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

Abstract
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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

1. Tramantano M
2. Sun L
3. Au C
4. Labuz D
5. Liu Z
6. Chou M
7. Shen C
8. Luk E
(2016) Constitutive H2A.Z turnover at yeast promoters requires the preinitiation complex
Publicly available at the NCBI Short Read Archive (accession no: SRP051897).

http://www.ncbi.nlm.nih.gov/sra/?term=SRP051897
1. Tramantano M
2. Sun L
3. Au C
4. Labuz D
5. Liu Z
6. Chou M
7. Shen C
8. Luk E
(2015) The transcription preinitiation complex regulates the eviction of the histone variant H2A.Z at yeast promoters
Publicly available at the NCBI BioProject database (accession no: PRJNA271808).

http://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA271808

The following previously published data sets were used

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2. Pugh BF
(2009) A compiled and systematic reference map of nucleosome positions across the Saccharomyces
Journal website.

http://www.genomebiology.com/2009/10/10/R109
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(2014) Subnucleosomal Structures and Nucleosome Asymmetry across a Genome
Publicly available at the NCBI Short Read Archive (accession no: SRA059355).

http://www.ncbi.nlm.nih.gov/sra/?term=SRA059355
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2. Bruzzone MJ
3. Jacquet P
4. Falcone JL
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6. Shore D
(2015) Nucleosome Stability Distinguishes Two Different Promoter Types at All Protein-Coding Genes in Yeast
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE73337).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE73337
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(2009) Quantification of the yeast transcriptome by single-molecule sequencing
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http://www.ncbi.nlm.nih.gov/sra/?term=SRA008810
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Publicly available at the NCBI Short Read Archive (accession no: SRA046523).

http://www.ncbi.nlm.nih.gov/sra/?term=SRA046523

Article and author information

Author details

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.
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.
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.
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.
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.
Mindy Chou

Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

Competing interests
The authors declare that no competing interests exist.
Chen Shen

Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

Competing interests
The authors declare that no competing interests exist.
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.

"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.

Copyright

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.