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CBP regulates recruitment and release of promoter-proximal RNA polymerase II

ABSTRACT: Transcription activation involves RNA polymerase II (Pol II) recruitment and release from the promoter into productive elongation, but how specific chromatin regulators control these steps is unclear. Here we identify a novel activity of the histone acetyltransferase p300/CBP in regulating promoter-proximal paused Pol II. We find that Drosophila CBP (nejire) inhibition impedes transcription through the +1 nucleosome leading to accumulation of Pol II at this position on all expressed genes. Promoters strongly occupied by CBP and GAGA-factor have high levels of paused Pol II, a unique chromatin signature and strong expression regardless of cell type. Interestingly, CBP activity is rate-limiting for Pol II recruitment to these highly-paused promoters through an interaction with TFIIB, but for transit into elongation by histone acetylation at other genes. Thus, CBP directly stimulates both Pol II recruitment and the ability to traverse the first nucleosome, thereby promoting transcription of most genes. This SuperSeries is composed of the SubSeries listed below.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE100614 | GEO | 2017/10/20

SECONDARY ACCESSION(S): PRJNA392292

REPOSITORIES: GEO

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CBP regulates promoter-proximal RNA polymerase II

Project description:Transcription activation involves RNA polymerase II (Pol II) recruitment and release from the promoter into productive elongation, but how specific chromatin regulators control these steps is not fully understood. Here we identify a novel activity of the co-regulator and histone acetyltransferase p300/CBP in positioning promoter-proximal paused Pol II. We find that CBP inhibition impedes transcription through the +1 nucleosome, causing âdribblingâ of Pol II from the canonical pause site genome-wide. We further discovered that promoters strongly occupied by Drosophila CBP and GAGA-factor have high levels of paused Pol II, a unique chromatin signature and strong expression regardless of cell type. Interestingly, CBP activity is rate-limiting for Pol II recruitment to these highly-paused promoters but for transit into elongation at other genes. Thus, we uncover a key role forÂ CBP during transcription in directly controlling different rate-limiting steps depending on promoter features. Examination of transcriptional regulation with and without CBP inhibition for 10 minutes in Drosophila S2 cells. Two biological replicates for each condition.

2016-08-01 | E-GEOD-81649 | biostudies-arrayexpress

CBP regulates promoter-proximal RNA polymerase II

Project description:Transcription activation involves RNA polymerase II (Pol II) recruitment and release from the promoter into productive elongation, but how specific chromatin regulators control these steps is not fully understood. Here we identify a novel activity of the co-regulator and histone acetyltransferase p300/CBP in positioning promoter-proximal paused Pol II. We find that CBP inhibition impedes transcription through the +1 nucleosome, causing “dribbling” of Pol II from the canonical pause site genome-wide. We further discovered that promoters strongly occupied by Drosophila CBP and GAGA-factor have high levels of paused Pol II, a unique chromatin signature and strong expression regardless of cell type. Interestingly, CBP activity is rate-limiting for Pol II recruitment to these highly-paused promoters but for transit into elongation at other genes. Thus, we uncover a key role for CBP during transcription in directly controlling different rate-limiting steps depending on promoter features.

2016-08-01 | GSE81649 | GEO

RNA Polymerase II-associated factor 1 regulates the release and phosphorylation of paused RNA Polymerase II

Project description:Release of promoter-proximal paused RNA polymerase II (Pol II) during early elongation is a critical step in transcriptional regulation in metazoan cells. Paused Pol II release is thought to require the kinase activity of cyclin-dependent kinase 9 (CDK9) for the phosphorylation of DRB sensitivity-inducing factor, negative elongation factor, and C-terminal domain (CTD) serine-2 of Pol II. We found that Pol II-associated factor 1 (PAF1) is a critical regulator of paused Pol II release, that positive transcription elongation factor b (P-TEFb) directly regulates the initial recruitment of PAF1 complex (PAF1C) to genes, and that the subsequent recruitment of CDK12 is dependent on PAF1C. These findings reveal cooperativity among P-TEFb, PAF1C, and CDK12 in pausing release and Pol II CTD phosphorylation. Comparison of the chromatin occupancy of [1] PAF1, CDC73, LEO1, CTR9, total Pol II, and CTD serine 2-phosphorylated Pol II by ChIP-seq in THP1 cells; [2] PAF1, Pol II, Pol II (ser-5p), CDK12, and CDK9 by ChIP-seq in control and PAF1 knockdown cells; [3] LEO1 and Pol II by ChIP-seq in control and flavopiridol treated THP1 cells.

2015-12-11 | E-GEOD-62171 | biostudies-arrayexpress

RNA Polymerase II-associated factor 1 regulates the release and phosphorylation of paused RNA Polymerase II

2015-12-11 | GSE62171 | GEO

Drosophila TFIIB ChIP-seq after CBP inhibition

Project description:TFIIB chromatin binding is drastically reduced genome-wide after 10 min of CBP (also known as nejire) inhibition.

2017-10-20 | GSE100613 | GEO

Stable pausing by RNA polymerase II provides an opportunity to target and integrate regulatory signals

Project description:Metazoan gene expression is often regulated after the recruitment of RNA polymerase II (Pol II) to promoters, through the controlled release of promoter-proximally paused Pol II into productive RNA synthesis. Despite the prevalence of paused Pol II, very little is known about the dynamics of these early elongation complexes or the fate of short transcription start site-associated (tss) RNAs they produce. Here, we demonstrate that paused elongation complexes can be remarkably stable, with half-lives exceeding 15 minutes at genes with inefficient pause release. Promoter-proximal termination by Pol II is infrequent and released tssRNAs are targeted for rapid degradation. Further, we provide evidence that the predominant tssRNA species observed are nascent RNAs held within early elongation complexes. We propose that stable pausing of polymerase provides a temporal window of opportunity for recruitment of factors to modulate gene expression and that the nascent tssRNA represents an appealing target for these interactions. This submission includes 13 raw data files. Four samples (chromatin, soluble, mock-treated, and Rrp40-depleted) are represented by two biological replicate raw data files, while five samples (cells, DMSO, FP, mock-treated + FP, and Rrp-40depleted + FP) are represented by single raw data files.

2013-10-31 | E-GEOD-49078 | biostudies-arrayexpress

Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation: ChIP-chip data

Project description:Metazoan transcription is controlled through either coordinated recruitment of transcription machinery to the gene promoter, or subsequently, through regulated pausing of RNA polymerase II (Pol II) in early elongation. We report that a key difference between genes that use these distinct regulatory strategies lies in the chromatin architecture specified by their DNA sequences. Pol II pausing is prominent at highly-regulated genes whose sequences inherently disfavor nucleosome formation within the gene, but favor nucleosomal occlusion of the promoter. Pausing of polymerase maintains these genes in an active state by inhibiting the formation of repressive promoter chromatin. In contrast, promoters of housekeeping genes that lack paused Pol II are deprived of nucleosomes regardless of polymerase binding, but show higher nucleosome occupancy downstream. Our results suggest that the âdefaultâ chromatin state of a gene instructs its regulation, and that highly-regulated promoters have evolved to encourage competition between nucleosomes and paused Pol II for promoter occupancy. All experiments were done using two channels per chip, comparing DNA immunoprecipitated by the indicated antibody to matching input chromatin used for affinity purification. Where appropriate, replicate data sets were averaged.

2010-10-18 | E-GEOD-20471 | biostudies-arrayexpress

Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation: ChIP-chip data

Project description:Metazoan transcription is controlled through either coordinated recruitment of transcription machinery to the gene promoter, or subsequently, through regulated pausing of RNA polymerase II (Pol II) in early elongation. We report that a key difference between genes that use these distinct regulatory strategies lies in the chromatin architecture specified by their DNA sequences. Pol II pausing is prominent at highly-regulated genes whose sequences inherently disfavor nucleosome formation within the gene, but favor nucleosomal occlusion of the promoter. Pausing of polymerase maintains these genes in an active state by inhibiting the formation of repressive promoter chromatin. In contrast, promoters of housekeeping genes that lack paused Pol II are deprived of nucleosomes regardless of polymerase binding, but show higher nucleosome occupancy downstream. Our results suggest that the “default” chromatin state of a gene instructs its regulation, and that highly-regulated promoters have evolved to encourage competition between nucleosomes and paused Pol II for promoter occupancy.

2010-10-18 | GSE20471 | GEO

Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation: Expression data

Project description:Metazoan transcription is controlled through either coordinated recruitment of transcription machinery to the gene promoter, or subsequently, through regulated pausing of RNA polymerase II (Pol II) in early elongation. We report that a key difference between genes that use these distinct regulatory strategies lies in the chromatin architecture specified by their DNA sequences. Pol II pausing is prominent at highly-regulated genes whose sequences inherently disfavor nucleosome formation within the gene, but favor nucleosomal occlusion of the promoter. Pausing of polymerase maintains these genes in an active state by inhibiting the formation of repressive promoter chromatin. In contrast, promoters of housekeeping genes that lack paused Pol II are deprived of nucleosomes regardless of polymerase binding, but show higher nucleosome occupancy downstream. Our results suggest that the “default” chromatin state of a gene instructs its regulation, and that highly-regulated promoters have evolved to encourage competition between nucleosomes and paused Pol II for promoter occupancy.

2010-10-18 | GSE24133 | GEO

Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation: MNase-seq data

Project description:Metazoan transcription is controlled through either coordinated recruitment of transcription machinery to the gene promoter, or subsequently, through regulated pausing of RNA polymerase II (Pol II) in early elongation. We report that a key difference between genes that use these distinct regulatory strategies lies in the chromatin architecture specified by their DNA sequences. Pol II pausing is prominent at highly-regulated genes whose sequences inherently disfavor nucleosome formation within the gene, but favor nucleosomal occlusion of the promoter. Pausing of polymerase maintains these genes in an active state by inhibiting the formation of repressive promoter chromatin. In contrast, promoters of housekeeping genes that lack paused Pol II are deprived of nucleosomes regardless of polymerase binding, but show higher nucleosome occupancy downstream. Our results suggest that the "default" chromatin state of a gene instructs its regulation, and that highly-regulated promoters have evolved to encourage competition between nucleosomes and paused Pol II for promoter occupancy.

2010-10-18 | GSE22119 | GEO

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