Vaccinia virus hijacks ESCRT-mediated multivesicular body formation for virus egress
Poxvirus egress is a complex process whereby cytoplasmic single membrane-bound virions are wrapped in a cell-derived double membrane. These triple-membrane particles, termed intracellular enveloped virions (IEVs), are released from infected cells by fusion. Whereas the wrapping double membrane is th...
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| Veröffentlicht in: | Life science alliance 2021-08, Vol.4 (8), p.e202000910 |
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| creator | Huttunen, Moona Samolej, Jerzy Evans, Robert J Yakimovich, Artur White, Ian J Kriston-Vizi, Janos Martin-Serrano, Juan Sundquist, Wesley I Frickel, Eva-Maria Mercer, Jason |
| description | Poxvirus egress is a complex process whereby cytoplasmic single membrane-bound virions are wrapped in a cell-derived double membrane. These triple-membrane particles, termed intracellular enveloped virions (IEVs), are released from infected cells by fusion. Whereas the wrapping double membrane is thought to be derived from virus-modified trans-Golgi or early endosomal cisternae, the cellular factors that regulate virus wrapping remain largely undefined. To identify cell factors required for this process the prototypic poxvirus, vaccinia virus (VACV), was subjected to an RNAi screen directed against cellular membrane-trafficking proteins. Focusing on the endosomal sorting complexes required for transport (ESCRT), we demonstrate that ESCRT-III and VPS4 are required for packaging of virus into multivesicular bodies (MVBs). EM-based characterization of MVB-IEVs showed that they account for half of IEV production indicating that MVBs are a second major source of VACV wrapping membrane. These data support a model whereby, in addition to cisternae-based wrapping, VACV hijacks ESCRT-mediated MVB formation to facilitate virus egress and spread. |
| doi_str_mv | 10.26508/LSA.202000910 |
| format | Article |
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These triple-membrane particles, termed intracellular enveloped virions (IEVs), are released from infected cells by fusion. Whereas the wrapping double membrane is thought to be derived from virus-modified trans-Golgi or early endosomal cisternae, the cellular factors that regulate virus wrapping remain largely undefined. To identify cell factors required for this process the prototypic poxvirus, vaccinia virus (VACV), was subjected to an RNAi screen directed against cellular membrane-trafficking proteins. Focusing on the endosomal sorting complexes required for transport (ESCRT), we demonstrate that ESCRT-III and VPS4 are required for packaging of virus into multivesicular bodies (MVBs). EM-based characterization of MVB-IEVs showed that they account for half of IEV production indicating that MVBs are a second major source of VACV wrapping membrane. These data support a model whereby, in addition to cisternae-based wrapping, VACV hijacks ESCRT-mediated MVB formation to facilitate virus egress and spread.</description><identifier>ISSN: 2575-1077</identifier><identifier>EISSN: 2575-1077</identifier><identifier>DOI: 10.26508/LSA.202000910</identifier><identifier>PMID: 34145027</identifier><language>eng</language><publisher>United States: Life Science Alliance LLC</publisher><subject>ATPases Associated with Diverse Cellular Activities - metabolism ; Cell Line ; Endosomal Sorting Complexes Required for Transport - metabolism ; Endosomes - virology ; HeLa Cells ; Humans ; THP-1 Cells ; Vaccinia virus - genetics ; Vaccinia virus - pathogenicity ; Vacuolar Proton-Translocating ATPases - metabolism ; Viral Genome Packaging ; Virus Release</subject><ispartof>Life science alliance, 2021-08, Vol.4 (8), p.e202000910</ispartof><rights>2021 Huttunen et al.</rights><rights>2021 Huttunen et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c390t-daeb730d4dc08cc55d4c86c0813488595d695015ae26c288944c936506bbeda13</citedby><cites>FETCH-LOGICAL-c390t-daeb730d4dc08cc55d4c86c0813488595d695015ae26c288944c936506bbeda13</cites><orcidid>0000-0002-4745-0477 ; 0000-0003-0678-6510 ; 0000-0003-1466-9541</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321658/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321658/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34145027$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Huttunen, Moona</creatorcontrib><creatorcontrib>Samolej, Jerzy</creatorcontrib><creatorcontrib>Evans, Robert J</creatorcontrib><creatorcontrib>Yakimovich, Artur</creatorcontrib><creatorcontrib>White, Ian J</creatorcontrib><creatorcontrib>Kriston-Vizi, Janos</creatorcontrib><creatorcontrib>Martin-Serrano, Juan</creatorcontrib><creatorcontrib>Sundquist, Wesley I</creatorcontrib><creatorcontrib>Frickel, Eva-Maria</creatorcontrib><creatorcontrib>Mercer, Jason</creatorcontrib><title>Vaccinia virus hijacks ESCRT-mediated multivesicular body formation for virus egress</title><title>Life science alliance</title><addtitle>Life Sci Alliance</addtitle><description>Poxvirus egress is a complex process whereby cytoplasmic single membrane-bound virions are wrapped in a cell-derived double membrane. 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These data support a model whereby, in addition to cisternae-based wrapping, VACV hijacks ESCRT-mediated MVB formation to facilitate virus egress and spread.</description><subject>ATPases Associated with Diverse Cellular Activities - metabolism</subject><subject>Cell Line</subject><subject>Endosomal Sorting Complexes Required for Transport - metabolism</subject><subject>Endosomes - virology</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>THP-1 Cells</subject><subject>Vaccinia virus - genetics</subject><subject>Vaccinia virus - pathogenicity</subject><subject>Vacuolar Proton-Translocating ATPases - metabolism</subject><subject>Viral Genome Packaging</subject><subject>Virus Release</subject><issn>2575-1077</issn><issn>2575-1077</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUtLAzEUhYMoVmq3LmWWbqbmOZPZCKXUBxQEW92GTJK2qTOTmswU-u-Ntpa6ugfud899AXCD4BBnDPL76Ww0xBBDCAsEz8AVZjlLEczz8xPdA4MQ1pGJHKaMXoIeoYgyiPMrMP-QStnGymRrfReSlV1L9RmSyWz8Nk9ro61sjU7qrmrt1gSrukr6pHR6lyycr2VrXfOjDuVm6U0I1-BiIatgBofYB--Pk_n4OZ2-Pr2MR9NUkQK2qZamzAnUVCvIlWJMU8WzqBGhnLOC6axgEDFpcKYw5wWlqiBx8awsjZaI9MHD3nfTlXFUZZrWy0psvK2l3wknrfifaexKLN1WcIJRxng0uDsYePfVmdCK2gZlqko2xnVBYEYJZRnMYUSHe1R5F4I3i2MbBMXvN0QVpDh-Ixbcng53xP9uT74B67OGTw</recordid><startdate>20210801</startdate><enddate>20210801</enddate><creator>Huttunen, Moona</creator><creator>Samolej, Jerzy</creator><creator>Evans, Robert J</creator><creator>Yakimovich, Artur</creator><creator>White, Ian J</creator><creator>Kriston-Vizi, Janos</creator><creator>Martin-Serrano, Juan</creator><creator>Sundquist, Wesley I</creator><creator>Frickel, Eva-Maria</creator><creator>Mercer, Jason</creator><general>Life Science Alliance LLC</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4745-0477</orcidid><orcidid>https://orcid.org/0000-0003-0678-6510</orcidid><orcidid>https://orcid.org/0000-0003-1466-9541</orcidid></search><sort><creationdate>20210801</creationdate><title>Vaccinia virus hijacks ESCRT-mediated multivesicular body formation for virus egress</title><author>Huttunen, Moona ; 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These triple-membrane particles, termed intracellular enveloped virions (IEVs), are released from infected cells by fusion. Whereas the wrapping double membrane is thought to be derived from virus-modified trans-Golgi or early endosomal cisternae, the cellular factors that regulate virus wrapping remain largely undefined. To identify cell factors required for this process the prototypic poxvirus, vaccinia virus (VACV), was subjected to an RNAi screen directed against cellular membrane-trafficking proteins. Focusing on the endosomal sorting complexes required for transport (ESCRT), we demonstrate that ESCRT-III and VPS4 are required for packaging of virus into multivesicular bodies (MVBs). EM-based characterization of MVB-IEVs showed that they account for half of IEV production indicating that MVBs are a second major source of VACV wrapping membrane. 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| subjects | ATPases Associated with Diverse Cellular Activities - metabolism Cell Line Endosomal Sorting Complexes Required for Transport - metabolism Endosomes - virology HeLa Cells Humans THP-1 Cells Vaccinia virus - genetics Vaccinia virus - pathogenicity Vacuolar Proton-Translocating ATPases - metabolism Viral Genome Packaging Virus Release |
| title | Vaccinia virus hijacks ESCRT-mediated multivesicular body formation for virus egress |
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