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Ruler elements in chromatin remodelers set nucleosome array spacing and phasing.

ABSTRACT: Arrays of regularly spaced nucleosomes dominate chromatin and are often phased by alignment to reference sites like active promoters. How the distances between nucleosomes (spacing), and between phasing sites and nucleosomes are determined remains unclear, and specifically, how ATP-dependent chromatin remodelers impact these features. Here, we used genome-wide reconstitution to probe how Saccharomyces cerevisiae ATP-dependent remodelers generate phased arrays of regularly spaced nucleosomes. We find that remodelers bear a functional element named the 'ruler' that determines spacing and phasing in a remodeler-specific way. We use structure-based mutagenesis to identify and tune the ruler element residing in the Nhp10 and Arp8 modules of the INO80 remodeler complex. Generally, we propose that a remodeler ruler regulates nucleosome sliding direction bias in response to (epi)genetic information. This finally conceptualizes how remodeler-mediated nucleosome dynamics determine stable steady-state nucleosome positioning relative to other nucleosomes, DNA bound factors, DNA ends and DNA sequence elements.

SUBMITTER: Oberbeckmann E

PROVIDER: S-EPMC8163753 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Ruler elements in chromatin remodelers set nucleosome array spacing and phasing

Project description:Arrays of regularly spaced nucleosomes dominate chromatin and are often phased, i.e., aligned at reference sites like active promoters. How distances between nucleosomes and distances between phasing sites and nucleosomes are determined remained unclear, specifically, the role of ATP dependent chromatin remodelers in it. Here, we used a genome-wide reconstitution system to probe how yeast remodelers generate phased nucleosome arrays. We find that remodelers bear a structural element named the ‘ruler’ that sets nucleosome spacing, in the order Chd1 < ISW1a < ISW2 < INO80. Structure-based mutagenesis confirmed the functional significance of the ruler element in INO80. Differences in the ruler elements of different remodelers explain the observed nucleosome array features. More generally, we propose that remodelers use their rulers to regulate the direction of nucleosome sliding in response to nucleosome density and environment, leading to nucleosome positioning relative to other nucleosomes, DNA bound factors or DNA sequence elements.

2020-02-10 | GSE140614 | GEO

Ruler elements in chromatin remodelers set nucleosome array spacing and phasing

Project description:Ruler elements in chromatin remodelers set nucleosome array spacing and phasing

| PRJNA590247 | ENA

The ISW1 and CHD1 ATP-dependent chromatin remodelers compete to set nucleosome spacing in vivo.

Project description:Adenosine triphosphate-dependent chromatin remodeling machines play a central role in gene regulation by manipulating chromatin structure. Most genes have a nucleosome-depleted region at the promoter and an array of regularly spaced nucleosomes phased relative to the transcription start site. In vitro, the three known yeast nucleosome spacing enzymes (CHD1, ISW1 and ISW2) form arrays with different spacing. We used genome-wide nucleosome sequencing to determine whether these enzymes space nucleosomes differently in vivo We find that CHD1 and ISW1 compete to set the spacing on most genes, such that CHD1 dominates genes with shorter spacing and ISW1 dominates genes with longer spacing. In contrast, ISW2 plays a minor role, limited to transcriptionally inactive genes. Heavily transcribed genes show weak phasing and extreme spacing, either very short or very long, and are depleted of linker histone (H1). Genes with longer spacing are enriched in H1, which directs chromatin folding. We propose that CHD1 directs short spacing, resulting in eviction of H1 and chromatin unfolding, whereas ISW1 directs longer spacing, allowing H1 to bind and condense the chromatin. Thus, competition between the two remodelers to set the spacing on each gene may result in a highly dynamic chromatin structure.

| S-EPMC4889916 | biostudies-literature

The ISW1 and CHD1 ATP-dependent chromatin remodelers compete to set nucleosome spacing in vivo

Project description:We addressed the roles of three nucleosome spacing enzymes (ISW1, ISW2 and CHD1) in specifying chromatin organization in S. cerevisiae. Comparison of budding yeast nucleosome positions obtained using micrococcal nuclease digestion followed by paired-end sequencing (MNase-seq). We sequenced nucleosomes from isogenic strains with the isw1Î, isw2Î or chd1Î mutations in all combinations. We measured gene activity by ChIP-seq for the Rpb3 subunit of RNA polymerase II for some of these mutants.

2016-02-17 | E-GEOD-69400 | biostudies-arrayexpress

The ISW1 and CHD1 ATP-dependent chromatin remodelers compete to set nucleosome spacing in vivo

Project description:We addressed the roles of three nucleosome spacing enzymes (ISW1, ISW2 and CHD1) in specifying chromatin organization in S. cerevisiae.

2016-02-17 | GSE69400 | GEO

Nucleosome spacing and chromatin higher-order folding.

Project description:Packing of about two meters of the human genome DNA into chromatin occupying a several micron-sized cell nucleus requires a high degree of compaction in a manner that allows the information encoded on DNA to remain easily accessible. This packing is mediated by repeated coiling of DNA double helix around histones to form nucleosome arrays that are further folded into higher-order structures. Relatively straight DNA linkers separate the nucleosomes and the spacing between consecutive nucleosome varies between different cells and between different chromosomal loci. In a recent work ( 1) our group used a biochemically defined in vitro reconstituted system to explore how do various DNA linkers mediate nucleosome array packing into higher-order chromatin structures. For long nucleosome linkers (about 60 bp) we observed a more open chromatin structure and no effect of small linker length alterations (±2-4 bp) on chromatin folding. In striking contrast, for shorter linkers (20-32 bp) we found more compact packing with strong periodical dependence upon the linker DNA lengths. Our data together with high-resolution nucleosome position mapping provide evidence for the natural nucleosome repeats to support a chromatin architecture that, by default, restricts spontaneous folding of nucleosome arrays into compact chromatin fibers. We suggest that incomplete folding of the nucleosome arrays may promote global inter-array interactions that lead to chromatin condensation in metaphase chromosomes and heterochromatin.

| S-EPMC3515531 | biostudies-literature

Genome-wide nucleosome specificity and directionality of chromatin remodelers.

Project description:How chromatin remodelers cooperate to organize nucleosomes around the start and end of genes is not known. We determined the genome-wide binding of remodeler complexes SWI/SNF, RSC, ISW1a, ISW1b, ISW2, and INO80 to individual nucleosomes in Saccharomyces, and determined their functional contributions to nucleosome positioning through deletion analysis. We applied ultra-high-resolution ChIP-exo mapping to Isw2 to determine its subnucleosomal orientation and organization on a genomic scale. Remodelers interacted with selected nucleosome positions relative to the start and end of genes and produced net directionality in moving nucleosomes either away or toward nucleosome-free regions at the 5' and 3' ends of genes. Isw2 possessed a subnucleosomal organization in accord with biochemical and crystallographic-based models that place its linker binding region within promoters and abutted against Reb1-bound locations. Together, these findings reveal a coordinated position-specific approach taken by remodelers to organize genic nucleosomes into arrays.

| S-EPMC3397793 | biostudies-literature

Partitioned usage of chromatin remodelers by nucleosome-displacing factors.

Project description:Nucleosome-displacing-factors (NDFs) in yeast, similar to pioneer factors in higher eukaryotes, can open closed chromatin and generate nucleosome-depleted regions (NDRs). NDRs in yeast are also affected by ATP-dependent chromatin remodelers (CRs). However, how NDFs and CRs coordinate in nucleosome invasion and NDR formation is still unclear. Here, we design a high-throughput method to systematically study the interplay between NDFs and CRs. By combining an integrated synthetic oligonucleotide library with DNA methyltransferase-based, single-molecule nucleosome mapping, we measure the impact of CRs on NDRs generated by individual NDFs. We find that CRs are dispensable for nucleosome invasion by NDFs, and they function downstream of NDF binding to modulate the NDR length. A few CRs show high specificity toward certain NDFs; however, in most cases, CRs are recruited in a factor-nonspecific and NDR length-dependent manner. Overall, our study provides a framework to investigate how NDFs and CRs cooperate to regulate chromatin opening.

| S-EPMC9422437 | biostudies-literature

Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription.

Project description:Chromatin organization is essential for defining transcription units and maintaining genomic integrity in eukaryotes. In this study, we found that deletion of the Schizosaccharomyces pombe Chd1 chromatin remodelers, hrp1 and hrp3, causes strong, genome-wide accumulation of antisense transcripts. Nucleosome mapping revealed a specific role for Chd1 remodelers in the positioning of nucleosomes in gene coding regions. Other mutations associated with enhanced cryptic transcription activity, such as set2Δ, alp13Δ and FACT complex subunit pob3Δ, did not, or only mildly, affect nucleosome positioning. These data indicate several mechanisms in the repression of cryptic promoter activity in eukaryotic cells.

| S-EPMC3492713 | biostudies-literature

DNA topology in chromatin is defined by nucleosome spacing.

Project description:In eukaryotic nucleosomes, DNA makes ~1.7 superhelical turns around histone octamer. However, there is a long-standing discrepancy between the nucleosome core structure determined by x-ray crystallography and measurements of DNA topology in circular minichromosomes, indicating that there is only ~1.0 superhelical turn per nucleosome. Although several theoretical assumptions were put forward to explain this paradox by conformational variability of the nucleosome linker, none was tested experimentally. We analyzed topological properties of DNA in circular nucleosome arrays with precisely positioned nucleosomes. Using topological electrophoretic assays and electron microscopy, we demonstrate that the DNA linking number per nucleosome strongly depends on the nucleosome spacing and varies from -1.4 to -0.9. For the predominant {10n + 5} class of nucleosome repeats found in native chromatin, our results are consistent with the DNA topology observed earlier. Thus, we reconcile the topological properties of nucleosome arrays with nucleosome core structure and provide a simple explanation for the DNA topology in native chromatin with variable DNA linker length. Topological polymorphism of the chromatin fibers described here may reflect a more general tendency of chromosomal domains containing active or repressed genes to acquire different nucleosome spacing to retain topologically distinct higher-order structures.

| S-EPMC5659657 | biostudies-literature

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