Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo

Zhang, Yong; Moqtaderi, Zarmik; Rattner, Barbara P.; Euskirchen, Ghia; Snyder, M; Kadonaga, James T.; Liu, X Shirley; Struhl, Kevin

doi:10.1038/nsmb.1636

Cited by 341 publications

(563 citation statements)

References 34 publications

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“…Altogether our results agree with the central conclusions of recent experimental in vitro and in vivo studies of nucleosome positioning in S. cerevisiae (Zhang et al 2009), which provide additional evidence that intrinsic histone-DNA interactions make only a modest contribution to the in vivo intragenic nucleosome positioning pattern, the major determinant being the statistical ordering mainly induced by the excluding NFRs located at gene extremities.…”

Section: Proof Onlysupporting

confidence: 81%

Thermodynamics of Intragenic Nucleosome Ordering

et al. 2009

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Numerous AU2studies of chromatin structure showed that nucleosome free regions (NFRs) located at 59 gene ends contribute to transcription initiation regulation. Here, we determine the role of intragenic chromatin structure on gene expression regulation. We show that, along Saccharomyces cerevisiae genes, nucleosomes are highly organized following two types of architecture that depend only on the distance between the NFRs located at the 59 and 39 gene ends. In the first type, this distance constrains in vivo the positioning of n nucleosomes regularly organized in a ''crystal-like'' array. In the second type, this distance is such that the corresponding genes can accommodate either n or (n + 1) nucleosomes, thereby displaying two possible crystal-like arrays of n weakly compacted or n + 1 highly compacted nucleosomes. This adaptability confers ''bistable'' properties to chromatin and is a key to its dynamics. Compared to crystal-like genes, bi-stable genes present higher transcriptional plasticity, higher sensitivity to chromatin regulators, higher H3 turnover rate, and lower H2A.Z enrichment. The results strongly suggest that transcription elongation is facilitated by higher chromatin compaction. The data allow us to propose a new paradigm of transcriptional control mediated by the stability and the level of compaction of the intragenic chromatin architecture and open new ways for investigating eukaryotic gene expression regulation.

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Section: Proof Onlysupporting

confidence: 81%

Thermodynamics of Intragenic Nucleosome Ordering

et al. 2009

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“…For instance, Kaplan et al (23) concluded from genome-scale nucleosome mapping that intrinsic nucleosome sequence preferences have a dominant role in determining nucleosome organization in vivo. Shortly after this study, Zhang et al (24) reported a similar study on in vivo and in vitro assembled yeast chromatin, but using a somewhat different methodology. They and others (24,25) concluded that intrinsic histone-DNA interactions are not the major determinant of nucleosome positioning, but rather of nucleosome occupancy.…”

mentioning

confidence: 95%

“…Shortly after this study, Zhang et al (24) reported a similar study on in vivo and in vitro assembled yeast chromatin, but using a somewhat different methodology. They and others (24,25) concluded that intrinsic histone-DNA interactions are not the major determinant of nucleosome positioning, but rather of nucleosome occupancy. Positioning and occupancy of nucleosomes are closely related concepts; nucleosome positioning is the distribution of individual nucleosomes along the DNA sequence and can be thought of in terms of a single reference point on the nucleosome, such as its dyad of symmetry (9,26).…”

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confidence: 95%

Sequence-based prediction of single nucleosome positioning and genome-wide nucleosome occupancy

Heijden

Vugt

Logie

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Nucleosome positioning dictates eukaryotic DNA compaction and access. To predict nucleosome positions in a statistical mechanics model, we exploited the knowledge that nucleosomes favor DNA sequences with specific periodically occurring dinucleotides. Our model is the first to capture both dyad position within a few base pairs, and free binding energy within 2 kBT, for all the known nucleosome positioning sequences. By applying Percus’s equation to the derived energy landscape, we isolate sequence effects on genome-wide nucleosome occupancy from other factors that may influence nucleosome positioning. For both in vitro and in vivo systems, three parameters suffice to predict nucleosome occupancy with correlation coefficients of respectively 0.74 and 0.66. As predicted, we find the largest deviations in vivo around transcription start sites. This relatively simple algorithm can be used to guide future studies on the influence of DNA sequence on chromatin organization.

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“…Although several studies demonstrated that the intrinsic nucleosome organization determines many aspects of the nucleosome organization in vivo Zhang et al 2009), much less is known about the effect of the intrinsic organization on transcription. Our results thus suggest that intrinsic nucleosome organization may be an important component of the mapping between DNA sequence and transcription, and that changes in the DNA-encoded nucleosome organization of promoters may be a key genetic mechanism by which promoter activity changes are tuned during evolution ).…”

Section: Conclusion and Discussionmentioning

confidence: 99%

Compensation for differences in gene copy number among yeast ribosomal proteins is encoded within their promoters

Zeevi¹,

Sharon²,

Lotan-Pompan³

et al. 2011

Genome Res.

105

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Coordinate regulation of ribosomal protein (RP) genes is key for controlling cell growth. In yeast, it is unclear how this regulation achieves the required equimolar amounts of the different RP components, given that some RP genes exist in duplicate copies, while others have only one copy. Here, we tested whether the solution to this challenge is partly encoded within the DNA sequence of the RP promoters, by fusing 110 different RP promoters to a fluorescent gene reporter, allowing us to robustly detect differences in their promoter activities that are as small as~10%. We found that single-copy RP promoters have significantly higher activities, suggesting that proper RP stoichiometry is indeed partly encoded within the RP promoters. Notably, we also partially uncovered how this regulation is encoded by finding that RP promoters with higher activity have more nucleosome-disfavoring sequences and characteristic spatial organizations of these sequences and of binding sites for key RP regulators. Mutations in these elements result in a significant decrease of RP promoter activity. Thus, our results suggest that intrinsic (DNA-dependent) nucleosome organization may be a key mechanism by which genomes encode biologically meaningful promoter activities. Our approach can readily be applied to uncover how transcriptional programs of other promoters are encoded.

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Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo

Cited by 341 publications

References 34 publications

Thermodynamics of Intragenic Nucleosome Ordering

Thermodynamics of Intragenic Nucleosome Ordering

Sequence-based prediction of single nucleosome positioning and genome-wide nucleosome occupancy

Compensation for differences in gene copy number among yeast ribosomal proteins is encoded within their promoters

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