Host factor Rab11a is critical for efficient assembly of influenza A virus genomic segments
It is well documented that influenza A viruses selectively package 8 distinct viral ribonucleoprotein complexes (vRNPs) into each virion; however, the role of host factors in genome assembly is not completely understood. To evaluate the significance of cellular factors in genome assembly, we generat...
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| creator | Han, Julianna Ganti, Ketaki Sali, Veeresh Kumar Twigg, Carly Zhang, Yifeng Manivasagam, Senthamizharasi Liang, Chieh-Yu Vogel, Olivia A Huang, Iris Emmanuel, Shanan N Plung, Jesse Radoshevich, Lillianna Perez, Jasmine T Lowen, Anice C Manicassamy, Balaji |
| description | It is well documented that influenza A viruses selectively package 8 distinct viral ribonucleoprotein complexes (vRNPs) into each virion; however, the role of host factors in genome assembly is not completely understood. To evaluate the significance of cellular factors in genome assembly, we generated a reporter virus carrying a tetracysteine tag in the NP gene (NP-Tc virus) and assessed the dynamics of vRNP localization with cellular components by fluorescence microscopy. At early time points, vRNP complexes were preferentially exported to the MTOC; subsequently, vRNPs associated on vesicles positive for cellular factor Rab11a and formed distinct vRNP bundles that trafficked to the plasma membrane on microtubule networks. In Rab11a deficient cells, however, vRNP bundles were smaller in the cytoplasm with less co-localization between different vRNP segments. Furthermore, Rab11a deficiency increased the production of non-infectious particles with higher RNA copy number to PFU ratios, indicative of defects in specific genome assembly. These results indicate that Rab11a+ vesicles serve as hubs for the congregation of vRNP complexes and enable specific genome assembly through vRNP:vRNP interactions, revealing the importance of Rab11a as a critical host factor for influenza A virus genome assembly. |
| doi_str_mv | 10.1371/journal.ppat.1009517 |
| format | Article |
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To evaluate the significance of cellular factors in genome assembly, we generated a reporter virus carrying a tetracysteine tag in the NP gene (NP-Tc virus) and assessed the dynamics of vRNP localization with cellular components by fluorescence microscopy. At early time points, vRNP complexes were preferentially exported to the MTOC; subsequently, vRNPs associated on vesicles positive for cellular factor Rab11a and formed distinct vRNP bundles that trafficked to the plasma membrane on microtubule networks. In Rab11a deficient cells, however, vRNP bundles were smaller in the cytoplasm with less co-localization between different vRNP segments. Furthermore, Rab11a deficiency increased the production of non-infectious particles with higher RNA copy number to PFU ratios, indicative of defects in specific genome assembly. These results indicate that Rab11a+ vesicles serve as hubs for the congregation of vRNP complexes and enable specific genome assembly through vRNP:vRNP interactions, revealing the importance of Rab11a as a critical host factor for influenza A virus genome assembly.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1009517</identifier><identifier>PMID: 33970958</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>A549 Cells ; Actin ; Antibodies ; Assembly ; Biology and life sciences ; Cytoplasm ; Egress ; Exports ; Fluorescence ; Fluorescence microscopy ; Genetic aspects ; Genome, Viral ; Genomes ; Health aspects ; HEK293 Cells ; Host-virus relationships ; Humans ; Influenza ; Influenza A ; Influenza A virus - genetics ; Influenza A virus - isolation & purification ; Influenza viruses ; Influenza, Human - genetics ; Influenza, Human - virology ; Medicine and health sciences ; Microscopy ; Packaging ; Proteins ; rab GTP-Binding Proteins - genetics ; rab GTP-Binding Proteins - metabolism ; Reagents ; Research and Analysis Methods ; Ribonucleoproteins ; Ribonucleoproteins - genetics ; Ribonucleoproteins - metabolism ; Viral Proteins - genetics ; Viral Proteins - metabolism ; Virions ; Virulence (Microbiology) ; Virus Assembly ; Virus Replication ; Viruses</subject><ispartof>PLoS pathogens, 2021-05, Vol.17 (5), p.e1009517-e1009517</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Han et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Han et al 2021 Han et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c661t-b9dd8a258d2ad76cc2f0add686266a6451f7e2fbd8b84b202aa9e87fd2acae103</citedby><cites>FETCH-LOGICAL-c661t-b9dd8a258d2ad76cc2f0add686266a6451f7e2fbd8b84b202aa9e87fd2acae103</cites><orcidid>0000-0003-0294-9300 ; 0000-0002-3402-2609 ; 0000-0002-7348-0223 ; 0000-0002-8347-7167 ; 0000-0003-4624-7212 ; 0000-0003-1950-7031 ; 0000-0002-9687-3505 ; 0000-0003-1964-0967 ; 0000-0002-7972-2369 ; 0000-0002-7918-0395 ; 0000-0002-9829-112X</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/PMC8136845/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136845/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23864,27922,27923,53789,53791,79370,79371</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33970958$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shih, Shin-Ru</contributor><creatorcontrib>Han, Julianna</creatorcontrib><creatorcontrib>Ganti, Ketaki</creatorcontrib><creatorcontrib>Sali, Veeresh Kumar</creatorcontrib><creatorcontrib>Twigg, Carly</creatorcontrib><creatorcontrib>Zhang, Yifeng</creatorcontrib><creatorcontrib>Manivasagam, Senthamizharasi</creatorcontrib><creatorcontrib>Liang, Chieh-Yu</creatorcontrib><creatorcontrib>Vogel, Olivia A</creatorcontrib><creatorcontrib>Huang, Iris</creatorcontrib><creatorcontrib>Emmanuel, Shanan N</creatorcontrib><creatorcontrib>Plung, Jesse</creatorcontrib><creatorcontrib>Radoshevich, Lillianna</creatorcontrib><creatorcontrib>Perez, Jasmine T</creatorcontrib><creatorcontrib>Lowen, Anice C</creatorcontrib><creatorcontrib>Manicassamy, Balaji</creatorcontrib><title>Host factor Rab11a is critical for efficient assembly of influenza A virus genomic segments</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>It is well documented that influenza A viruses selectively package 8 distinct viral ribonucleoprotein complexes (vRNPs) into each virion; however, the role of host factors in genome assembly is not completely understood. To evaluate the significance of cellular factors in genome assembly, we generated a reporter virus carrying a tetracysteine tag in the NP gene (NP-Tc virus) and assessed the dynamics of vRNP localization with cellular components by fluorescence microscopy. At early time points, vRNP complexes were preferentially exported to the MTOC; subsequently, vRNPs associated on vesicles positive for cellular factor Rab11a and formed distinct vRNP bundles that trafficked to the plasma membrane on microtubule networks. In Rab11a deficient cells, however, vRNP bundles were smaller in the cytoplasm with less co-localization between different vRNP segments. Furthermore, Rab11a deficiency increased the production of non-infectious particles with higher RNA copy number to PFU ratios, indicative of defects in specific genome assembly. These results indicate that Rab11a+ vesicles serve as hubs for the congregation of vRNP complexes and enable specific genome assembly through vRNP:vRNP interactions, revealing the importance of Rab11a as a critical host factor for influenza A virus genome assembly.</description><subject>A549 Cells</subject><subject>Actin</subject><subject>Antibodies</subject><subject>Assembly</subject><subject>Biology and life sciences</subject><subject>Cytoplasm</subject><subject>Egress</subject><subject>Exports</subject><subject>Fluorescence</subject><subject>Fluorescence microscopy</subject><subject>Genetic aspects</subject><subject>Genome, Viral</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>HEK293 Cells</subject><subject>Host-virus relationships</subject><subject>Humans</subject><subject>Influenza</subject><subject>Influenza A</subject><subject>Influenza A virus - genetics</subject><subject>Influenza A virus - isolation & purification</subject><subject>Influenza viruses</subject><subject>Influenza, Human - genetics</subject><subject>Influenza, Human - virology</subject><subject>Medicine and health sciences</subject><subject>Microscopy</subject><subject>Packaging</subject><subject>Proteins</subject><subject>rab GTP-Binding Proteins - genetics</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>Reagents</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleoproteins</subject><subject>Ribonucleoproteins - genetics</subject><subject>Ribonucleoproteins - metabolism</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><subject>Virions</subject><subject>Virulence (Microbiology)</subject><subject>Virus Assembly</subject><subject>Virus 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factor Rab11a is critical for efficient assembly of influenza A virus genomic segments</title><author>Han, Julianna ; Ganti, Ketaki ; Sali, Veeresh Kumar ; Twigg, Carly ; Zhang, Yifeng ; Manivasagam, Senthamizharasi ; Liang, Chieh-Yu ; Vogel, Olivia A ; Huang, Iris ; Emmanuel, Shanan N ; Plung, Jesse ; Radoshevich, Lillianna ; Perez, Jasmine T ; Lowen, Anice C ; Manicassamy, Balaji</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c661t-b9dd8a258d2ad76cc2f0add686266a6451f7e2fbd8b84b202aa9e87fd2acae103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>A549 Cells</topic><topic>Actin</topic><topic>Antibodies</topic><topic>Assembly</topic><topic>Biology and life sciences</topic><topic>Cytoplasm</topic><topic>Egress</topic><topic>Exports</topic><topic>Fluorescence</topic><topic>Fluorescence microscopy</topic><topic>Genetic aspects</topic><topic>Genome, 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Balaji</au><au>Shih, Shin-Ru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host factor Rab11a is critical for efficient assembly of influenza A virus genomic segments</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2021-05-10</date><risdate>2021</risdate><volume>17</volume><issue>5</issue><spage>e1009517</spage><epage>e1009517</epage><pages>e1009517-e1009517</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>It is well documented that influenza A viruses selectively package 8 distinct viral ribonucleoprotein complexes (vRNPs) into each virion; however, the role of host factors in genome assembly is not completely understood. To evaluate the significance of cellular factors in genome assembly, we generated a reporter virus carrying a tetracysteine tag in the NP gene (NP-Tc virus) and assessed the dynamics of vRNP localization with cellular components by fluorescence microscopy. At early time points, vRNP complexes were preferentially exported to the MTOC; subsequently, vRNPs associated on vesicles positive for cellular factor Rab11a and formed distinct vRNP bundles that trafficked to the plasma membrane on microtubule networks. In Rab11a deficient cells, however, vRNP bundles were smaller in the cytoplasm with less co-localization between different vRNP segments. Furthermore, Rab11a deficiency increased the production of non-infectious particles with higher RNA copy number to PFU ratios, indicative of defects in specific genome assembly. 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| ispartof | PLoS pathogens, 2021-05, Vol.17 (5), p.e1009517-e1009517 |
| issn | 1553-7374 1553-7366 1553-7374 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS); PubMed Central |
| subjects | A549 Cells Actin Antibodies Assembly Biology and life sciences Cytoplasm Egress Exports Fluorescence Fluorescence microscopy Genetic aspects Genome, Viral Genomes Health aspects HEK293 Cells Host-virus relationships Humans Influenza Influenza A Influenza A virus - genetics Influenza A virus - isolation & purification Influenza viruses Influenza, Human - genetics Influenza, Human - virology Medicine and health sciences Microscopy Packaging Proteins rab GTP-Binding Proteins - genetics rab GTP-Binding Proteins - metabolism Reagents Research and Analysis Methods Ribonucleoproteins Ribonucleoproteins - genetics Ribonucleoproteins - metabolism Viral Proteins - genetics Viral Proteins - metabolism Virions Virulence (Microbiology) Virus Assembly Virus Replication Viruses |
| title | Host factor Rab11a is critical for efficient assembly of influenza A virus genomic segments |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-13T19%3A12%3A12IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Host%20factor%20Rab11a%20is%20critical%20for%20efficient%20assembly%20of%20influenza%20A%20virus%20genomic%20segments&rft.jtitle=PLoS%20pathogens&rft.au=Han,%20Julianna&rft.date=2021-05-10&rft.volume=17&rft.issue=5&rft.spage=e1009517&rft.epage=e1009517&rft.pages=e1009517-e1009517&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1009517&rft_dat=%3Cgale_plos_%3EA663949304%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2541853762&rft_id=info:pmid/33970958&rft_galeid=A663949304&rft_doaj_id=oai_doaj_org_article_90b1301d28c24690ba02d23585dab79c&rfr_iscdi=true |