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The HSV-1 ICP22 protein selectively impairs histone repositioning upon Pol II transcription downstream of genes

Author

Listed:
  • Lara Djakovic

    (Julius-Maximilians-University Würzburg)

  • Thomas Hennig

    (Julius-Maximilians-University Würzburg)

  • Katharina Reinisch

    (Ludwig-Maximilians-Universität München)

  • Andrea Milić

    (Julius-Maximilians-University Würzburg)

  • Adam W. Whisnant

    (Julius-Maximilians-University Würzburg)

  • Katharina Wolf

    (Julius-Maximilians-University Würzburg)

  • Elena Weiß

    (Ludwig-Maximilians-Universität München)

  • Tobias Haas

    (Julius-Maximilians-University Würzburg)

  • Arnhild Grothey

    (Julius-Maximilians-University Würzburg)

  • Christopher S. Jürges

    (Julius-Maximilians-University Würzburg)

  • Michael Kluge

    (Ludwig-Maximilians-Universität München)

  • Elmar Wolf

    (University of Würzburg
    University of Würzburg)

  • Florian Erhard

    (Julius-Maximilians-University Würzburg)

  • Caroline C. Friedel

    (Ludwig-Maximilians-Universität München)

  • Lars Dölken

    (Julius-Maximilians-University Würzburg
    Helmholtz-Center for Infection Research (HZI))

Abstract

Herpes simplex virus 1 (HSV-1) infection and stress responses disrupt transcription termination by RNA Polymerase II (Pol II). In HSV-1 infection, but not upon salt or heat stress, this is accompanied by a dramatic increase in chromatin accessibility downstream of genes. Here, we show that the HSV-1 immediate-early protein ICP22 is both necessary and sufficient to induce downstream open chromatin regions (dOCRs) when transcription termination is disrupted by the viral ICP27 protein. This is accompanied by a marked ICP22-dependent loss of histones downstream of affected genes consistent with impaired histone repositioning in the wake of Pol II. Efficient knock-down of the ICP22-interacting histone chaperone FACT is not sufficient to induce dOCRs in ΔICP22 infection but increases dOCR induction in wild-type HSV-1 infection. Interestingly, this is accompanied by a marked increase in chromatin accessibility within gene bodies. We propose a model in which allosteric changes in Pol II composition downstream of genes and ICP22-mediated interference with FACT activity explain the differential impairment of histone repositioning downstream of genes in the wake of Pol II in HSV-1 infection.

Suggested Citation

  • Lara Djakovic & Thomas Hennig & Katharina Reinisch & Andrea Milić & Adam W. Whisnant & Katharina Wolf & Elena Weiß & Tobias Haas & Arnhild Grothey & Christopher S. Jürges & Michael Kluge & Elmar Wolf , 2023. "The HSV-1 ICP22 protein selectively impairs histone repositioning upon Pol II transcription downstream of genes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40217-w
    DOI: 10.1038/s41467-023-40217-w
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    References listed on IDEAS

    as
    1. Lucia Falbo & Erica Raspelli & Francesco Romeo & Simona Fiorani & Federica Pezzimenti & Francesca Casagrande & Ilaria Costa & Dario Parazzoli & Vincenzo Costanzo, 2020. "SSRP1-mediated histone H1 eviction promotes replication origin assembly and accelerated development," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Xiuye Wang & Thomas Hennig & Adam W. Whisnant & Florian Erhard & Bhupesh K. Prusty & Caroline C. Friedel & Elmira Forouzmand & William Hu & Luke Erber & Yue Chen & Rozanne M. Sandri-Goldin & Lars Dölk, 2020. "Herpes simplex virus blocks host transcription termination via the bimodal activities of ICP27," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    3. Robert E. Thurman & Eric Rynes & Richard Humbert & Jeff Vierstra & Matthew T. Maurano & Eric Haugen & Nathan C. Sheffield & Andrew B. Stergachis & Hao Wang & Benjamin Vernot & Kavita Garg & Sam John &, 2012. "The accessible chromatin landscape of the human genome," Nature, Nature, vol. 489(7414), pages 75-82, September.
    4. Andrzej J. Rutkowski & Florian Erhard & Anne L’Hernault & Thomas Bonfert & Markus Schilhabel & Colin Crump & Philip Rosenstiel & Stacey Efstathiou & Ralf Zimmer & Caroline C. Friedel & Lars Dölken, 2015. "Widespread disruption of host transcription termination in HSV-1 infection," Nature Communications, Nature, vol. 6(1), pages 1-15, November.
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