WDR82/PNUTS-PP1 Prevents Transcription-Replication Conflicts by Promoting RNA Polymerase II Degradation on Chromatin

  • Cell Rep. 2020 Dec 1;33(9):108469. doi: 10.1016/j.celrep.2020.108469.
Helga B Landsverk  1 Lise E Sandquist  2 Lilli T E Bay  2 Barbara Steurer  3 Coen Campsteijn  4 Ole J B Landsverk  5 Jurgen A Marteijn  3 Eva Petermann  6 Laura Trinkle-Mulcahy  7 Randi G Syljuåsen  8
Affiliations
  • 1. Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, 0379 Oslo, Norway. Electronic address: [email protected].
  • 2. Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, 0379 Oslo, Norway.
  • 3. Department of Molecular Genetics, Oncode Institute, Erasmus MC, University Medical Center Rotterdam, 3015 GE Rotterdam, the Netherlands.
  • 4. Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo, 0372 Oslo, Norway.
  • 5. Department of Pathology, Oslo University Hospital, 0372 Oslo, Norway.
  • 6. Institute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK.
  • 7. Department of Cellular and Molecular Medicine and Ottawa Institute of Systems Biology, University of Ottawa, Ottawa, ON K1H 8M5, Canada.
  • 8. Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, 0379 Oslo, Norway. Electronic address: [email protected].
Abstract

Transcription-replication (T-R) conflicts cause replication stress and loss of genome integrity. However, the transcription-related processes that restrain such conflicts are poorly understood. Here, we demonstrate that the RNA polymerase II (RNAPII) C-terminal domain (CTD) Phosphatase protein Phosphatase 1 (PP1) nuclear targeting subunit (PNUTS)-PP1 inhibits replication stress. Depletion of PNUTS causes lower EdU uptake, S phase accumulation, and slower replication fork rates. In addition, the PNUTS binding partner WDR82 also promotes RNAPII-CTD dephosphorylation and suppresses replication stress. RNAPII has a longer residence time on chromatin after depletion of PNUTS or WDR82. Furthermore, the RNAPII residence time is greatly enhanced by Proteasome inhibition in control cells but less so in PNUTS- or WDR82-depleted cells, indicating that PNUTS and WDR82 promote degradation of RNAPII on chromatin. Notably, reduced replication is dependent on transcription and the phospho-CTD binding protein CDC73 after depletion of PNUTS/WDR82. Altogether, our results suggest that RNAPII-CTD dephosphorylation is required for the continuous turnover of RNAPII on chromatin, thereby preventing T-R conflicts.

Keywords
CDC73; CTD phosphorylation; Cancer; PNUTS; PP1 phosphatase; Proteasome-mediated degradation; RNA polymerase II; Replication stress; Transcription-replication conflicts; WDR82.