A stable mode of bookmarking by TBP recruits RNA Polymerase II to mitotic chromosomes

  1. Sheila S Teves  Is a corresponding author
  2. Luye An
  3. Aarohi Bhargava-Shah
  4. Liangqi Xie
  5. Xavier Darzacq
  6. Robert Tjian  Is a corresponding author
  1. University of California, Berkeley, United States
  2. Cornell University, United States

Abstract

Maintenance of transcription programs is challenged during mitosis when chromatin becomes condensed and transcription is silenced. How do the daughter cells re-establish the original transcription program? Here, we report that the TATA-binding protein (TBP), a key component of the core transcriptional machinery, remains bound globally to active promoters in mouse embryonic stem cells during mitosis. Using live-cell single-molecule imaging, we observed that TBP mitotic binding is highly stable, with an average residence time of minutes, in stark contrast to typical TFs with residence times of seconds. To test the functional effect of mitotic TBP binding, we used a drug-inducible degron system and found that TBP promotes the association of RNA Polymerase II with mitotic chromosomes, and facilitates transcriptional reactivation following mitosis. These results suggest that the core transcriptional machinery promotes efficient transcription maintenance globally.

Data availability

Sequencing data have been deposited in GEO under accession code GSE109964.

The following data sets were generated
The following previously published data sets were used
    1. Tveves SS
    2. Tjian R
    (2016) Global accessibility of mitotic chromosomes
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE85184).

Article and author information

Author details

  1. Sheila S Teves

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    sheila.teves@berkeley.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1220-2414
  2. Luye An

    Department of Biochemistry, Molecular, and Cell Biology, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  3. Aarohi Bhargava-Shah

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  4. Liangqi Xie

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  5. Xavier Darzacq

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2537-8395
  6. Robert Tjian

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    jmlim@berkeley.edu
    Competing interests
    Robert Tjian, One of the three founding funders of eLife and a member of eLife's Board of Directors..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0539-8217

Funding

Jane Coffin Childs Memorial Fund for Medical Research

  • Sheila S Teves

Howard Hughes Medical Institute

  • Robert Tjian

Siebel Stem Cell Institute

  • Sheila S Teves
  • Robert Tjian

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2018, Teves et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sheila S Teves
  2. Luye An
  3. Aarohi Bhargava-Shah
  4. Liangqi Xie
  5. Xavier Darzacq
  6. Robert Tjian
(2018)
A stable mode of bookmarking by TBP recruits RNA Polymerase II to mitotic chromosomes
eLife 7:e35621.
https://doi.org/10.7554/eLife.35621

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https://doi.org/10.7554/eLife.35621