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RNA binding by the histone methyltransferases Set1 and Set2

ABSTRACT: Histone methylation at H3K4 and H3K36 is commonly associated with genes actively transcribed by RNA polymerase II (RNAPII) and is catalyzed by Saccharomyces cerevisiae Set1 and Set2, respectively. Here we report that both methyltransferases can be UV cross-linked to RNA in vivo. High-throughput sequencing of the bound RNAs revealed strong Set1 enrichment near the transcription start site, whereas Set2 was distributed along pre-mRNAs. A subset of transcripts showed notably high enrichment for Set1 or Set2 binding relative to RNAPII, suggesting functional post-transcriptional interactions. In particular, Set1 was strongly bound to the SET1 mRNA, Ty1 retrotransposons, and noncoding RNAs from the ribosomal DNA (rDNA) intergenic spacers, consistent with its previously reported silencing roles. Set1 lacking RNA recognition motif 2 (RRM2) showed reduced in vivo cross-linking to RNA and reduced chromatin occupancy. In addition, levels of H3K4 trimethylation were decreased, whereas levels of dimethylation were increased. We conclude that RNA binding by Set1 contributes to both chromatin association and methyltransferase activity.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE89238 | GEO | 2017/05/18

SECONDARY ACCESSION(S): PRJNA350794

REPOSITORIES: GEO

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RNA binding by the histone methyltransferases Set1 and Set2

Project description:Histone methylation at H3K4 and H3K36 is commonly associated with genes actively transcribed by RNA polymerase II (RNAPII) and is catalyzed by Saccharomyces cerevisiae Set1 and Set2, respectively. Here we report that both methyltransferases can be UV cross-linked to RNA in vivo. High-throughput sequencing of the bound RNAs revealed strong Set1 enrichment near the transcription start site, whereas Set2 was distributed along pre-mRNAs. A subset of transcripts showed notably high enrichment for Set1 or Set2 binding relative to RNAPII, suggesting functional post-transcriptional interactions. In particular, Set1 was strongly bound to the SET1 mRNA, Ty1 retrotransposons, and noncoding RNAs from the ribosomal DNA (rDNA) intergenic spacers, consistent with its previously reported silencing roles. Set1 lacking RNA recognition motif 2 (RRM2) showed reduced in vivo cross-linking to RNA and reduced chromatin occupancy. In addition, levels of H3K4 trimethylation were decreased, whereas levels of dimethylation were increased. We conclude that RNA binding by Set1 contributes to both chromatin association and methyltransferase activity.

2017-05-17 | GSE87919 | GEO

Binding to RNA regulates Set1 function [CRAC-seq]

Project description:The Set1 family of histone H3 lysine 4 (H3K4) methyltransferases is highly conserved from yeast to humans. Here we show that the Set1 complex (Set1C) directly binds RNA in vitro through the regions that comprise the double RNA recognition motifs (dRRM) and N-SET domain within Set1 and its subunit Spp1. To investigate the functional relevance of RNA binding, we performed UV RNA cross-linking (CRAC) for Set1 and RNA polymerase II in parallel with ChIP-seq experiments. Set1 binds nascent transcripts through its dRRM. RNA binding is important to define the appropriate topology of Set1C distribution along transcription units and correlates with the efficient deposition of the H3K4me3 mark. In addition, we uncovered that Set1 binds to different classes of RNAs to levels that largely exceed the levels of binding to the general population of transcripts, suggesting the Set1 persists on these RNAs after transcription. This class includes RNAs derived from SET1, Ty1 retrotransposons, specific transcription factors genes and snRNAs. We propose that Set1 modulates adaptive responses, as exemplified by the posttranscriptional inhibition of Ty1 retrotransposition.

2017-10-03 | GSE104485 | GEO

Binding to RNA regulates Set1 function [ChIP-seq]

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The Set1 N-terminal domain and Swd2 interact with the RNA polymerase II CTD to recruit COMPASS

Project description:Methylation of histone H3 lysine 4 (H3K4) by the Set1/COMPASS complex is coupled with active transcription, and this modification is important for regulating gene expression. Set1/COMPASS associates with the RNA polymerase II (RNApII) C-terminal domain (CTD) to establish proper levels and distribution of H3K4 methylations.To ask how the Set1-RNApII CTD binding affects the occupancy and overall level of H3K4 methylations, ChIP-Seq was pefromed in cells transformed with full length or N-terminal truncated Set1. Our results indicate that Set1-RNApII CTD interaction is necessary for maintaining H3K4 methylations throughout the genes.

2019-10-02 | GSE138281 | GEO

Histone H3 lysine 4 trimethylation regulates RNA polymerase II promoter-proximal pause-release

Project description:Trimethylation of histone H3 lysine 4 (H3K4me3) is associated with transcriptional start sites and proposed to regulate transcription initiation. However, redundant functions of the H3K4 SET1/COMPASS methyltransferase complexes complicate elucidation of the specific role of H3K4me3 in transcriptional regulation. Here, we show that acute ablation of shared subunits of the SET1/COMPASS complexes leads to complete loss of all H3K4 methylation. H3K4me3 turnover occurs more rapidly than H3K4me1 and H3K4me2 and is dependent on KDM5 demethylases. Surprisingly, acute loss of H3K4me3 does not have detectable effects on transcriptional initiation but leads to a widespread decrease in transcriptional output, an increase in RNA polymerase II (RNAPII) pausing and slower elongation. Our study demonstrates a distinct role for H3K4me3 in transcriptional pause-release and elongation rather than transcriptional initiation.

2023-03-14 | PXD028858 | Pride

H3K4me3 regulates RNA polymerase II promoter-proximal pause-release

Project description:Trimethylation of histone H3 lysine 4 (H3K4me3) is associated with transcriptional start sites and proposed to regulate transcription initiation. However, redundant functions of the H3K4 SET1/COMPASS methyltransferase complexes complicate elucidation of the specific role of H3K4me3 in transcriptional regulation. Here, by using mouse embryonic stem cells (mESCs) as a model system, we show that acute ablation of shared subunits of the SET1/COMPASS complexes leads to complete loss of all H3K4 methylation. H3K4me3 turnover occurs more rapidly than H3K4me1 and H3K4me2 and is dependent on KDM5 demethylases. Surprisingly, acute loss of H3K4me3 does not have detectable effects on transcriptional initiation but leads to a widespread decrease in transcriptional output, an increase in RNA polymerase II (RNAPII) pausing and slower elongation. Notably, we show that H3K4me3 is required for the recruitment of the Integrator Complex Subunit 11 (INTS11), which is essential for the eviction of paused RNAPII and transcriptional elongation. Thus, our study demonstrates a distinct role for H3K4me3 in transcriptional pause-release and elongation rather than transcriptional initiation.

2023-02-10 | PXD039176 | Pride

Determinants of H3K4me pattern establishment

Project description:A hallmark of genes transcribed by RNA polymerase II (RNApII) is a "gradient" of histone H3 lysine 4 (H3K4) methylation. Various factors differentially bind to H3K4me3 near promoters, H3K4me2 just downstream, and H3K4me1 further downstream to modulate gene expression. Set1/COMPASS, the single S. cerevisiae H3K4 methyltransferase, binds transcribing RNApII, but COMPASS may also be allosterically regulated by specific subunits and histone H2B ubiquitylation. To ask whether differential H3K4 methylation is determined by regulated activity at specific gene locations or by the amount of time COMPASS spends near the nucleosome, ChIP-Seq analyses was performed in cells with altered transcription elongation rates or with Set1 fused to RNApII. Our results support a simple model where higher H3K4 methylations result from both increased duration and frequency of COMPASS proximity to the nucleosome.

2017-11-12 | GSE95356 | GEO

Regulation of chromatin structure by Set1 H3K4 methyltransferase and Jhd2 H3K4 demethylase [histone turnover]

Project description:Histone H3K4 methylation is connected to gene transcription from yeast to humans, but its mechanistic role in transcription and chromatin dynamics remains poorly understood. Here, we investigated the functions for Set1 and Jhd2, the sole H3K4 methyltransferase and H3K4 demethylase, respectively, in S. cerevisiae. Our data show that Set1 and Jhd2 predominantly co-regulate transcription. We find combined activities of Set1 and Jhd2 via H3K4 methylation contribute to positive or negative transcriptional regulation at shared target genes. Providing mechanistic insights, our data reveal that Set1 and Jhd2 together control nucleosomal occupancy during transcriptional co-regulation. Moreover, we find a remarkable genome-wide co-regulation of nucleosome and chromatin structure by Set1 and Jhd2 at different groups of transcriptionally active or inactive genes and at different regions within yeast genes. Overall, our study prompts a model wherein combined actions of Set1 and Jhd2 via H3K4 methylationâdemethylation control chromatin dynamics during various facets of transcriptional regulation. Genome-wide nucleosome maps were generated from three different yeast strains representing no tag control, 8V5-Set1 and Jhd2-12V5. Cells were cross-linked with formaldehyde, spheroplasted, nuclei were isolated and chromatin was prepared using micrococcal nuclease digestion, chromatin immunoprecipitation was performed using an epitope-tag specific antibody, libraries were prepared from ChIP and input DNA, sequenced, and analyzed separately.

2016-06-15 | E-GEOD-81021 | biostudies-arrayexpress

Regulation of chromatin structure by Set1 H3K4 methyltransferase and Jhd2 H3K4 demethylase [ChIP-seq]

Project description:Histone H3K4 methylation is connected to gene transcription from yeast to humans, but its mechanistic role in transcription and chromatin dynamics remains poorly understood. Here, we investigated the functions for Set1 and Jhd2, the sole H3K4 methyltransferase and H3K4 demethylase, respectively, in S. cerevisiae. Our data show that Set1 and Jhd2 predominantly co-regulate transcription. We find combined activities of Set1 and Jhd2 via H3K4 methylation contribute to positive or negative transcriptional regulation at shared target genes. Providing mechanistic insights, our data reveal that Set1 and Jhd2 together control nucleosomal occupancy during transcriptional co-regulation. Moreover, we find a remarkable genome-wide co-regulation of nucleosome and chromatin structure by Set1 and Jhd2 at different groups of transcriptionally active or inactive genes and at different regions within yeast genes. Overall, our study prompts a model wherein combined actions of Set1 and Jhd2 via H3K4 methylationâ??demethylation control chromatin dynamics during various facets of transcriptional regulation. Genome-wide nucleosome maps were generated from three different yeast strains representing no tag control, 8V5-Set1 and Jhd2-12V5. Cells were cross-linked with formaldehyde, spheroplasted, nuclei were isolated and chromatin was prepared using micrococcal nuclease digestion , chromatin immunoprecipitation was performed using an epitope-tag specific antibody, libraries were prepared from ChIP and input DNA, sequenced, and analyzed separately.

2016-06-15 | E-GEOD-81022 | biostudies-arrayexpress

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