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HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [ChIP-seq]

ABSTRACT: Zygotic genome activation (ZGA) is an impressed biological event following fertilization during early embryo development. Precise reprogramming of epigenetic modifications (e.g. histone H3 lysine 27 acetylation, H3K27ac) have been found contribute to safeguard ZGA in zebrafish and Drosophila, but the dynamic of H3K27ac and the underlying regulation mechanism in mammal embryos are still enigmatic yet. As the main erasers for histone acetylation, histone deacetylase 1 and 2 (HDAC1 and HDAC2) are reported essential for mouse oogenesis and embryo lineage development, while it is unclear if they are functional for ZGA. Here, we observed significant global decrease of H3K27ac during ZGA in both mouse and bovine embryos, and accumulation of HDAC1/2 is responsible for the decline of H3K27ac. Repression of HDAC1/2 by dominant negative mutation led to arrested development at late 2-cell stage in mouse embryos, accompanied by downregulation of genes supposed to be expressed during ZGA. ChIP-seq revealed abnormal distribution of H3K27ac, and DUX participates in H3K27ac aberrant hyper-acetylation in embryos overexpressed mutant HDAC1/2. Moreover, suppression of HDAC1/2 also restrains H3K4me3 removal at gene body regions via impeding expression of KDM5s during mouse ZGA, and compensatory exogenous Kdm5b mRNA can fix the exceeding H3K4me3 and failed ZGA. Intriguingly, function of HDAC1/2 seems to be conservative between mouse and bovine embryos. Together, this study reveals that HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3.

ORGANISM(S): Mus musculus

PROVIDER: GSE182554 | GEO | 2022/05/21

REPOSITORIES: GEO

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HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [RNA-seq]

Project description:Zygotic genome activation (ZGA) is an impressed biological event following fertilization during early embryo development. Precise reprogramming of epigenetic modifications (e.g. histone H3 lysine 27 acetylation, H3K27ac) have been found contribute to safeguard ZGA in zebrafish and Drosophila, but the dynamic of H3K27ac and the underlying regulation mechanism in mammal embryos are still enigmatic yet. As the main erasers for histone acetylation, histone deacetylase 1 and 2 (HDAC1 and HDAC2) are reported essential for mouse oogenesis and embryo lineage development, while it is unclear if they are functional for ZGA. Here, we observed significant global decrease of H3K27ac during ZGA in both mouse and bovine embryos, and accumulation of HDAC1/2 is responsible for the decline of H3K27ac. Repression of HDAC1/2 by dominant negative mutation led to arrested development at late 2-cell stage in mouse embryos, accompanied by downregulation of genes supposed to be expressed during ZGA. ChIP-seq revealed abnormal distribution of H3K27ac, and DUX participates in H3K27ac aberrant hyper-acetylation in embryos overexpressed mutant HDAC1/2. Moreover, suppression of HDAC1/2 also restrains H3K4me3 removal at gene body regions via impeding expression of KDM5s during mouse ZGA, and compensatory exogenous Kdm5b mRNA can fix the exceeding H3K4me3 and failed ZGA. Intriguingly, function of HDAC1/2 seems to be conservative between mouse and bovine embryos. Together, this study reveals that HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3.

2022-05-21 | GSE182553 | GEO

Dynamic landscapes of H3K27ac in mouse preimplantation embryos

Project description:Histone acetylation H3K27ac is a well-established chromatin marker for active enhancers and promoters. However, reprogramming dynamics of H3K27ac during maternal-to-zygotic transition (MZT) in mammalian embryos has not been well studied. By profiling the allelic landscape of H3K27ac during mouse MZT, here we show that H3K27ac undergoes three waves of rapid global transitions from oocyte to 2-cell stages. Notably, germinal vesicle (GV) oocyte and zygote are globally hyperacetylated by forming noncanonical broad H3K27ac domains that correlate with broad H3K4me3 and open chromatin. H3K27ac also marks genomic regions primed for activation including ZGA gene promoters, retrotransposons, and active alleles of imprinted genes. Importantly, both CBP/p300 and HDAC activities play important roles in regulating the H3K27ac dynamics and are essential for pre-implantation development. Specifically, CBP/p300 deposits broad H3K27ac domains in zygotes and open condensed chromatin at putative enhancers to ensure proper ZGA. In contrast, HDACs mediate the broad to canonical H3K27ac transition to safeguard ZGA by preventing premature expression of developmental genes and promoting ZGA gene activation. Our study demonstrates that coordinated activities of CBP/p300 and HDACs during mouse MZT are essential for ZGA and mouse pre-implantation development.

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HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3

Project description:HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3

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HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [RNA-seq]

Project description:HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [RNA-seq]

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HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [ChIP-seq]

Project description:HDAC1/2 is indispensable for mouse and bovine ZGA via regulating distribution of H3K27ac and H3K4me3 [ChIP-seq]

| PRJNA756788 | ENA

Unique Broad Histone Lysine 4 Methylation Domains in Mouse Oocytes and Dynamic Regulation during Maternal to Zygotic Transition

Project description:The maternal to zygotic transition (MZT) involves the transfer of genome regulation from the oocyte to the embryo and is essential for the formation of totipotent embryos. However, regulatory mechanisms are still poorly understood despite recent progress in mapping the dynamics in RNA transcripts and DNA methylation1-9. Previous studies suggest that dynamic histone modifications may play important roles in MZT10-12, however direct measurements of chromatin states has been hindered by technical difficulties in profiling histone modifications from small quantities of cells. We have developed a micro-scale chromatin immunoprecipitation and sequencing (μChIP-seq) method and used it to profile histone H3 lysine methylation (H3K4me3) and acetylation (H3K27ac) genome-wide in the mouse oocyte, 2- cell and 8-cell stage embryo. Strikingly, we show that ~22% of the oocyte genome is associated with broad H3K4me3 domains that are anti-correlated with DNA methylation. Most H3K4me3 signal is rapidly lost and constricted to TSS regions in 2-cell embryos, concomitant with the onset of major zygotic genome activation (ZGA). We provide evidence that these broad H3K4me3 domains are established by Mll2 and actively removed by Kdm5a and Kdm5b, and likely play instrumental roles in MZT by defining regions of DNA demethylation in oocytes and the 2-cell embryo. Furthermore, broad H3K4me3 domains specify H3K27ac patterns in the early embryo and ZGA genes are generally related to broad H3K4me3 domains, suggesting a fundamental role in MZT. Our results provide insights into how the developmental program can be set up in the oocyte and transferred to the zygotic genome.

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Project description:Zygotic gene activation (ZGA) is the first transcription event in life, and is associated with extensive epigenetic reprogramming, which is involved with dynamic incorporation of histone variant H3.3. H3.3 plays essential roles during mouse pre-implantation development. However, the coexistence of distinct sources of H3.3 in early embryos, including paternal and maternal allele-expressed H3.3 (paH3.3 and maH3.3), complicates our ability to track their individual dynamics, which may have distinct roles in embryonic development. In this study, by taking advantage of our H3.3B-HA-tagged mouse model, we illustrated the paH3.3 and maH3.3 landscapes in mouse early embryos, and described the manner of maternal mRNAs-derived H3.3 (mH3.3) on paternal genome reprogramming. We found the deposition of mH3.3 is required for cleavage development and minor ZGA, mechanistically, by mH3.3S31p-meditated acetylation at lysine 27. And, we propose that the mH3.3K27ac modification displaces the repressive histone modifications, thus enabling the activation of minor ZGA genes. Taken together, we demonstrate the central role of mH3.3 in reprogramming parental genomes by establishment of H3K27ac.

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2024-09-12 | GSE242958 | GEO

key histone modifications in porcine oocytes and early embryos

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