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The Epstein-Barr virus episome maneuvers between nuclear chromatin compartments during reactivation

Stephanie A. Moquin, Sean Thomas, Sean Whalen, Alix Warburton, Samantha G. Fernanadez, Alison A. McBride, Katherine S. Pollard, JJ L. Miranda
doi: https://doi.org/10.1101/177345
Stephanie A. Moquin
1Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California, USA
2Gladstone Institute of Virology and Immunology, San Francisco, California, USA
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Sean Thomas
3Gladstone Institutes, San Francisco, California, USA
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Sean Whalen
3Gladstone Institutes, San Francisco, California, USA
4Division of Biostatistics, Institute for Human Genetics, and Institute for Computational Health Sciences, University of California, San Francisco, California, USA
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Alix Warburton
5Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Samantha G. Fernanadez
2Gladstone Institute of Virology and Immunology, San Francisco, California, USA
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Alison A. McBride
5Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Katherine S. Pollard
3Gladstone Institutes, San Francisco, California, USA
4Division of Biostatistics, Institute for Human Genetics, and Institute for Computational Health Sciences, University of California, San Francisco, California, USA
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JJ L. Miranda
1Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California, USA
2Gladstone Institute of Virology and Immunology, San Francisco, California, USA
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  • For correspondence: jj.miranda@ucsf.edu
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ABSTRACT

The human genome is structurally organized in three-dimensional space to facilitate functional partitioning of transcription. We learned that the latent episome of the human Epstein-Barr virus (EBV) preferentially associates with gene-poor chromosomes and avoids gene-rich chromosomes. Kaposi’s sarcoma-associated herpesvirus behaves similarly, but human papillomavirus does not. Contacts localize on the EBV side to OriP, the latent origin of replication. This genetic element, and the EBNA1 protein that binds there, are sufficient to reconstitute chromosome association preferences of the entire episome. Contacts localize on the human side to gene-poor regions of chromatin distant from transcription start sites. Upon reactivation from latency, however, the episome moves away from repressive heterochromatin and toward active euchromatin. Our work adds three-dimensional relocalization to the molecular events that occur during reactivation. Involvement of a myriad of interchromosomal associations also suggests a role for this type of long - range association in gene regulation.

IMPORTANCE The human genome is structurally organized in three-dimensional space, and this structure functionally affects transcriptional activity. We set out to investigate whether a double stranded DNA virus, Epstein-Barr virus (EBV), uses similar mechanisms as the human genome to regulate transcription. We found that the EBV genome associates with repressive compartments of the nucleus during latency and active compartments during reactivation. This study is advances our knowledge of the EBV life cycle, adding three-dimensional re-localization as a novel component to the molecular events that occur during reactivation. Furthermore, the data adds to our understanding of nuclear compartments, showing that disperse interchromosomal interactions may be important for regulating transcription.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 17, 2017.
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The Epstein-Barr virus episome maneuvers between nuclear chromatin compartments during reactivation
Stephanie A. Moquin, Sean Thomas, Sean Whalen, Alix Warburton, Samantha G. Fernanadez, Alison A. McBride, Katherine S. Pollard, JJ L. Miranda
bioRxiv 177345; doi: https://doi.org/10.1101/177345
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The Epstein-Barr virus episome maneuvers between nuclear chromatin compartments during reactivation
Stephanie A. Moquin, Sean Thomas, Sean Whalen, Alix Warburton, Samantha G. Fernanadez, Alison A. McBride, Katherine S. Pollard, JJ L. Miranda
bioRxiv 177345; doi: https://doi.org/10.1101/177345

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