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Transient DNA Binding Induces RNA Polymerase II Compartmentalization During Herpesviral Infection Distinct From Phase Separation

View ORCID ProfileDavid T McSwiggen, View ORCID ProfileAnders S Hansen, Hervé Marie-Nelly, View ORCID ProfileSheila Teves, View ORCID ProfileAlec B Heckert, View ORCID ProfileClaire Dugast-Darzacq, Yvonne Hao, Kayla K Umemoto, View ORCID ProfileRobert Tjian, View ORCID ProfileXavier Darzacq
doi: https://doi.org/10.1101/375071
David T McSwiggen
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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Anders S Hansen
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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Hervé Marie-Nelly
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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Sheila Teves
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
3Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, BC, Canada, BC V6T 1Z4
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Alec B Heckert
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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Claire Dugast-Darzacq
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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Yvonne Hao
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
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Kayla K Umemoto
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
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Robert Tjian
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
4Howard Hughes Medical Institute, University of California Berkeley, CA, USA, 94720
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  • For correspondence: jmlim@berkeley.edu darzacq@berkeley.edu
Xavier Darzacq
1Department of Molecular and Cell Biology, University of California Berkeley, CA, USA, 94720
2California Institute of Regenerative Medicine Center of Excellence, University of California Berkeley, CA, USA, 94720
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  • For correspondence: jmlim@berkeley.edu darzacq@berkeley.edu
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Summary

During lytic infection, Herpes Simplex Virus 1 generates replication compartments (RCs) in host nuclei that efficiently recruit protein factors, including host RNA Polymerase II (Pol II). Pol II and other cellular factors form hubs in uninfected cells that are proposed to phase separate via multivalent protein-protein interactions mediated by their intrinsically disordered regions. Using a battery of live cell microscopic techniques, we show that although RCs superficially exhibit many characteristics of phase separation, the recruitment of Pol II instead derives from nonspecific interactions with the viral DNA. We find that the viral genome remains nucleosome-free, profoundly affecting the way Pol II explores RCs by causing it to repetitively visit nearby binding sites, thereby creating local Pol II accumulations. This mechanism, distinct from phase separation, allows viral DNA to outcompete host DNA for cellular proteins. Our work provides new insights into the strategies used to create local molecular hubs in cells.

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Posted July 30, 2018.
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Transient DNA Binding Induces RNA Polymerase II Compartmentalization During Herpesviral Infection Distinct From Phase Separation
David T McSwiggen, Anders S Hansen, Hervé Marie-Nelly, Sheila Teves, Alec B Heckert, Claire Dugast-Darzacq, Yvonne Hao, Kayla K Umemoto, Robert Tjian, Xavier Darzacq
bioRxiv 375071; doi: https://doi.org/10.1101/375071
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Transient DNA Binding Induces RNA Polymerase II Compartmentalization During Herpesviral Infection Distinct From Phase Separation
David T McSwiggen, Anders S Hansen, Hervé Marie-Nelly, Sheila Teves, Alec B Heckert, Claire Dugast-Darzacq, Yvonne Hao, Kayla K Umemoto, Robert Tjian, Xavier Darzacq
bioRxiv 375071; doi: https://doi.org/10.1101/375071

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