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Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals

ABSTRACT: Embryonic development yields many different cell types in response to just a few families of inductive signals. The property of signal-receiving cells that determines how they respond to inductive signals is known as competence, and it differs in different cell types. Here, we explore the ways in which maternal factors modify chromatin to specify initial competence in the frog Xenopus tropicalis. We identify early-engaged regulatory DNA sequences, and infer from them critical activators of the zygotic genome. Of these, we show that the pioneering activity of the maternal pluripotency factors Pou5f3 and Sox3 determines competence for germ layer formation by extensively remodelling compacted chromatin before the onset of inductive signalling. This remodelling includes the opening and marking of thousands of regulatory elements, extensive chromatin looping, and the co-recruitment of signal-mediating transcription factors. Our work identifies significant developmental principles that inform our understanding of how pluripotent stem cells interpret inductive signals.

ORGANISM(S): Xenopus tropicalis

PROVIDER: GSE113186 | GEO | 2019/04/16

REPOSITORIES: GEO

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Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals

Project description:Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals

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Project description:The emergence of distinct cell types during embryonic development relies on the ability of progenitor cells to properly interpret environmental cues; yet how this developmental competence is established is unknown. Here we show that epigenetic priming of enhancers signifies developmental competence. Chromatin mapping during endodermal lineage diversification of human pluripotent stem cells revealed en masse acquisition of a poised chromatin state at enhancers for multiple descendant lineages in developmental intermediates. The responsiveness of developmental intermediates to lineage-inductive signals is dependent on a poised enhancer state. We further find that lineage-specific enhancers are first recognized by transcription factors involved in chromatin priming, while subsequent recruitment of lineage-inductive transcription factors leads to enhancer and target gene activation. Together, our results identify acquisition of a poised chromatin state at enhancers as a general mechanism by which progenitor cells gain the competence to rapidly activate lineage-specific genes in response to inductive signals.

2015-03-31 | GSE54471 | GEO

Pou5f3 and Sox19b select gene expression repertoire at zebrafish Zygotic Genome Activation

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Project description:Pioneer transcription factors Nanog, Pou5f3 and Sox19b promote chromatin accessibility on the enhancers of the early zebrafish embryos. It is poorly understood how they act together; it is commonly assumed that they act additively or cooperatively to clear chromatin from the nucleosomes. We investigated this question by comparing chromatin accessibility (Omni ATAC-seq) in seven mutant genotypes: single, double and triple maternal-zygotic mutants by Pou5f3, Sox19b and Nanog, and the wild-type embryos. We found, that at most of the directly bound sites, either Pou or Nanog is required for chromatin accessibility; while at the minority of the sites two factors act additively. Further, on the sites, where Pou5f3 promotes chromatin accessibility, Nanog often suppresses it, and vice versa. To explain this phenomenon, we suggest a model of nucleosome-mediated competition between pioneer transcription factors: Pou5f3 and Nanog compete for the same binding motif on the DNA, but only one of the factors has a pioneer activity on this site. This entry contains only part fo the Omni-ATAC-seq experiments, the other part is in the previously released entry GSE188364.

2023-08-02 | GSE215956 | GEO

ATAC-seq identifies accessible chromatin domains in gastrula stage Xenopus laevis

Project description:In the embryo, inductive cues are interpreted by competent tissues in a spatially and temporally restricted manner, and the mechanisms for the loss of responsiveness are not well understood. To test the hypothesis that loss of competence is associated with changes in chromatin accessibility, we adapted the assay for transposase-accessible chromatin with high throughput sequencing (ATAC-seq) for use in Xenopus laevis to evaluate genome-wide changes in chromatin accessibility in early and late gastrula stages. ATAC-seq was performed on presumptive ectoderm (animal caps) explanted at the blastula stage and cultured until siblings reached early (stage 10) or late (stage 12) gastrula stage. Approximately 70,000 accessible regions were identified at intergenic regions, introns, promoters, and transcription termination sites at both stages. Accessibility decreased from stage 10 to stage 12 at 279 promoters, including developmental regulators such as Foxh1, chordin, and VegT. Accessible chromatin domains overlap extensively with previously reported p300 binding sites, consistent with putative cis-regulatory modules (pCRMs), and these pCRMs are enriched for binding motifs for pluripotency factors, including Sox, Oct/Pou, and KLF binding motifs. Dorsal Wnt target gene promoters are not accessible after the loss of competence, but inhibition of histone deacetylases increases acetylation at these promoters and extends competence for dorsal gene induction by Wnt signaling. In contrast, the promoters for genes involved in mesoderm and neural crest development remain open through gastrulation, and histone deacetylase inhibition does not extend competence for mesoderm or neural crest induction. These data suggest that chromatin state regulates the loss of competence to inductive signals in a context-dependent manner.

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Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation.

Project description:In many organisms, early embryonic development is driven by maternally provided transcription factors until the controlled onset of transcription during zygotic genome activation (ZGA). The regulation of chromatin accessibility and its relationship to gene activity during this transition remains poorly understood. Here, we generated chromatin accessibility maps for the early stages of zebrafish development spanning genome activation and the onset of lineage specification. We find that during this period, chromatin accessibility increases at regulatory elements. This is independent of RNA pol II-mediated transcription, with the exception of the miR-430 locus. Instead, accessibility often precedes the transcription of associated genes. Loss of the maternal transcription factors pou5f3, sox19b, and nanog, which are known to be required for zebrafish ZGA, results in decreased accessibility at regulatory elements. Finally, we show that accessibility of regulatory regions, especially when established by Pou5f3, Sox19b and Nanog, is predictive for future transcription. Together, our results suggest that maternally provided transcription factors prime genes for activity during zygotic genome activation.

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Transcriptional profiling of inductive prostatic mesenchyme

2007-12-21 | GSE7899 | GEO

Regulation of chromatin accessibility in early zebrafish embryos by Pou5f3 and Sox19b transcription factors.

Project description:Pou5f3 and Sox19b transcription factors promote chromatin accessibility and activate zygotic transcription in zebrafish embryos. It is poorly understood how two transcription factors act together on chromatin. To answer this question, we performed Omni-ATAC-seq on the zebrafish embryos, single and double mutants by Pou5f3 and Sox19b, as well as the wild-type, at two blastula developmental stages, oblong and dome. We report, that chromatin accessibility on 48% of all putative enhancers depends on Pou5f3 and Sox19b. Out of them, accessibility on 33% enhancers is reduced in the double mutant and of 15% is increased. Enhancers with reduced and increased chromatin accessibility differ in GC content and transcription factors binding motif frequency, and are linked to early and late developmental regulatory genes, respectively. Our results indicate that Pou5f3 and Sox19b not only activate early zygotic genes, but also prevent premature activation of late developmental enhancers.

2022-01-07 | GSE188364 | GEO

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