1. Chromosomes and Gene Expression
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Live-cell single particle imaging reveals the role of RNA polymerase II in histone H2A.Z eviction

  1. Anand Ranjan
  2. Vu Q Nguyen
  3. Sheng Liu
  4. Jan Wisniewski
  5. Jee Min Kim
  6. Xiaona Tang
  7. Gaku Mizuguchi
  8. Ejlal Elalaoui
  9. Timothy J Nickels
  10. Vivian Jou
  11. Brian P English
  12. Qinsi Zheng
  13. Ed Luk
  14. Luke D Lavis
  15. Timothee Lionnet
  16. Carl Wu  Is a corresponding author
  1. Johns Hopkins University, United States
  2. National Cancer Institute, United States
  3. Janelia Research Campus, Howard Hughes Medical Institute, United States
  4. Stony Brook University, United States
  5. New York University, United States
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Cite this article as: eLife 2020;9:e55667 doi: 10.7554/eLife.55667

Abstract

The H2A.Z histone variant, a genome-wide hallmark of permissive chromatin, is enriched near transcription start sites in all eukaryotes. H2A.Z is deposited by the SWR1 chromatin remodeler and evicted by unclear mechanisms. We tracked H2A.Z in living yeast at single-molecule resolution, and found that H2A.Z eviction is dependent on RNA Polymerase II (Pol II) and the Kin28/Cdk7 kinase, which phosphorylates Serine 5 of heptapeptide repeats on the carboxy-terminal domain of the largest Pol II subunit Rpb1. These findings link H2A.Z eviction to transcription initiation, promoter escape and early elongation activities of Pol II. Because passage of Pol II through +1 nucleosomes genome-wide would obligate H2A.Z turnover, we propose that global transcription at yeast promoters is responsible for eviction of H2A.Z. Such usage of yeast Pol II suggests a general mechanism coupling eukaryotic transcription to erasure of the H2A.Z epigenetic signal.

Data availability

Imaging data have been deposited at Dryad and can be identified by doi:10.5061/dryad.43cp80c

The following data sets were generated

Article and author information

Author details

  1. Anand Ranjan

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Vu Q Nguyen

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sheng Liu

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jan Wisniewski

    Experimental Immunology Branch, National Cancer Institute, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jee Min Kim

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Xiaona Tang

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Gaku Mizuguchi

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ejlal Elalaoui

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Timothy J Nickels

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Vivian Jou

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Brian P English

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4037-6294
  12. Qinsi Zheng

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Ed Luk

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6619-2258
  14. Luke D Lavis

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Timothee Lionnet

    Langone Medical Center, Institute of System Genetics, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Carl Wu

    Department of Biology, Johns Hopkins University, Baltimore, United States
    For correspondence
    wuc@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6933-5763

Funding

National Institutes of Health (GM125831)

  • Carl Wu

National Institutes of Health (GM127538)

  • Timothee Lionnet

National Institutes of Health (GM104111)

  • Ed Luk

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

Reviewing Editor

  1. Geeta J Narlikar, University of California, San Francisco, United States

Publication history

  1. Received: January 31, 2020
  2. Accepted: April 24, 2020
  3. Accepted Manuscript published: April 27, 2020 (version 1)
  4. Version of Record published: May 29, 2020 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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