science ®Google Scholar
• Mauthe M, Orhon I, Rocchi C, et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy. 2018;14(8):1435–1455.
   PubMed Web of Science ®Google Scholar
• Brimacombe CL, Grove J, Meredith LW, et al. Neutralizing antibody-resistant hepatitis C virus cell-to-cell transmission. J Virol. 2011;85(1):596–605.
   PubMed Web of Science ®Google Scholar
• Lee CY, Kam YW, Fric J, et al. Chikungunya virus neutralization antigens and direct cell-to-cell transmission are revealed by human antibody-escape mutants. PLoS Pathog. 2011;7(12):e1002390.
   PubMed Web of Science ®Google Scholar
• Favoreel HW, Van Minnebruggen G, Adriaensen D, et al. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an alphaherpesvirus are associated with enhanced spread. Proc Natl Acad Sci U S A. 2005;102(25):8990–8995.
   PubMed Web of Science ®Google Scholar
• Narasimhulu V, Bellamy-McIntyre AK, Laumaea AE, et al. Distinct functions for the membrane-proximal ectodomain region (MPER) of HIV-1 gp41 in cell-free and cell-cell viral transmission and cell-cell fusion. J Biol Chem. 2018;293(16):6099–6120.
   PubMed Web of Science ®Google Scholar
• Dutartre H, Clavière M, Journo C, et al. Cell-free versus cell-to-cell infection by human immunodeficiency virus type 1 and human T-lymphotropic virus type 1: exploring the link among viral source, viral trafficking, and viral replication. J Virol. 2016;90(17):7607–7617.
   PubMed Web of Science ®Google Scholar
• Shahid MA, Abubakar M, Hameed S, et al. Avian influenza virus (H5N1); effects of physico-chemical factors on its survival. Virol J. 2009;6(1):38.
   PubMedGoogle Scholar
• Tkach M, Kowal J, Théry C. Why the need and how to approach the functional diversity of extracellular vesicles. Philos Trans R Soc London B: Biol Sci. 2018;373(1737):20160479.
   PubMed Web of Science ®Google Scholar
• van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228.
   PubMed Web of Science ®Google Scholar
• Boulanger CM, Loyer X, Rautou PE, et al. Extracellular vesicles in coronary artery disease. Nature reviews. Cardiology. 2017;14:259–272.
   PubMed Web of Science ®Google Scholar
• Muralidharan-Chari V, Clancy J, Plou C, et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol. 2009;19(22):1875–1885.
   PubMed Web of Science ®Google Scholar
• Sinha S, Hoshino D, Hong NH, et al. Cortactin promotes exosome secretion by controlling branched actin dynamics. J Cell Biol. 2016;214(2):197–213.
   PubMed Web of Science ®Google Scholar
• Haraszti RA, Didiot MC, Sapp E, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5(1):32570.
   PubMed Web of Science ®Google Scholar
• Böing AN, Van Der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014;3(1):10.3402.
   Google Scholar
• Momen-Heravi F. Isolation of extracellular vesicles by ultracentrifugation. Methods Mol Biol. 2017;1660:25–32.
   PubMedGoogle Scholar
• Ford T, Graham J, Rickwood D. Iodixanol: a nonionic iso-osmotic centrifugation medium for the formation of self-generated gradients. Anal Biochem. 1994;220(2):360–366.
   PubMed Web of Science ®Google Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221(1):3–12.
   PubMed Web of Science ®Google Scholar
• Choi Y, Bowman JW, Jung JU. Autophagy during viral infection – a double-edged sword. Nat Rev Microbiol. 2018;16(6):341–354.
   PubMed Web of Science ®Google Scholar
• Viret C, Rozières A, Faure M. Autophagy during early virus-host cell interactions. J Mol Biol. 2018;430(12):1696–1713.
   PubMed Web of Science ®Google Scholar
• Zhu E, Wu H, Chen W, et al. Classical swine fever virus employs the PERK- and IRE1-dependent autophagy for viral replication in cultured cells. Virulence. 2021;12(1):130–149.
   PubMed Web of Science ®Google Scholar
• Pei J, Deng J, Ye Z, et al. Absence of autophagy promotes apoptosis by modulating the ROS-dependent RLR signaling pathway in classical swine fever virus-infected cells. Autophagy. 2016;12(10):1738–1758.
   PubMed Web of Science ®Google Scholar
• Ponpuak M, Mandell MA, Kimura T, et al. Secretory autophagy. Curr Opin Cell Biol. 2015;35:106–116.
   PubMed Web of Science ®Google Scholar
• Robinson SM, Tsueng G, Sin J, et al. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog. 2014;10(4):e1004045.
   PubMed Web of Science ®Google Scholar
• Jackson WT, Giddings TH Jr, Taylor MP, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005;3(5):e156.
   PubMed Web of Science ®Google Scholar
• Phillips DM. The role of cell-to-cell transmission in HIV infection. AIDS. 1994;8(6):719–732.
   PubMed Web of Science ®Google Scholar
• Nolte-’t Hoen E, Cremer T, Gallo RC, et al. Extracellular vesicles and viruses: are they close relatives? Proc Natl Acad Sci U S A. 2016;113(33):9155–9161.
   PubMed Web of Science ®Google Scholar
• Criscuolo E, Castelli M, Diotti RA, et al. Cell-to-cell spread blocking activity is extremely limited in the sera of herpes simplex virus 1 (HSV-1)- and HSV-2-infected subjects. J Virol. 2019;93(11):e00070–19.
   PubMed Web of Science ®Google Scholar
• Chahar HS, Bao X, Casola A. Exosomes and their role in the life cycle and pathogenesis of RNA viruses. Viruses. 2015;7(6):3204–3225.
   PubMed Web of Science ®Google Scholar
• Kouwaki T, Fukushima Y, Daito T, et al. Extracellular vesicles including exosomes regulate innate immune responses to hepatitis B virus infection. Front Immunol. 2016;7:335.
   PubMed Web of Science ®Google Scholar
• Kloss M, Decker P, Baltz KM, et al. Interaction of monocytes with NK cells upon toll-like receptor-induced expression of the NKG2D ligand MICA. The Journal of Immunology. 2008;181(10):6711–6719.
   PubMed Web of Science ®Google Scholar
• Ebihara T, Masuda H, Akazawa T, et al. Induction of NKG2D ligands on human dendritic cells by TLR ligand stimulation and RNA virus infection. Int Immunol. 2007;19(10):1145–1155.
   PubMed Web of Science ®Google Scholar
• Giannecchini S. Evidence of the mechanism by which polyomaviruses exploit the extracellular vesicle delivery system during infection. Viruses. 2020;12(6):E585.
   PubMed Web of Science ®Google Scholar