Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle
In infected cells rotavirus (RV) replicates in viroplasms, cytosolic structures that require a stabilized microtubule (MT) network for their assembly, maintenance of the structure and perinuclear localization. Therefore, we hypothesized that RV could interfere with the MT-breakdown that takes place...
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| creator | Glück, Selene Buttafuoco, Antonino Meier, Anita F Arnoldi, Francesca Vogt, Bernd Schraner, Elisabeth M Ackermann, Mathias Eichwald, Catherine |
| description | In infected cells rotavirus (RV) replicates in viroplasms, cytosolic structures that require a stabilized microtubule (MT) network for their assembly, maintenance of the structure and perinuclear localization. Therefore, we hypothesized that RV could interfere with the MT-breakdown that takes place in mitosis during cell division. Using synchronized RV-permissive cells, we show that RV infection arrests the cell cycle in S/G2 phase, thus favoring replication by improving viroplasms formation, viral protein translation, and viral assembly. The arrest in S/G2 phase is independent of the host or viral strain and relies on active RV replication. RV infection causes cyclin B1 down-regulation, consistent with blocking entry into mitosis. With the aid of chemical inhibitors, the cytoskeleton network was linked to specific signaling pathways of the RV-induced cell cycle arrest. We found that upon RV infection Eg5 kinesin was delocalized from the pericentriolar region to the viroplasms. We used a MA104-Fucci system to identify three RV proteins (NSP3, NSP5, and VP2) involved in cell cycle arrest in the S-phase. Our data indicate that there is a strong correlation between the cell cycle arrest and RV replication. |
| doi_str_mv | 10.1371/journal.pone.0179607 |
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Therefore, we hypothesized that RV could interfere with the MT-breakdown that takes place in mitosis during cell division. Using synchronized RV-permissive cells, we show that RV infection arrests the cell cycle in S/G2 phase, thus favoring replication by improving viroplasms formation, viral protein translation, and viral assembly. The arrest in S/G2 phase is independent of the host or viral strain and relies on active RV replication. RV infection causes cyclin B1 down-regulation, consistent with blocking entry into mitosis. With the aid of chemical inhibitors, the cytoskeleton network was linked to specific signaling pathways of the RV-induced cell cycle arrest. We found that upon RV infection Eg5 kinesin was delocalized from the pericentriolar region to the viroplasms. We used a MA104-Fucci system to identify three RV proteins (NSP3, NSP5, and VP2) involved in cell cycle arrest in the S-phase. Our data indicate that there is a strong correlation between the cell cycle arrest and RV replication.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0179607</identifier><identifier>PMID: 28622358</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Apoptosis ; Assembly ; Biology and Life Sciences ; Breakdown ; Cell cycle ; Cell division ; Control ; Correlation ; Cyclin B1 ; Cyclin B1 - metabolism ; Cyclin-dependent kinases ; Cytoskeleton ; Cytoskeleton - metabolism ; Cytoskeleton - virology ; Dogs ; G2 phase ; G2 Phase Cell Cycle Checkpoints ; Gene expression ; Genetic aspects ; Genomes ; HEK293 Cells ; Humans ; Infections ; Inhibitors ; Interphase ; Kinases ; Kinesin ; Kinesin - metabolism ; Localization ; Macaca mulatta ; Madin Darby Canine Kidney Cells ; Maintenance ; Mitosis ; Permissive cells ; Phosphorylation ; Physical Sciences ; Physiological aspects ; Proteins ; Replication ; Research and Analysis Methods ; Rotavirus ; Rotavirus - physiology ; Rotaviruses ; S Phase Cell Cycle Checkpoints ; Signal Transduction ; Viral infections ; Viral proteins ; Viral Proteins - metabolism ; Virology ; Virus replication ; Virus Replication - physiology ; Viruses</subject><ispartof>PloS one, 2017-06, Vol.12 (6), p.e0179607-e0179607</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Glück 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>2017 Glück et al 2017 Glück et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-fc2ab36cddee6e171c86161a2f61d69aa9131670259a59677c71f688baa92b1c3</citedby><cites>FETCH-LOGICAL-c692t-fc2ab36cddee6e171c86161a2f61d69aa9131670259a59677c71f688baa92b1c3</cites><orcidid>0000-0003-0001-4843</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/PMC5473577/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5473577/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28622358$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Glück, Selene</creatorcontrib><creatorcontrib>Buttafuoco, Antonino</creatorcontrib><creatorcontrib>Meier, Anita F</creatorcontrib><creatorcontrib>Arnoldi, Francesca</creatorcontrib><creatorcontrib>Vogt, Bernd</creatorcontrib><creatorcontrib>Schraner, Elisabeth M</creatorcontrib><creatorcontrib>Ackermann, Mathias</creatorcontrib><creatorcontrib>Eichwald, Catherine</creatorcontrib><title>Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In infected cells rotavirus (RV) replicates in viroplasms, cytosolic structures that require a stabilized microtubule (MT) network for their assembly, maintenance of the structure and perinuclear localization. Therefore, we hypothesized that RV could interfere with the MT-breakdown that takes place in mitosis during cell division. Using synchronized RV-permissive cells, we show that RV infection arrests the cell cycle in S/G2 phase, thus favoring replication by improving viroplasms formation, viral protein translation, and viral assembly. The arrest in S/G2 phase is independent of the host or viral strain and relies on active RV replication. RV infection causes cyclin B1 down-regulation, consistent with blocking entry into mitosis. With the aid of chemical inhibitors, the cytoskeleton network was linked to specific signaling pathways of the RV-induced cell cycle arrest. We found that upon RV infection Eg5 kinesin was delocalized from the pericentriolar region to the viroplasms. We used a MA104-Fucci system to identify three RV proteins (NSP3, NSP5, and VP2) involved in cell cycle arrest in the S-phase. Our data indicate that there is a strong correlation between the cell cycle arrest and RV replication.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Assembly</subject><subject>Biology and Life Sciences</subject><subject>Breakdown</subject><subject>Cell cycle</subject><subject>Cell division</subject><subject>Control</subject><subject>Correlation</subject><subject>Cyclin B1</subject><subject>Cyclin B1 - metabolism</subject><subject>Cyclin-dependent kinases</subject><subject>Cytoskeleton</subject><subject>Cytoskeleton - metabolism</subject><subject>Cytoskeleton - virology</subject><subject>Dogs</subject><subject>G2 phase</subject><subject>G2 Phase Cell Cycle Checkpoints</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Infections</subject><subject>Inhibitors</subject><subject>Interphase</subject><subject>Kinases</subject><subject>Kinesin</subject><subject>Kinesin - metabolism</subject><subject>Localization</subject><subject>Macaca mulatta</subject><subject>Madin Darby Canine Kidney Cells</subject><subject>Maintenance</subject><subject>Mitosis</subject><subject>Permissive cells</subject><subject>Phosphorylation</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Replication</subject><subject>Research and Analysis Methods</subject><subject>Rotavirus</subject><subject>Rotavirus - physiology</subject><subject>Rotaviruses</subject><subject>S Phase Cell Cycle Checkpoints</subject><subject>Signal Transduction</subject><subject>Viral infections</subject><subject>Viral proteins</subject><subject>Viral Proteins - metabolism</subject><subject>Virology</subject><subject>Virus replication</subject><subject>Virus Replication - physiology</subject><subject>Viruses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1rFDEUhgdR7If-A9EBoejFbvMxk0xuhFK0LhQKrfY2nMlkdrJkJ9skU-2_N-tOy470QnKRkPOcN8mbN8veYTTHlOPTlRt8D3a-cb2eI8wFQ_xFdogFJTNGEH25tz7IjkJYIVTSirHX2QGpGCG0rA6z22sX4d74IeReb6xREI3rcxNy5bzXFqJu8l8mdvnN6QXJTR-133QQdA6pHGLu2jx2Ou9cWittba4elNVvslct2KDfjvNx9vPb1x_n32eXVxeL87PLmWKCxFmrCNSUqabRmmnMsaoYZhhIy3DDBIDAFDOOSCmgFIxzxXHLqqpOFVJjRY-zDzvdjXVBjpYEiQVGRYWEQIlY7IjGwUpuvFmDf5AOjPy74fxSgo8m3VliVJEWKHCCoKioqGlTi7rhDeeNYAUkrS_jaUO91o3SffRgJ6LTSm86uXT3siw4LTlPAp9GAe_uhmSfXJuwdQ167YbdvbmoClYm9OM_6POvG6klpAeYvnXpXLUVlWeFKDlKoSCJmj9DpdHotVEpP61J-5OGz5OGxET9Oy5hCEEubq7_n726nbIne2ynwcYuODtsMxemYLEDlXcheN0-mYyR3Mb_0Q25jb8c45_a3u9_0FPTY97pH94Q_wQ</recordid><startdate>20170616</startdate><enddate>20170616</enddate><creator>Glück, Selene</creator><creator>Buttafuoco, Antonino</creator><creator>Meier, Anita F</creator><creator>Arnoldi, Francesca</creator><creator>Vogt, Bernd</creator><creator>Schraner, Elisabeth M</creator><creator>Ackermann, Mathias</creator><creator>Eichwald, Catherine</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-0001-4843</orcidid></search><sort><creationdate>20170616</creationdate><title>Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle</title><author>Glück, Selene ; Buttafuoco, Antonino ; Meier, Anita F ; Arnoldi, Francesca ; Vogt, Bernd ; Schraner, Elisabeth M ; Ackermann, Mathias ; Eichwald, Catherine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-fc2ab36cddee6e171c86161a2f61d69aa9131670259a59677c71f688baa92b1c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Assembly</topic><topic>Biology and Life Sciences</topic><topic>Breakdown</topic><topic>Cell cycle</topic><topic>Cell division</topic><topic>Control</topic><topic>Correlation</topic><topic>Cyclin B1</topic><topic>Cyclin B1 - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Glück, Selene</au><au>Buttafuoco, Antonino</au><au>Meier, Anita F</au><au>Arnoldi, Francesca</au><au>Vogt, Bernd</au><au>Schraner, Elisabeth M</au><au>Ackermann, Mathias</au><au>Eichwald, Catherine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-06-16</date><risdate>2017</risdate><volume>12</volume><issue>6</issue><spage>e0179607</spage><epage>e0179607</epage><pages>e0179607-e0179607</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In infected cells rotavirus (RV) replicates in viroplasms, cytosolic structures that require a stabilized microtubule (MT) network for their assembly, maintenance of the structure and perinuclear localization. Therefore, we hypothesized that RV could interfere with the MT-breakdown that takes place in mitosis during cell division. Using synchronized RV-permissive cells, we show that RV infection arrests the cell cycle in S/G2 phase, thus favoring replication by improving viroplasms formation, viral protein translation, and viral assembly. The arrest in S/G2 phase is independent of the host or viral strain and relies on active RV replication. RV infection causes cyclin B1 down-regulation, consistent with blocking entry into mitosis. With the aid of chemical inhibitors, the cytoskeleton network was linked to specific signaling pathways of the RV-induced cell cycle arrest. We found that upon RV infection Eg5 kinesin was delocalized from the pericentriolar region to the viroplasms. We used a MA104-Fucci system to identify three RV proteins (NSP3, NSP5, and VP2) involved in cell cycle arrest in the S-phase. Our data indicate that there is a strong correlation between the cell cycle arrest and RV replication.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28622358</pmid><doi>10.1371/journal.pone.0179607</doi><tpages>e0179607</tpages><orcidid>https://orcid.org/0000-0003-0001-4843</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Apoptosis Assembly Biology and Life Sciences Breakdown Cell cycle Cell division Control Correlation Cyclin B1 Cyclin B1 - metabolism Cyclin-dependent kinases Cytoskeleton Cytoskeleton - metabolism Cytoskeleton - virology Dogs G2 phase G2 Phase Cell Cycle Checkpoints Gene expression Genetic aspects Genomes HEK293 Cells Humans Infections Inhibitors Interphase Kinases Kinesin Kinesin - metabolism Localization Macaca mulatta Madin Darby Canine Kidney Cells Maintenance Mitosis Permissive cells Phosphorylation Physical Sciences Physiological aspects Proteins Replication Research and Analysis Methods Rotavirus Rotavirus - physiology Rotaviruses S Phase Cell Cycle Checkpoints Signal Transduction Viral infections Viral proteins Viral Proteins - metabolism Virology Virus replication Virus Replication - physiology Viruses |
| title | Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle |
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