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CHD1 in yeast is recruited by transcription elongation factors and maintains H3K4me3/H3K36me3 domains at actively transcribed and spliced genes

ABSTRACT: Chd1 is a conserved ATP-dependent chromatin remodeler that maintains the nucleosomal structure of chromatin, but the determinants of its specificity and its impact on gene expression are not well defined. To identify the determinants of Chd1 binding specificity in the yeast genome, we investigated Chd1 occupancy in mutants of several candidate factors. We found that several components of the PAF1 transcription elongation complex contribute to Chd1 recruitment to highly transcribed genes, and identified Spt4 as a factor that appears to negatively modulate Chd1 binding to chromatin. We discovered that CHD1 loss alters H3K4me3 and H3K36me3 patterns throughout the yeast genome. Interestingly, the aberrant histone H3 methylation patterns were predominantly observed within 1 kb from the transcription start site, where both histone H3 methylation marks co-occur. A reciprocal change between the two marks was obvious in the absence of Chd1, suggesting a role for CHD1 in establishing or maintaining the boundaries of these largely mutually exclusive histone marks. Strikingly, intron-containing genes were most susceptible to CHD1 loss, and exhibited a high degree of histone H3 methylation changes. Intron retention was significantly lower in the absence of CHD1, suggesting that CHD1 function as a chromatin remodeler could indirectly affect RNA splicing. This SuperSeries is composed of the SubSeries listed below.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE90998 | GEO | 2017/04/26

SECONDARY ACCESSION(S): PRJNA356615

REPOSITORIES: GEO

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A Key Role for Chd1 in Histone H3 Dynamics at the 3' Ends of Long Genes in Yeast (Flag-tagged histone H3 to total histone H3)

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Project description:Chd proteins are ATP-dependent chromatin remodeling enzymes implicated in biological functions from transcriptional elongation to control of pluripotency. Here, we examine roles of Chd1 in replication- independent dynamics of histone H3 in yeast. Using genome-wide ChIP on chip analysis, we find that Chd1 influences histone turnover at the 5’ and 3’ ends of genes, accelerating H3 replacement at the 5’ ends of genes while protecting the 3’ ends of genes from excessive H3 turnover. Although consistent with a direct role for Chd1 in exchange, these results may indicate that Chd1 stabilizes nucleosomes perturbed by transcription. Curiously, we observe a strong effect of gene length on Chd1’s effects on H3 turnover. Finally, we show that Chd1 also affects histone H3K4 and H3K36 methylation patterns over genes, likely as a consequence of its effects on histone replacement. In control experiments, we measure effects of deletion of CHD1 on RNA polymerase II distribution across the genome and on gene expression. We also examine the effect of deleting the TOP1 gene, alone and in combination with deletion of CHD1, on histone replacement. Taken together, our results emphasize a role for Chd1 in histone replacement in both budding yeast and Drosophila, and surprisingly show that the major effects of Chd1 on turnover occur at the 3’ ends of genes.

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Project description:Chd proteins are ATP-dependent chromatin remodeling enzymes implicated in biological functions from transcriptional elongation to control of pluripotency. Here, we examine roles of Chd1 in replication- independent dynamics of histone H3 in yeast. Using genome-wide ChIP on chip analysis, we find that Chd1 influences histone turnover at the 5’ and 3’ ends of genes, accelerating H3 replacement at the 5’ ends of genes while protecting the 3’ ends of genes from excessive H3 turnover. Although consistent with a direct role for Chd1 in exchange, these results may indicate that Chd1 stabilizes nucleosomes perturbed by transcription. Curiously, we observe a strong effect of gene length on Chd1’s effects on H3 turnover. Finally, we show that Chd1 also affects histone H3K4 and H3K36 methylation patterns over genes, likely as a consequence of its effects on histone replacement. In control experiments, we measure effects of deletion of CHD1 on RNA polymerase II distribution across the genome and on gene expression. We also examine the effect of deleting the TOP1 gene, alone and in combination with deletion of CHD1, on histone replacement. Taken together, our results emphasize a role for Chd1 in histone replacement in both budding yeast and Drosophila, and surprisingly show that the major effects of Chd1 on turnover occur at the 3’ ends of genes.

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Nucleosome recognition and DNA distortion by the Chd1 remodeler revealed at 2.6 Å resolution

Project description:Chromatin remodelers are ATP-dependent enzymes that reorganize nucleosomes within all eukaryotic genomes. The Chd1 remodeler specializes in shifting nucleosomes into evenly spaced arrays, a defining characteristic of chromatin in gene bodies that blocks spurious transcription initiation. Linked to some forms of autism and commonly mutated in prostate cancer, Chd1 is essential for maintaining pluripotency in stem cells. Here we report a complex of yeast Chd1 bound to a nucleosome in a nucleotide-free state, determined by cryo-electron microscopy (cryo-EM) to 2.6 Å resolution. The structure shows a bulge of the DNA tracking strand where the ATPase motor engages the nucleosome, consistent with an initial stage in DNA translocation. Unlike other remodeler-nucleosome complexes, nucleosomal DNA compensates for the remodeler-induced bulge with a bulge of the complementary DNA strand one helical turn downstream from the ATPase motor. Unexpectedly, the structure also reveals an N-terminal binding motif, called ChEx, which binds on the exit-side acidic patch of the nucleosome. The ChEx motif can displace a LANA-based peptide from the acidic patch, which suggests a means by which Chd1 remodelers may block competing chromatin remodelers from acting on the opposite side of the nucleosome.

2022-02-23 | PXD025287 | Pride

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