Merkel Cell Polyomavirus DNA Replication Induces Senescence in Human Dermal Fibroblasts in a Kap1/Trim28-Dependent Manner
Identifieur interne : 000113 ( an2020/Analysis ); précédent : 000112; suivant : 000114Merkel Cell Polyomavirus DNA Replication Induces Senescence in Human Dermal Fibroblasts in a Kap1/Trim28-Dependent Manner
Auteurs : Svenja Siebels [Allemagne] ; Manja Czech-Sioli [Allemagne] ; Michael Spohn [Allemagne] ; Claudia Schmidt [Allemagne] ; Juliane Theiss [Allemagne] ; Daniela Indenbirken [Allemagne] ; Thomas Günther [Allemagne] ; Adam Grundhoff [Allemagne] ; Nicole Fischer [Allemagne]Source :
- mBio [ 2150-7511 ] ; 2020.
Abstract
We here describe Kap1 as a restriction factor in MCPyV infection. We report a novel, indirect mechanism by which Kap1 affects MCPyV replication. In contrast with from other DNA viruses, Kap1 does not associate with the viral genome in MCPyV infection and has no impact on viral gene expression. In MCPyV-infected nHDF cells, Kap1 phosphorylation (pKap1 S824) accumulates because of genomic stress mainly induced by viral DNA replication. In contrast, ectopic expression of LT or LT MCPyV mutants, previously shown to be important for induction of genotoxic stress, does not result in a similar extent of pKap1 accumulation. We show that cells actively replicating MCPyV accumulate pKap1 (in a manner dependent on the presence of ATM) and display a senescence phenotype reflected by G2 arrest. These results are supported by transcriptome analyses showing that LT antigen, in a manner dependent on the presence of Kap1, induces expression of secreted factors, which is known as the senescence-associated secretory phenotype (SASP).
Url:
DOI: 10.1128/mBio.00142-20
PubMed: 32156811
PubMed Central: 7064754
Affiliations:
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Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Czech Sioli, Manja" sort="Czech Sioli, Manja" uniqKey="Czech Sioli M" first="Manja" last="Czech-Sioli">Manja Czech-Sioli</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Spohn, Michael" sort="Spohn, Michael" uniqKey="Spohn M" first="Michael" last="Spohn">Michael Spohn</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Schmidt, Claudia" sort="Schmidt, Claudia" uniqKey="Schmidt C" first="Claudia" last="Schmidt">Claudia Schmidt</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Theiss, Juliane" sort="Theiss, Juliane" uniqKey="Theiss J" first="Juliane" last="Theiss">Juliane Theiss</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Indenbirken, Daniela" sort="Indenbirken, Daniela" uniqKey="Indenbirken D" first="Daniela" last="Indenbirken">Daniela Indenbirken</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Gunther, Thomas" sort="Gunther, Thomas" uniqKey="Gunther T" first="Thomas" last="Günther">Thomas Günther</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Grundhoff, Adam" sort="Grundhoff, Adam" uniqKey="Grundhoff A" first="Adam" last="Grundhoff">Adam Grundhoff</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author><author><name sortKey="Fischer, Nicole" sort="Fischer, Nicole" uniqKey="Fischer N" first="Nicole" last="Fischer">Nicole Fischer</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg</wicri:regionArea><placeName><settlement type="city">Hambourg</settlement><region type="land" nuts="2">Hambourg</region></placeName></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We here describe Kap1 as a restriction factor in MCPyV infection. We report a novel, indirect mechanism by which Kap1 affects MCPyV replication. In contrast with from other DNA viruses, Kap1 does not associate with the viral genome in MCPyV infection and has no impact on viral gene expression. In MCPyV-infected nHDF cells, Kap1 phosphorylation (pKap1 S824) accumulates because of genomic stress mainly induced by viral DNA replication. In contrast, ectopic expression of LT or LT MCPyV mutants, previously shown to be important for induction of genotoxic stress, does not result in a similar extent of pKap1 accumulation. We show that cells actively replicating MCPyV accumulate pKap1 (in a manner dependent on the presence of ATM) and display a senescence phenotype reflected by G<sub>2</sub> arrest. These results are supported by transcriptome analyses showing that LT antigen, in a manner dependent on the presence of Kap1, induces expression of secreted factors, which is known as the senescence-associated secretory phenotype (SASP).</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Becker, Jc" uniqKey="Becker J">JC Becker</name></author><author><name sortKey="Stang, A" uniqKey="Stang A">A Stang</name></author><author><name sortKey="Hausen, Az" uniqKey="Hausen A">AZ Hausen</name></author><author><name sortKey="Fischer, N" uniqKey="Fischer N">N Fischer</name></author><author><name sortKey="Decaprio, Ja" uniqKey="Decaprio J">JA DeCaprio</name></author><author><name sortKey="Tothill, Rw" uniqKey="Tothill R">RW Tothill</name></author><author><name sortKey="Lyngaa, R" uniqKey="Lyngaa R">R Lyngaa</name></author><author><name sortKey="Hansen, Uk" uniqKey="Hansen U">UK Hansen</name></author><author><name sortKey="Ritter, C" 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Nicole" uniqKey="Fischer N" first="Nicole" last="Fischer">Nicole Fischer</name><name sortKey="Grundhoff, Adam" sort="Grundhoff, Adam" uniqKey="Grundhoff A" first="Adam" last="Grundhoff">Adam Grundhoff</name><name sortKey="Gunther, Thomas" sort="Gunther, Thomas" uniqKey="Gunther T" first="Thomas" last="Günther">Thomas Günther</name><name sortKey="Indenbirken, Daniela" sort="Indenbirken, Daniela" uniqKey="Indenbirken D" first="Daniela" last="Indenbirken">Daniela Indenbirken</name><name sortKey="Schmidt, Claudia" sort="Schmidt, Claudia" uniqKey="Schmidt C" first="Claudia" last="Schmidt">Claudia Schmidt</name><name sortKey="Spohn, Michael" sort="Spohn, Michael" uniqKey="Spohn M" first="Michael" last="Spohn">Michael Spohn</name><name sortKey="Theiss, Juliane" sort="Theiss, Juliane" uniqKey="Theiss J" first="Juliane" last="Theiss">Juliane Theiss</name><name sortKey="Theiss, Juliane" sort="Theiss, Juliane" uniqKey="Theiss J" first="Juliane" last="Theiss">Juliane 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