Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae

Lantermann, Alexandra B.; Straub, Tobias; Strålfors, Annelie; Yuan, Guo‐Cheng; Ekwall, Karl; Korber, Philipp

doi:10.1038/nsmb.1741

Cited by 230 publications

(323 citation statements)

References 55 publications

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“…This reflects the fact that in vitro reconstitutions are performed in the absence of other factors and that possible variations in post-translational modification are statistically distributed over all the nucleosomes, whereas in natively assembled chromatin, variations in histone content are due to biochemical activities recruited to specific DNA loci. The average distribution of nucleosomes around transcription start sites (TSS) is regulated in vivo (52)(53)(54)(55). In yeast and other eukaryotic cells, the þ1 nucleosome is well positioned and the degree of positioning decreases progressively downstream in the coding region.…”

Section: Resultsmentioning

confidence: 99%

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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Section: Resultsmentioning

confidence: 99%

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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“…In vivo, this can vary from ∼154 bp in Schizosaccharomyces pombe chromatin (Lantermann et al 2010) to ∼240 bp in the sperm of certain echinoderms (Spadafora et al 1976;Zalenskaya et al 1981;, the most widespread naturally occurring NRLs being in the range of 186-208 bp. However, the NRLs reported for in vivo chromatin fibers are average values and do not necessarily imply regular spacing of nucleosomes.…”

Section: -Nm Fibermentioning

confidence: 99%

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

Muskhelishvili

Travers

2016

Biophys Rev

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We argue that dynamic changes in DNA supercoiling in vivo determine both how DNA is packaged and how it is accessed for transcription and for other manipulations such as recombination. In both bacteria and eukaryotes, the principal generators of DNA superhelicity are DNA translocases, supplemented in bacteria by DNA gyrase. By generating gradients of superhelicity upstream and downstream of their site of activity, translocases enable the differential binding of proteins which preferentially interact with respectively more untwisted or more writhed DNA. Such preferences enable, in principle, the sequential binding of different classes of protein and so constitute an essential driver of chromatin organization.Keywords DNA supercoiling . DNA translocases . Chromatin organization . Superhelicity gradients . DNA untwisting . DNAwrithing Dynamic changes of DNA supercoiling act as a driving force behind the alterations of genetic activity and DNA compaction both in eukaryotes and prokaryotes. Both these processes involve formation of spatially organized nucleoprotein structures by DNA architectural proteins. Whereas in eukaryotes the paradigmal example is the histone octamer, in prokaryotes a similar function is attributed to a small class of highly abundant nucleoid-associated proteins. We argue that, depending on the primary sequence organization, the changes of superhelicity elicit various alterations of local DNA geometry, while these, in turn, facilitate the assembly of distinct nucleoprotein structures pertinent to genetic function. Genome-wide conversion of the superhelical energy into various three-dimensional DNA structures thus acts as an analogue code coordinating the energy supply with the genetic expression of the chromosome.Recent studies make it increasingly clear that the DNA double helix carries at least two types of encoded information and that these include the well-known genetic code and the structural information determining the form and physical properties of the double helix itself. Since both these information types are inscribed in the same DNA sequence, and yet one is discrete whereas the other is continuous, they have been respectively dubbed the digital and analog DNA codes (Marr et al. 2008;Travers et al. 2012;Muskhelishvili and Travers 2013). The potential of the DNA to adopt distinct configurations is strongly modulated by DNA supercoiling, which is increasingly recognized as one of the major forces coordinating the cellular DNA transactions in both prokaryotes (including Archaea) and eukaryotes.DNA supercoiling can be generated by the simple application of torque to the double helix (Strick et al. 1998) but, importantly, because the DNA molecule itself possesses chirality-it is, after all, a right-handed double helix-the local structures stabilized by changes in superhelical density depend on both the sign and strength of the applied torque. For example, both positive and negative torque (respectively overand underwinding of the double helix) can change the intrinsic coiling of ...

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“…Since the earliest studies on baker's yeast, inquiries into nucleosome positioning have been extended to the genomes of many other organisms, such as Schizosaccharomyces pombe (21) and various other species of yeast (22), Caenorhabditis elegans (23,24), Plasmodium falciparum (25), flies (26), zebrafish (27), Arabidopsis thaliana (28), mice (29,30), and humans (30)(31)(32)(33)(34)(35). Most of these studies were conducted in vivo, and therefore do not allow for isolation of effects encoded into the genomic sequences.…”

Section: Introductionmentioning

confidence: 99%

“…An important role is also played by the active regulation of transcription. In yeast, the promoters of actively transcribed genes show much more pronounced nucleosome depletion than those of inactive genes (21).…”

Section: Introductionmentioning

confidence: 99%

Genomes of Multicellular Organisms Have Evolved to Attract Nucleosomes to Promoter Regions

Tompitak

Vaillant

Schiessel

2017

Biophysical Journal

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Sequences that influence nucleosome positioning in promoter regions, and their relation to gene regulation, have been the topic of much research over the last decade. In yeast, significant nucleosome-depleted regions are found, which facilitate transcription. With the arrival of nucleosome positioning maps for the human genome, it was discovered that in our genome, unlike in that of yeast, promoters encode for high nucleosome occupancy. In this work, we look at the genomes of a range of different organisms, to provide a catalog of nucleosome positioning signals in promoters across the tree of life. We utilize a computational model of the nucleosome, based on crystallographic analyses of the structure and elasticity of the nucleosome, to predict the nucleosome positioning signals in promoter regions. To be able to apply our model to large genomic datasets, we introduce an approximative scheme that makes use of the limited range of correlations in nucleosomal sequence preferences to create a computationally efficient approximation of the full biophysical model. Our predictions show that a clear distinction between unicellular and multicellular life is visible in the intrinsically encoded nucleosome affinity. Furthermore, the strength of the nucleosome positioning signals correlates with the complexity of the organism. We conclude that encoding for high nucleosome occupancy, as in the human genome, is in fact a universal feature of multicellular life.

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Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae

Cited by 230 publications

References 55 publications

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

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

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

Genomes of Multicellular Organisms Have Evolved to Attract Nucleosomes to Promoter Regions

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