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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.

2022-08-30 | GSE207222 | GEO

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

| PRJNA756787 | ENA

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

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]

| PRJNA756789 | 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.

2016-09-08 | GSE72784 | GEO

key histone modifications in porcine oocytes and early embryos

Project description:Conservation and species specificity are both unveiled in the reprogramming process of epigenetic modifications in early embryos. Pig is important agricultural livestock that closely related to human life and understanding the mechanisms of epigenetic reprogramming in porcine embryos could be assistive to the pig breeding industry and also informative to human embryo research. Nevertheless, current knowledge of epigenetic reprogramming in porcine embryos is elusive. We profile H3K4me3, H3K27me3, and H3K27ac modifications in porcine oocytes and preimplant embryos. Our data reveal the existence of unusual broad H3K4me3 domains not only in oocytes but also expanded in pre-ZGA embryos and demonstrates the extensive transitions of unusual broad H3K4me3 domains and their roles during embryogenesis. Notably, broad H3K27me3 and H3K27ac enriched domains are found to be preferably colocalized in these broad H3K4me3 domains when comparing to it in mice and human. By knocking down KDM5B in pig embryos, cleavage and developments were disrupted as demonstrated in mouse.

2022-07-08 | GSE163709 | GEO

Chromatin remodeling in bovine oocytes and preimplantation embryos

Project description:Profiles of H3K4me3, H3K27ac, H3K27me3 and H3K9me3 in bovine GV oocytes and preimplantation embryos, and the characterization of chromatin accessibility in bovine blastocyst, inner cell mass and trophectoderm.

2023-02-16 | GSE193640 | GEO

Resetting histone modifications during human parental-to-zygotic transition

Project description:Histone modifications regulate gene expression and development. To address how they are reprogrammed in human early development, we investigated key histone marks in human oocytes and early embryos. Unlike that in mouse, the permissive mark H3K4me3 largely exhibits canonical patterns at promoters in human oocytes. After fertilization, pre-zygotic genome activation (ZGA) embryos acquire permissive chromatin and widespread H3K4me3 in CpG-rich regulatory regions. By contrast, the repressive mark H3K27me3 undergoes global depletion. CpG-rich regulatory regions then resolve to either active or repressed states upon ZGA, followed by subsequent restoration of H3K27me3 at developmental genes. Finally, through combining chromatin and transcriptome maps, we revealed transcription circuitry and asymmetric H3K27me3 patterning during early lineage specification. Collectively, our data unveil a priming phase connecting human parental-to-zygotic epigenetic transition.

2019-07-05 | GSE124718 | GEO

Histone deacetylase 1 maintains lineage integrity through histone acetylome refinement during early embryogenesis

Project description:Histone acetylation is a pivotal epigenetic modification that controls chromatin structures and regulates gene expression. It plays an essential role in modulating zygotic transcription and cell lineage specification of developing embryos. While the outcomes of many inductive signals have been described to require enzymatic activities of histone acetyltransferases and deacetylases (HDACs), the mechanisms by which HDACs confines the utilization of the zygotic genome are not well-characterized. Here, we show that histone deacetylase 1 (Hdac1) progressively binds to the zygotic genome from early blastula and onward. The recruitment of Hdac1 to the genome at the blastula stage is instructed maternally. Cis-regulatory modules (CRMs) bound by Hdac1 possess distinctive epigenetic signatures. We highlight a dual functional model of Hdac1 where Hdac1 not only sustains a histone hypoacetylation state on inactive chromatin but also participates in dynamic histone acetylation cycles on active chromatin. As a result, Hdac1 maintains differential histone acetylation states of bound CRMs between different germ layers and reinforces the transcriptional program underlying cell lineage identities both in time and space. Taken together, our study reveals a comprehensive role of Hdac1 during early vertebrate embryogenesis.

2023-03-27 | GSE198378 | GEO

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