Cohesin facilitates zygotic genome activation in zebrafish

Meier, Michael; Grant, Jenny; Dowdle, Amy; Thomas, Amarni; Gerton, Jennifer; Collas, Philippe; O’Sullivan, Justin M.; Horsfield, Julia A.

doi:10.1101/214023

Cited by 15 publications

(17 citation statements)

References 88 publications

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“…The nuclear to cytoplasmic ratio (N/C), which gradually increases due to the reductive nature of early divisions, plays a critical role in triggering MBT (26,28,29). In parallel, gradual dilution of maternally expressed transcription repressors and reduction of replication and transcription factors, resulting from the lack of transcription, were shown to control ZGA (19,26,(30)(31)(32)(33). Whether and how these factors are coordinated between single cells in the embryo is largely unknown.…”

Section: Significancementioning

confidence: 99%

Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis

Adar-Levor

Nachmias

Gal-Oz

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Animal cytokinesis ends with the formation of a thin intercellular membrane bridge that connects the two newly formed sibling cells, which is ultimately resolved by abscission. While mitosis is completed within 15 min, the intercellular bridge can persist for hours, maintaining a physical connection between sibling cells and allowing exchange of cytosolic components. Although cell–cell communication is fundamental for development, the role of intercellular bridges during embryogenesis has not been fully elucidated. In this work, we characterized the spatiotemporal characteristics of the intercellular bridge during early zebrafish development. We found that abscission is delayed during the rapid division cycles that occur in the early embryo, giving rise to the formation of interconnected cell clusters. Abscission was accelerated when the embryo entered the midblastula transition (MBT) phase. Components of the ESCRT machinery, which drives abscission, were enriched at intercellular bridges post-MBT and, interfering with ESCRT function, extended abscission beyond MBT. Hallmark features of MBT, including transcription onset and cell shape modulations, were more similar in interconnected sibling cells compared to other neighboring cells. Collectively, our findings suggest that delayed abscission in the early embryo allows clusters of cells to coordinate their behavior during embryonic development.

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Section: Significancementioning

confidence: 99%

Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis

Adar-Levor

Nachmias

Gal-Oz

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Is chromatin organization a prerequisite for ZGA? In zebrafish, cohesin depletion in early embryos leads to a delay in ZGA many cell cycles later [ 66 ], which could be due to either direct or indirect effects. It is also not known whether chromatin organization is perturbed under these conditions.…”

Section: Coordination Of 3d Chromatin Organization and Zgamentioning

confidence: 99%

The emergence of genome architecture and zygotic genome activation

Vallot

Tachibana

2020

Current Opinion in Cell Biology

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The fusion of two transcriptionally silent gametes, egg and sperm, generates a totipotent zygote that activates zygotic transcription to support further development. Although the molecular details of zygotic genome activation (ZGA) are not well understood in most species, an emerging concept is that one or more pioneer transcription factors trigger zygotic transcription. Concomitantly, extensive changes in 3D chromatin organization occur during development. In this review, we discuss recent advances in understanding when and how genome architecture emerges in early metazoan embryos, how the zygotic genome is activated, and how these events might be coordinated. We also highlight some of the unknowns that may be critical to address in the future.

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“…In human, a mutation of NIPBL is associated to the Cornelia de Lange syndrome, a developmental disorder (Newkirk et al, 2017). In zebrafish, the zygotic genome activation is facilitated by cohesin and was a key for the embryogenesis (Meier et al, 2018). Intriguingly, the cohesin complex has been proposed to modulate estrogen-dependent gene transcription and a link has been established with breast cancer (Antony et al, 2015).…”

Section: Effects Of Ee2 On the Liver Methylomementioning

confidence: 99%

Genome-wide DNA methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus

Voisin

Ulloa

Stockwell

et al. 2020

Preprint

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Organisms exposed to endocrine disruptors in early life can show altered phenotype later in adulthood. Although the mechanisms underlying these long-term effects remain poorly understood, an increasing body of evidence points toward the potential role of epigenetic processes. In the present study, we exposed hatchlings of an isogenic lineage of the self-fertilizing fish mangrove rivulus for 28 days to 4 and 120 ng/L of 17-α-ethinylestradiol. After a recovery period of 140 days, reduced representation bisulfite sequencing (RRBS) was performed on the liver in order to assess the hepatic genome-wide methylation landscape. Across all treatment comparisons, a total of 146 differentially methylated fragments (DMFs) were reported, mostly for the group exposed to 4 ng/L, suggesting a non-monotonic effect of EE2 exposure. Gene ontology analysis revealed networks involved in lipid metabolism, cellular processes, connective tissue function, molecular transport and inflammation. The highest effect was reported for nipped-B-like protein B (NIPBL) promoter region after exposure to 4 ng/L EE2 (+ 21.9%), suggesting that NIPBL could be an important regulator for long-term effects of EE2. Our results also suggest a significant role of DNA methylation in intergenic regions and potentially in transposable elements. These results support the ability of early exposure to endocrine disruptors of inducing epigenetic alterations during adulthood, providing plausible mechanistic explanations for long-term phenotypic alteration. Additionally, this work demonstrates the usefulness of isogenic lineages of the self-fertilizing mangrove rivulus to better understand the biological significance of long-term alterations of DNA methylation by diminishing the confounding factor of genetic variability.

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Cohesin facilitates zygotic genome activation in zebrafish

Abstract: 2223

Cited by 15 publications

References 88 publications

Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis

Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis

The emergence of genome architecture and zygotic genome activation

Genome-wide DNA methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus

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