Cell Cycle–Specified Fluctuation of Nucleosome Occupancy at Gene Promoters
Open accessAbstract
The packaging of DNA into nucleosomes influences the accessibility of underlying regulatory information. Nucleosome occupancy and positioning are best characterized in the budding yeast Saccharomyces cerevisiae, albeit in asynchronous cell populations or on individual promoters such as PHO5 and GAL1-10. Using FAIRE (formaldehyde-assisted isolation of regulatory elements) and whole-genome microarrays, we examined changes in nucleosome occupancy throughout the mitotic cell cycle in synchronized populations of S. cerevisiae. Perhaps surprisingly, nucleosome occupancy did not exhibit large, global variation between cell cycle phases. However, nucleosome occupancy at the promoters of cell cycle-regulated genes was reduced specifically at the cell cycle phase in which that gene exhibited peak expression, with the notable exception of S-phase genes. We present data that establish FAIRE as a high-throughput method for assaying nucleosome occupancy. For the first time in any system, nucleosome occupancy was mapped genome-wide throughout the cell cycle. Fluctuation of nucleosome occupancy at promoters of most cell cycle-regulated genes provides independent evidence that periodic expression of these genes is controlled mainly at the level of transcription. The promoters of G2/M genes are distinguished from other cell cycle promoters by an unusually low baseline nucleosome occupancy throughout the cell cycle. This observation, coupled with the maintenance throughout the cell cycle of the stereotypic nucleosome occupancy states between coding and non-coding loci, suggests that the largest component of variation in nucleosome occupancy is "hard wired," perhaps at the level of DNA sequence.
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Tissue-specific gene expression can be dictated by tissue-specific transcription factor binding and by the tissue-specific recruitment of nucleosome-remodeling complexes to transcription factor occupied loci.
“These data, taken together with our expression analyses, indicate that tissue-specific gene expression can be dictated by tissue-specific transcription factor binding and by the tissue-specific recruitment of nucleosome-remodeling complexes (e.g., SWI/SNF) (Hogan et al. 2006;Schwabish and Struhl 2007) to transcription factor occupied loci.”
From Locus co-occupancy, nucleosome positioning, and H3K4me1 regulate the functionality of FOXA2-, HNF4A-, and PDX1-bound loci in islets and liver (2010) · cites this paper as Hogan et al. 2006
The Discussion (‘Nucleosome Occupancy: Cause or Effect?’; page unavailable) describes stepwise recruitment of Swi5, SWI/SNF, SAGA, and SBF at the yeast HO promoter. It does not establish tissue-specific recruitment or tissue-specific gene expression, and it says the proposed SWI/SNF-mediated nucleosome depletion may facilitate SBF binding rather than follow it. (LLM, conf=0.86)
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- Authors
- Hogan, G. J., Lee, C.-K., & Lieb, J. D.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Lieb, Jason D
- ORCID
- Lee, Cheol-Koo
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2006-09-22
- Volume
- 2
- Issue
- 9
- Pages
- e158
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC1570381
- OpenAlex
- W1983386103
- Cited by
- 109
- References
- 58
- Citations by year
- 2025: 2 · 2022: 2 · 2020: 3 · 2019: 3 · 2018: 4 · 2017: 4 · 2016: 8 · 2015: 3 · 2014: 10 · 2013: 7 · 2012: 7
- FWCI
- 4.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Frances C. and William P. Smallwood Foundation
- National Institutes of Health
- National Institute of General Medical Sciences (GM 072518, R01GM072518)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- nucleosome occupancy, cell cycle, promoter, Saccharomyces cerevisiae, FAIRE, mitotic cycle, cell cycle-regulated genes, transcriptional regulation, DNA accessibility, nucleosome positioning, genome-wide mapping
- MeSH terms
- Cell Cycle, Genes, Fungal, Histones, Lipoproteins, Mitosis, Molecular Sequence Data, Mutation, Nucleosomes, Pheromones, Promoter Regions, Genetic, Saccharomyces cerevisiae, Cell Adhesion Molecules, G1 Phase, G2 Phase, S Phase, Cyclins, Cyclin B, Saccharomyces cerevisiae Proteins, Microarray Analysis
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