scholarly journals TALE and NF-Y co-occupancy marks enhancers of developmental control genes during zygotic genome activation in zebrafish

2019 ◽  
Author(s):  
William Stanney ◽  
Franck Ladam ◽  
Ian J. Donaldson ◽  
Teagan J. Parsons ◽  
René Maehr ◽  
...  
Keyword(s):  
Gene Expression ◽  
Transcriptional Regulation ◽  
Transcription Factors ◽  
Maternal Factors ◽  
Zygotic Genome Activation ◽  
Enhancer Activity ◽  
Genome Activation ◽  
Expression Program ◽  
Zygotic Genome

SUMMARYAnimal embryogenesis is initiated by maternal factors, but zygotic genome activation (ZGA) shifts control to the embryo at early blastula stages. ZGA is thought to be mediated by specialized maternally deposited transcription factors (TFs), but here we demonstrate that NF-Y and TALE – TFs with known later roles in embryogenesis – co-occupy unique genomic elements at zebrafish ZGA. We show that these elements are selectively associated with early-expressed genes involved in transcriptional regulation and possess enhancer activity in vivo. In contrast, we find that elements individually occupied by either NF-Y or TALE are associated with genes acting later in development – such that NF-Y controls a cilia gene expression program while TALE TFs control expression of hox genes. We conclude that NF-Y and TALE have a shared role at ZGA, but separate roles later during development, demonstrating that combinations of known TFs can regulate subsets of key developmental genes at vertebrate ZGA.

scholarly journals Endodermal Maternal Transcription Factors Establish Super-Enhancers during Zygotic Genome Activation

Cell Reports ◽  
2019 ◽  
Vol 27 (10) ◽  
pp. 2962-2977.e5 ◽  
Author(s):  
Kitt D. Paraiso ◽  
Ira L. Blitz ◽  
Masani Coley ◽  
Jessica Cheung ◽  
Norihiro Sudou ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Zygotic Genome Activation ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals Maternal Dppa2 and Dppa4 are dispensable for zygotic genome activation but important for offspring survival

Development ◽  
2021 ◽  
Vol 148 (24) ◽  
Author(s):  
Oana Kubinyecz ◽  
Fatima Santos ◽  
Deborah Drage ◽  
Wolf Reik ◽  
Melanie A. Eckersley-Maslin
Keyword(s):  
Null Allele ◽  
Embryonic Stem ◽  
Offspring Survival ◽  
Zygotic Genome Activation ◽  
Molecular Events ◽  
Genome Activation ◽  
Mitotic Chromatin ◽  
Zygotic Genome

ABSTRACT Zygotic genome activation (ZGA) represents the initiation of transcription following fertilisation. Despite its importance, we know little of the molecular events that initiate mammalian ZGA in vivo. Recent in vitro studies in mouse embryonic stem cells have revealed developmental pluripotency associated 2 and 4 (Dppa2/4) as key regulators of ZGA-associated transcription. However, their roles in initiating ZGA in vivo remain unexplored. We reveal that Dppa2/4 proteins are present in the nucleus at all stages of preimplantation development and associate with mitotic chromatin. We generated conditional single and double maternal knockout mouse models to deplete maternal stores of Dppa2/4. Importantly, Dppa2/4 maternal knockout mice were fertile when mated with wild-type males. Immunofluorescence and transcriptome analyses of two-cell embryos revealed that, although ZGA took place, there were subtle defects in embryos that lacked maternal Dppa2/4. Strikingly, heterozygous offspring that inherited the null allele maternally had higher preweaning lethality than those that inherited the null allele paternally. Together, our results show that although Dppa2/4 are dispensable for ZGA transcription, maternal stores have an important role in offspring survival, potentially via epigenetic priming of developmental genes.

scholarly journals Pluripotency factors select gene expression repertoire at Zygotic Genome Activation

2020 ◽  
Author(s):  
Meijiang Gao ◽  
Marina Veil ◽  
Marcus Rosenblatt ◽  
Anna Gebhard ◽  
Helge Hass ◽  
...  
Keyword(s):  
Gene Expression ◽  
Transcription Factors ◽  
Early Gene ◽  
Zebrafish Embryos ◽  
Fate Specification ◽  
Pluripotency Factors ◽  
Zygotic Transcription ◽  
Simultaneous Loss ◽  
Genome Activation ◽  
Zygotic Genome

AbstractAwakening of zygotic transcription in animal embryos relies on maternal pioneer transcription factors. The interplay of global and specific functions of these proteins remains poorly understood. Here, we analyzed nucleosome positioning, H3K27 acetylation, transcription, and gastrulation rates in zebrafish embryos lacking pluripotency factors Pou5f3 and Sox19b. We show that the bulk transcriptional onset does not require Sox19b and Pou5f3, but is sensitive to their balance. Pou5f3 docks H3K27ac on the enhancers of genes involved in gastrulation and ventral fate specification. Sox19b facilitates Pou5f3 access to one-third of these enhancers. The genes regulating mesendodermal and dorsal fates are primed for activation independently on Pou5f3 and Sox19b. Strikingly, the loss of either factor results in activation of silent enhancers; simultaneous loss of both leads to premature expression of differentiation genes. Our results uncover how independent activities of maternal Pou5f3 and Sox19b add up or antagonize to determine the early gene expression repertoire.

scholarly journals Combinatorial action of NF–Y and TALE at embryonic enhancers defines distinct gene expression programs during zygotic genome activation in zebrafish

2020 ◽  
Vol 459 (2) ◽  
pp. 161-180 ◽  
Author(s):  
William Stanney ◽  
Franck Ladam ◽  
Ian J. Donaldson ◽  
Teagan J. Parsons ◽  
René Maehr ◽  
...  
Keyword(s):  
Gene Expression ◽  
Zygotic Genome Activation ◽  
Distinct Gene ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals DPPA2 and DPPA4 are dispensable for mouse zygotic genome activation and preimplantation development

2021 ◽  
Author(s):  
Zhiyuan Chen ◽  
Zhenfei Xie ◽  
Yi Zhang
Keyword(s):  
Stem Cells ◽  
Embryonic Stem Cells ◽  
Embryonic Stem ◽  
Preimplantation Development ◽  
Dependent Manner ◽  
Maternal Factors ◽  
Zygotic Genome Activation ◽  
Cell Embryo ◽  
Genome Activation ◽  
Zygotic Genome

How maternal factors in oocytes initiate zygotic genome activation (ZGA) remains elusive. Recent studies indicate that DPPA2 and DPPA4 are required for establishing a 2-cell embryo-like (2C-like) state in mouse embryonic stem cells (ESCs) in a DUX-dependent manner. These results suggest that DPPA2 and DPPA4 are essential maternal factors that regulate Dux and ZGA in embryos. By analyzing maternal knockout and maternal-zygotic knockout embryos, we unexpectedly found that Dux activation, ZGA, and preimplantation development are normal in embryos without DPPA2 or DPPA4. Thus, unlike in ESCs/2C-like cells, DPPA2 and DPPA4 are dispensable for ZGA and preimplantation development.

scholarly journals Prepatterning of Developmental Gene Expression by Modified Histones before Zygotic Genome Activation

2011 ◽  
Vol 21 (6) ◽  
pp. 993-1004 ◽  
Author(s):  
Leif C. Lindeman ◽  
Ingrid S. Andersen ◽  
Andrew H. Reiner ◽  
Nan Li ◽  
Håvard Aanes ◽  
...  
Keyword(s):  
Gene Expression ◽  
Zygotic Genome Activation ◽  
Developmental Gene ◽  
Developmental Gene Expression ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals Histone variant H2A.Z regulates zygotic genome activation

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Dafne Ibarra-Morales ◽  
Michael Rauer ◽  
Piergiuseppe Quarato ◽  
Leily Rabbani ◽  
Fides Zenk ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
De Novo ◽  
Housekeeping Genes ◽  
Histone Variant ◽  
Small Subset ◽  
Zygotic Genome Activation ◽  
Transcription Start Sites ◽  
Genome Activation ◽  
Zygotic Genome

AbstractDuring embryogenesis, the genome shifts from transcriptionally quiescent to extensively active in a process known as Zygotic Genome Activation (ZGA). In Drosophila, the pioneer factor Zelda is known to be essential for the progression of development; still, it regulates the activation of only a small subset of genes at ZGA. However, thousands of genes do not require Zelda, suggesting that other mechanisms exist. By conducting GRO-seq, HiC and ChIP-seq in Drosophila embryos, we demonstrate that up to 65% of zygotically activated genes are enriched for the histone variant H2A.Z. H2A.Z enrichment precedes ZGA and RNA Polymerase II loading onto chromatin. In vivo knockdown of maternally contributed Domino, a histone chaperone and ATPase, reduces H2A.Z deposition at transcription start sites, causes global downregulation of housekeeping genes at ZGA, and compromises the establishment of the 3D chromatin structure. We infer that H2A.Z is essential for the de novo establishment of transcriptional programs during ZGA via chromatin reorganization.

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

2019 ◽  
Author(s):  
Máté Pálfy ◽  
Gunnar Schulze ◽  
Eivind Valen ◽  
Nadine L. Vastenhouw
Keyword(s):  
Transcription Factors ◽  
Rna Polymerase ◽  
Rna Polymerase Ii ◽  
Regulatory Elements ◽  
Chromatin Accessibility ◽  
Zebrafish Genome ◽  
Zygotic Genome Activation ◽  
Lineage Specification ◽  
Genome Activation ◽  
Zygotic Genome

ABSTRACTIn many organisms, early embryonic development is driven by maternally provided factors until the controlled onset of transcription during zygotic genome activation. The regulation of chromatin accessibility and its relationship to gene activity during this transition remains poorly understood. Here, we generated chromatin accessibility maps from genome activation until the onset of lineage specification. During this period, chromatin accessibility increases at regulatory elements. This increase is independent of RNA polymerase II-mediated transcription, with the exception of the hyper-transcribed 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 genome activation, results in decreased accessibility at regulatory elements. Importantly, the accessibility of regulatory regions, especially when established by Pou5f3, Sox19b and Nanog, is predictive for future transcription. Our results show that the maternally provided transcription factors Pou5f3, Sox19b, and Nanog open up chromatin and prime genes for activity during zygotic genome activation in zebrafish.

scholarly journals The histone deacetylase activity of HDAC1/2 is required to safeguard zygotic genome activation in mice and cattle

2021 ◽  
Author(s):  
Yanna Dang ◽  
Shuang Li ◽  
Panpan Zhao ◽  
Lieying Xiao ◽  
Lefeng Wang ◽  
...  
Keyword(s):  
Gene Expression ◽  
Histone Deacetylase ◽  
Dynamic Change ◽  
Ectopic Expression ◽  
Gene Expression Pattern ◽  
Subsequent Development ◽  
Dominant Negative Mutant ◽  
Zygotic Genome Activation ◽  
Genome Activation ◽  
Zygotic Genome

ABSTRACTThe genome is transcriptionally inert at fertilization and must be activated through a remarkable developmental process called zygotic genome activation (ZGA). The gene expression pattern formed over the course of ZGA is required for establishing totipotency in early embryos and subsequent development. Substantial epigenetic reprogramming contributes significantly to the pronounced change in gene expression during ZGA, however the mechanism has yet to be resolved. Here, we find histone deacetylase 1 and 2 (HDAC1/2) are critical histone modifiers that regulate ZGA through the histone deacetylase activity. Notably, we show that H3K27ac level declines dramatically during ZGA with a dynamic change in its genome-wide distribution. In mouse embryos, ectopic expression of HDAC1/2 dominant negative mutant leads to a failure of H3K27ac removal and a developmental arrest at 2-cell stage. RNA-seq results reveal a remarkable transcriptomic change with 6565 differentially expressed genes identified. Further analysis shows 64% of down-regulated genes are ZGA genes and 49% of up-regulated genes are developmental genes. Low input ChIP-seq analysis exhibits an increase and decrease of H3K27ac enrichment at the promoter region of up- and down-regulated genes, respectively. Moreover, HDAC1 mutants prohibited removal of broad H3K4me3 domain via impeding the expression of Kdm5s during ZGA. Importantly, the developmental block can be greatly overcome through injection of Kdm5b mRNA and expression of the majority of dysregulated genes partially corrected. Similar functional significance of HDAC1/2 in ZGA is conserved in bovine embryos. Together, we propose that HDAC1/2 is indispensable for mouse and bovine ZGA via creating correct transcriptional repressive and active states.

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