Dataset Information

Ubiquitous nucleosome crowding in the yeast genome.

ABSTRACT: Nucleosomes may undergo a conformational change in which a stretch of DNA peels off the histone octamer surface as a result of thermal fluctuations or interactions with chromatin remodelers. Thus, neighboring nucleosomes may invade each other's territories by DNA unwrapping and translocation, or through initial assembly in partially wrapped states. A recent high-resolution map of distances between dyads of neighboring nucleosomes in Saccharomyces cerevisiae reveals that nucleosomes frequently overlap DNA territories of their neighbors. This conclusion is supported by lower-resolution maps of S. cerevisiae nucleosome lengths based on micrococcal nuclease digestion and paired-end sequencing. The average length of wrapped DNA follows a stereotypical pattern in genes and promoters, correlated with the well-known distribution of nucleosome occupancy: nucleosomal DNA tends to be shorter in promoters and longer in coding regions. To explain these observations, we have developed a biophysical model that uses a 10-11-bp periodic histone-DNA binding energy profile. The profile is based on the pattern of histone-DNA contacts in nucleosome crystal structures, as well as the idea of linker length discretization caused by higher-order chromatin structure. Our model is in agreement with the observed genome-wide distributions of interdyad distances, wrapped DNA lengths, and nucleosome occupancies. Furthermore, our approach explains in vitro measurements of the accessibility of nucleosome-covered target sites and nucleosome-induced cooperativity between DNA-binding factors. We rule out several alternative scenarios of histone-DNA interactions as inconsistent with the genomic data.

SUBMITTER: Chereji RV

PROVIDER: S-EPMC3986120 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Ubiquitous nucleosome crowding in the yeast genome.

Chereji Răzvan V RV Morozov Alexandre V AV

Proceedings of the National Academy of Sciences of the United States of America 20140324 14

Nucleosomes may undergo a conformational change in which a stretch of DNA peels off the histone octamer surface as a result of thermal fluctuations or interactions with chromatin remodelers. Thus, neighboring nucleosomes may invade each other's territories by DNA unwrapping and translocation, or through initial assembly in partially wrapped states. A recent high-resolution map of distances between dyads of neighboring nucleosomes in Saccharomyces cerevisiae reveals that nucleosomes frequently ov ...[more]

PMID: 24706846

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Project description:BackgroundRecently, a number of high-resolution genome-wide maps of nucleosome locations in S. cerevisiae have been derived experimentally. However, nucleosome positions are determined in vivo by the combined effects of numerous factors. Consequently, nucleosomes are not simple static units, which may explain the discrepancies in reported nucleosome positions as measured by different experiments. In order to more accurately depict the genome-wide nucleosome distribution, we integrated multiple nucleosomal positioning datasets using a multi-angle analysis strategy.ResultsTo evaluate the contribution of chromatin structure to transcription, we used the vast amount of available nucleosome analyzed data. Analysis of this data allowed for the comprehensive identification of the connections between promoter nucleosome positioning patterns and various transcription-dependent properties. Further, we characterised the function of nucleosome destabilisation in the context of transcription regulation. Our results indicate that genes with similar nucleosome occupancy patterns share general transcription attributes. We identified the local regulatory correlation (LRC) regions for two distinct types of nucleosomes and we assessed their regulatory properties. We also estimated the nucleosome reproducibility and measurement accuracy for high-confidence transcripts. We found that by maintaining a distance of approximately 13 bp between the upstream border of the +1 nucleosome and the transcription start sites (TSSs), the stable +1 nucleosome may form a barrier against the accessibility of the TSS and shape an optimum chromatin conformation for gene regulation. An in-depth analysis of nucleosome positioning in normally growing and heat shock cells suggested that the extent and patterns of nucleosome sliding are associated with gene activation.ConclusionsOur results, which combine different types of data, suggest that cross-platform information, including discrepancy and consistency, reflects the mechanisms of nucleosome packaging in vivo more faithfully than individual studies. Furthermore, nucleosomes can be divided into two classes according to their stable and dynamic characteristics. We found that two different nucleosome-positioning characteristics may significantly impact transcription programs. Besides, some positioned-nucleosomes are involved in the transition from stable state to dynamic state in response to abrupt environmental changes.

Dataset Information

Ubiquitous nucleosome crowding in the yeast genome.

Publications

Ubiquitous nucleosome crowding in the yeast genome.

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