Restriction of histone gene transcription to S phase by phosphorylation of a chromatin boundary protein
Open accessAbstract
The cell cycle-regulated expression of core histone genes is required for DNA replication and proper cell cycle progression in eukaryotic cells. Although some factors involved in histone gene transcription are known, the molecular mechanisms that ensure proper induction of histone gene expression during S phase remain enigmatic. Here we demonstrate that S-phase transcription of the model histone gene HTA1 in yeast is regulated by a novel attach–release mechanism involving phosphorylation of the conserved chromatin boundary protein Yta7 by both cyclin-dependent kinase 1 (Cdk1) and casein kinase 2 (CK2). Outside S phase, integrity of the AAA-ATPase domain is required for Yta7 boundary function, as defined by correct positioning of the histone chaperone Rtt106 and the chromatin remodeling complex RSC. Conversely, in S phase, Yta7 is hyperphosphorylated, causing its release from HTA1 chromatin and productive transcription. Most importantly, abrogation of Yta7 phosphorylation results in constitutive attachment of Yta7 to HTA1 chromatin, preventing efficient transcription post-recruitment of RNA polymerase II (RNAPII). Our study identified the chromatin boundary protein Yta7 as a key regulator that links S-phase kinases with RNAPII function at cell cycle-regulated histone gene promoters.
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Rtt106 recruitment to the histone promoters almost completely depends on Asf1, HIR and acetylation of histone H3 at K56 (H3K56Ac), and is limited by Yta7.
“Rtt106 recruitment to the histone promoters almost completely depends on Asf1, HIR and acetylation of histone H3 at K56 (H3K56Ac), and is limited by Yta7, a bromodomain- and AAA-ATPase domain-containing boundary protein31,32,35.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [35]
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- Authors
- Kurat, C. F., Lambert, J.-P., van Dyk, D., Tsui, K., van Bakel, H., Kaluarachchi, S., Friesen, H., Kainth, P., Nislow, C., Figeys, D., Fillingham, J., & Andrews, B. J.
- Affiliations
- University of Toronto (CA)
- University of Ottawa (CA)
- Toronto Metropolitan University (CA)
- ORCID
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-12-01
- Volume
- 25
- Issue
- 23
- Pages
- 2489-2501
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC3243059
- OpenAlex
- W2132447281
- Cited by
- 41
- References
- 67
- Citations by year
- 2026: 3 · 2025: 1 · 2023: 1 · 2022: 6 · 2021: 5 · 2020: 3 · 2019: 2 · 2018: 2 · 2017: 3 · 2015: 3 · 2014: 6 · 2013: 5 · 2012: 1
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (BMB-210972)
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- histone gene transcription, S phase, phosphorylation, cyclin-dependent kinase 1, casein kinase 2, histone chaperone, RNA polymerase II, cell cycle regulation, yeast
- MeSH terms
- Chromatin, Chromosomal Proteins, Non-Histone, Histones, Phosphorylation, Saccharomyces cerevisiae, Transcription, Genetic, S Phase, CDC2 Protein Kinase, Cell Cycle Proteins, Saccharomyces cerevisiae Proteins, Casein Kinase II
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