Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex

  1. Michael Tramantano
  2. Lu Sun
  3. Christy Au
  4. Daniel Labuz
  5. Zhimin Liu
  6. Mindy Chou
  7. Chen Shen
  8. Ed Luk  Is a corresponding author
  1. Stony Brook University, United States
  2. Cold Spring Harbor Laboratory, United States

Abstract

The assembly of the preinitiation complex (PIC) occurs upstream of the +1 nucleosome which, in yeast, obstructs the transcription start site and is frequently assembled with the histone variant H2A.Z. To understand the contribution of the transcription machinery in the disassembly of the +1 H2A.Z nucleosome, conditional mutants were used to block PIC assembly. A quantitative ChIP-seq approach, which allows detection of global occupancy change, was employed to measure H2A.Z occupancy. Blocking PIC assembly resulted in promoter-specific H2A.Z accumulation, indicating that the PIC is required to evict H2A.Z. By contrast, H2A.Z eviction was unaffected upon depletion of INO80, a remodeler previously reported to displace nucleosomal H2A.Z. Robust PIC-dependent H2A.Z eviction was observed at active and infrequently transcribed genes, indicating that constitutive H2A.Z turnover is a general phenomenon. Finally, sites with strong H2A.Z turnover precisely mark transcript starts, providing a new metric for identifying cryptic and alternative sites of initiation.

Data availability

The following data sets were generated
The following previously published data sets were used
    1. Rhee HS
    2. et al.
    (2014) Subnucleosomal Structures and Nucleosome Asymmetry across a Genome
    Publicly available at the NCBI Short Read Archive (accession no: SRA059355).
    1. Raz LD et al.
    (2009) Quantification of the yeast transcriptome by single-molecule sequencing
    Publicly available at the NCBI Short Read Archive (accession no: SRA008810).

Article and author information

Author details

  1. Michael Tramantano

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Lu Sun

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Christy Au

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Daniel Labuz

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zhimin Liu

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mindy Chou

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Chen Shen

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ed Luk

    Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United States
    For correspondence
    ed.luk@stonybrook.edu
    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

Funding

National Institute of General Medical Sciences (RO1 GM104111)

  • Ed Luk

National Institute of General Medical Sciences (T32 GM008468)

  • Michael Tramantano

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

Reviewing Editor

  1. Julie Ahringer, University of Cambridge, United Kingdom

Version history

  1. Received: January 6, 2016
  2. Accepted: July 12, 2016
  3. Accepted Manuscript published: July 20, 2016 (version 1)
  4. Version of Record published: August 23, 2016 (version 2)

Copyright

© 2016, Tramantano 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. Michael Tramantano
  2. Lu Sun
  3. Christy Au
  4. Daniel Labuz
  5. Zhimin Liu
  6. Mindy Chou
  7. Chen Shen
  8. Ed Luk
(2016)
Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex
eLife 5:e14243.
https://doi.org/10.7554/eLife.14243

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https://doi.org/10.7554/eLife.14243

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