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Nucleosome organization dynamics during fertilization reveals regulation factors of zygotic gene activation in mouse (RNA-seq)

ABSTRACT: Chromatin remodeling is essential for the reprogramming process after fertilization. However, the detailed mechanism remains unclear to date. In this study, we reported the dynamic changes of nucleosome occupancy and positioning in pronuclear stages using low-input MNase-seq. We found distinct features of inheritance and reconstruction on nucleosome position can be observed in the male and female genome. Genome-wide de novo nucleosome occupancy in the paternal genome was observed as early as 1 hour after the injection of sperm. The nucleosome positioning pattern was further rebuilt continually to form nucleosome depletion regions (NDR) on promoter and transcription factor (TF) binding sites. The formation of promoter NDRs occurred faster on zygotic genome activation genes, which rely on the function of Brd4 but independent of transcription elongation or DNA replication. Importantly, we found the establishment of NDR on TF binding motifs might be associated with its potential pioneer function in zygotic genome activation (ZGA). Further verification suggested predicted factors Mlx and Rfx1 play important roles in minor and major ZGA, respectively. Our data do not only provided the first insight of nucleosome positioning dynamics in the very early stage of embryogenesis but also provided a way to identify key TF regulators in the developmental process.

ORGANISM(S): Mus musculus

PROVIDER: GSE140876 | GEO | 2022/04/02

REPOSITORIES: GEO

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Nucleosome organization dynamics during fertilization reveals regulation factors of zygotic gene activation in mouse (MNase-seq)

Project description:Chromatin remodeling is essential for epigenome reprogramming after fertilization. However, the underlying mechanisms of chromatin remodeling remain to be explored. Here, we investigated the dynamic changes in nucleosome occupancy and positioning in pronucleus-stage zygotes using low-input MNase-seq. We observed distinct features of inheritance and reconstruction of nucleosome position in both male and female genomes. Genome-wide de novo nucleosome occupancy in the paternal genome was observed as early as 1 hour after the injection of sperm. The nucleosome positioning pattern was continually rebuilt to form nucleosome depletion regions (NDRs) at promoters and transcription factor (TF) binding sites. NDRs formed more quickly on the promoters of genes involved in zygotic genome activation (ZGA), and their formation is closely connected with histone acetylation, but not transcription elongation or DNA replication. Importantly, we found that NDR establishment on the binding motifs of specific TFs might be associated with their potential pioneer functions in ZGA. Further investigations suggested that the predicted factors MLX and RFX1 played important roles in regulating minor and major ZGA, respectively. Our data not only elucidate the nucleosome positioning dynamics in both male and female pronuclei following fertilization, but also provide an efficient method for identifying key transcription regulators during development.

2022-04-02 | GSE140875 | GEO

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Suppression of pervasive noncoding transcription in embryonic stem cells by esBAF

Project description:Approximately 75% of the human genome is transcribed, the majority of which does not encode protein. However, most noncoding RNA (ncRNA) is rapidly degraded after transcription, and relatively few have established functions, questioning the significance of this observation. Here we show that esBAF, a SWI/SNF family nucleosome remodeling factor, suppresses transcription of ncRNAs from approximately 57,000 nucleosome-depleted regions (NDRs) throughout the genome of mouse embryonic stem cells (ESCs). We show that esBAF functions both to keep NDRs nucleosome-free and to promote elevated nucleosome occupancy adjacent to NDRs. Reduction of adjacent nucleosome occupancy upon esBAF depletion is strongly correlated with ncRNA expression, suggesting that flanking nucleosomes form a barrier to pervasive transcription. Upon forcing nucleosome occupancy near an NDR using a nucleosome-positioning sequence, we find that esBAF is no longer required to silence transcription. These data reveal a novel role for esBAF in suppressing pervasive transcription from open chromatin regions in ESCs. Examine nucleosome occupancy (MNase-Seq) and transcript production (CapSeq and RNA-Seq) in EGFP KD and Smarca4 KD ESCs

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Suppression of pervasive noncoding transcription in embryonic stem cells by esBAF

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Pou5f3, SoxB1 and Nanog remodel chromatin on High Nucleosome Affinity Regions at Zygotic Genome Activation.

Project description:Purpose: Find out the consequences of Pou5f3/Oct4 and Nanog binding to the nucleosome distribution before and after Zygotic Genome Activation Methods: MNase-seq of the wild-type(WT), Pou5f3 (MZspg) and Nanog (MZnanog) mutant zebrafish embryos at 512-cell stage and dome stage. Results: Nanog, Sox19b and Pou5f3 bind to the High Nucleosome Affinity Regions (HNARs). HNARs are spanning over 600 bp, featuring high in vivo and predicted in vitro nucleosome occupancy and high predicted propeller twist DNA shape value. We suggest a two-step model, where the same intrinsic DNA properties of HNAR promote both high nucleosome occupancy and differential binding of TFs. In the first step, already prior to ZGA, Pou5f3 and Nanog reduce nucleosome occupancy on HNARs genome-wide. In the second step, Nanog and Pou5f3/SoxB1 complex maintain open chromatin state on the subset of HNARs, acting synergistically. Nanog binds to the HNAR center, while the Pou5f3/SoxB1 complex stabilizes the flanks.

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TF co-binding to nucleosome arrays

Project description:Cell type maintenance and conversion require the combined action of transcription factors (TFs), but the underlying principles remain elusive. Here, we investigated how four TF combinations lead to different reprogramming outputs by studying TF occupancy, nucleosome positioning, and genome 3D organization. We reveal that TF combinations target nucleosome with distinct 3D nucleosome conformations. We also reveal that TFs employ different motif readout mechanisms to reach their cell type specific targets. Moreover, the ability of pioneer TFs to enable non-pioneer factors the access to closed chromatin is markedly different across combinations. Overall, our findings uncover distinct modes of action for TFs during reprogramming.

2024-09-27 | GSE201852 | GEO

OBOX regulates murine zygotic genome activation and early development

Project description:Zygotic genome activation (ZGA) activates the quiescent genome to enable the maternal-to-zygotic transition. However, the identity of transcription factors (TFs) that underlie mammalian ZGA in vivo remains unresolved. Here, we showed that OBOX, a PRD-like homeobox domain TF family that includes 66 members (OBOX1-8), are key regulators of mouse ZGA. Knockout mice deficient for maternally transcribed Obox1/2/5/7 and zygotically expressed Obox3/4 led to 2-4 cell arrest accompanied by impaired ZGA. Maternal and zygotic expressed OBOX redundantly support embryonic development as Obox KO defects can be rescued by restoring either of them. Chromatin binding analysis revealed Obox knockout preferentially affected OBOX-binding targets. Mechanistically, OBOX facilitated RNA Pol II ?pre-configuration?, as Pol II relocates from the initial 1-cell binding targets to ZGA gene promoters and distal enhancers. The impaired Pol II pre-configuration in Obox mutants was accompanied by downregulation of ZGA genes, chromatin accessibility transition defects, as well as aberrant activation of one-cell Pol II targets. Finally, OBOX ectopically activated ZGA genes and MERVL in mESCs. Hence, these data demonstrate that OBOX regulates murine ZGA and early embryogenesis.

2023-04-24 | GSE215813 | GEO

Quantitative proteomics reveals the dynamic proteome landscape of zebrafish embryos during maternal-to-zygotic transition and its relationship to zygotic genome activation

Project description:Upon fertilization, the embryonic genome remains transcriptionally inactive until the mid-blastula transition. Zygotic genome activation (ZGA) of vertebrate embryos has been extensively studied using nucleic acid-based strategies, but proteomics data are still scarce, impeding the full mechanistic understanding of how ZGA is executed during the maternal-to-zygotic transition (MZT). Here, we performed quantitative proteomics to decipher the proteome landscape of zebrafish embryos during the MZT, quantifying nearly 5,000 proteins across four embryonic stages. The stage-specific clustering based on protein expression pattern revealed that helicases (i.e., eif4a2 and ruvbl1) facilitate pluripotency factors (i.e., nanog, pou5f3, ctcf, and hmga1) triggering ZGA in zebrafish, accompanied by the maternal product decay with P-bodies and ubiquitin dependent proteolytic pathway. Dozens of transcription factors show wave-like expression patterns during MZT, implying their diverse functions in triggering the ZGA and modulating differentiation for organ development. The combination of morpholino knockdown and quantitative proteomics demonstrated that maternal Nanog is required for proper embryogenesis by regulating 1) interactions with other pluripotency factors, 2) F-actin band formation, 3) cell cycle checkpoints and 4) maternal product degradation. This study represents the most systematic proteomics survey of developmentally regulated proteins and their expression profiles accompanying MZT in zebrafish, which is a valuable proteome resource for understanding ZGA.

2024-05-01 | PXD036678 | Pride

Genome-wide maps of NME2 in A549 lung adenocarcinoma cells.

Project description:It is widely believed that reorganization of nucleosomes result in availability of transcription factor (TF) binding sites for eukaryotic gene regulation. Recent findings also show TFs induced during physiological perturbations can alter nucleosome occupancy to facilitate DNA binding. Although, these suggest a close relationship between TF binding and nucleosomes, the nature of this interaction, or to what extent it influences transcription is not clear. Moreover, since physiological perturbations induced multiple TFs, relatively direct effect of any TF on nucleosome occupancy remains poorly addressed. With these in mind, we used a single TF to induce physiological changes and following characterization of the two states (before and after induction of the TF) we determined: (a) genome wide binding sites of the TF, (b) promoter nucleosome occupancy and (c) transcriptome profiles, independently in both conditions. We find only ~20% of TF binding results from nucleosome repositioning - interestingly, almost all corresponding genes were transcriptionally altered. Whereas, when TF-occupancy was independent of nucleosome repositioning only a small fraction of corresponding genes were expressed/repressed. These observations suggest a model where TF occupancy leads to transcriptional change only when coupled with nucleosome repositioning in close proximity. This, to our knowledge, for the first time also helps explain why genome wide TF occupancy (e.g., from ChIP-sequencing) typically overlaps with only a small fraction of genes that change expression. The nature of interaction between TF binding and nucleosomes and what extent it influences transcription

2014-08-04 | E-GEOD-40300 | biostudies-arrayexpress

Nucleosome positioning in A549 cells before/after NME2 induction

Project description:Previous studies have analyzed patterns of transcription, transcription factor (TF) binding or mapped nucleosome occupancy across the genome. These suggest that the three aspects are genetically connected but the cause and effect relationships are still unknown. For example, physiologic TF binding studies involve many TFs, consequently, it is difficult to assign nucleosome reorganization to the binding site occupancy of any particular TF. Therefore, several aspects remain unclear: does TF binding influence nucleosome (re)organizations locally (in close vicinity of their binding sites) or impact the chromatin landscape at a more global level; are all or only a fraction of TF binding a result of reorganization in nucleosome occupancy; finally, do all TF binding and associated nucleosome occupancy changes result in altered gene expression? With these in mind, we sought to study a single TF that induces physiological changes, and following characterization of the two states (before and after induction of the TF) we determined: (a) genomic binding sites of the TF, (b) promoter nucleosome occupancy and (c) transcriptome profiles, independently in both conditions. Results demonstrate that TF binding influences expression of the target gene only when it is coupled to nucleosome repositioning at or close to its binding site, and not when transcription factor binding occurs without local associated nucleosome reorganization. The nature of interaction between TF binding and nucleosomes and what extent it influences transcription

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