Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation

Bošković, Ana; Bender, Ambre; Gall, Laurence; Ziegler-Birling, Céline; Beaujean, Nathalie; Torres-Padilla, Maria-Elena

doi:10.4161/epi.20584

Cited by 69 publications

(56 citation statements)

References 60 publications

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“…One can speculate that the rise of H3K36me3 at 4-cell stage is a response to an extensive polymerase pause release that promotes EGA and that does not happen again until blastocyst. However, Bošković et al reported that, in mouse, H3K36me3 was only present in maternal chromatin immediately after fertilization and was absent in other stages of embryos, but was absent in all stages of bovine preimplantation embryos after fertilization [56]. These observations contrast with our results, possibly because of differences in the antibodies used.…”

Section: Discussioncontrasting

confidence: 99%

Changes in Histone H3 Lysine 36 Methylation in Porcine Oocytes and Preimplantation Embryos

Diao

Oqani

et al. 2014

PLoS ONE

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Histone H3 lysine 36 (H3K36) methylation is known to be associated with transcriptionally active genes, and is considered a genomic marker of active loci. To investigate the changes in H3K36 methylation in pig, we determined the mono-, di-, and tri-methylations of H3K36 (H3K36me1, H3K36me2 and H3K36me3, respectively) in porcine fetal fibroblasts, oocytes and preimplantation embryos by immunocytochemistry using specific antibodies and confocal microscopy. These analyses revealed that only H3K36me3 in porcine fetal fibroblasts consistently colocalized with transcription sites identified as actively synthesizing RNA based on fluorouridine (FU) incorporation. Treatment of cells with flavopiridol, which blocks transcription elongation, completely abrogated both H3K36me3 signals and RNA synthesis. All three types of H3K36 methylation were present and did not significantly differ during oocyte maturation. In parthenogenetic embryos, H3K36me1 and -me2 were detected in 1-cell through blastocyst-stage embryos. In contrast, H3K36me3 was not detected in most 1-cell stage embryos. H3K36me3 signals became detectable in 2-cell stage embryos, peaked at the 4-cell stage, decreased at the 8-cell stage, and then became undetectable at blastocyst stages in both parthenogenetic and in vitro-fertilized (IVF) embryos. Unlike the case in IVF embryos, H3K36me3 could not be demethylated completely during the 1-cell stage in somatic cell nuclear transfer (SCNT) embryos. These results collectively indicate that H3K36me3, but not H3K36me1 or -me2, is associated with transcription elongation in porcine fetal fibroblasts. H3K36me3 is developmentally regulated and may be a histone mark of embryonic gene activation in pig. Aberrant H3K36 tri-methylation occurred during the nuclear reprogramming of SCNT embryos.

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Section: Discussioncontrasting

confidence: 99%

Changes in Histone H3 Lysine 36 Methylation in Porcine Oocytes and Preimplantation Embryos

Diao

Oqani

et al. 2014

PLoS ONE

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“…These data confirm and extend the previous observation that H3K4me3 levels are first detectable at the MBT (Chen et al, 2013). Interestingly global H3K36me3 levels are also below the level of detection in the mouse embryo as it undergoes the first wave of zygotic genome activation (Boskovic et al, 2012). (Harrison et al, 2011).…”

Section: Early Transcription Does Not Require Marks Canonically Assocsupporting

confidence: 90%

Establishment of regions of genomic activity during theDrosophilamaternal to zygotic transition

Harrison

Kaplan

2014

Preprint

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We describe the genome-wide distributions and temporal dynamics of nucleosomes and post-translational histone modifications throughout the maternal-to-zygotic transition in embryos of Drosophila melanogaster. At mitotic cycle 8, when few zygotic genes are being transcribed, embryonic chromatin is in a relatively simple state: there are few nucleosome free regions, undetectable levels of the histone methylation marks characteristic of mature chromatin, and low levels of histone acetylation at a relatively small number of loci. Histone acetylation increases by cycle 12, but it is not until cycle 14 that nucleosome free regions and domains of histone methylation become widespread. Early histone acetylation is strongly associated with regions that we have previously shown to be bound in early embryos by the maternally deposited transcription factor Zelda, suggesting that Zelda triggers a cascade of events, including the accumulation of specific histone modifications, that plays a role in the subsequent activation of these sequences.

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“…For example, histone N-terminal tails are hyperacetylated in both paternal and maternal chromatins after fertilization [38]. In addition, asymmetric distribution of H3K36me3 and H3K79me2/3 are lost at the 1-cell stage, leading to global hypomethylation of these residues on both chromatins [39,40]. Furthermore, global replacement of histone variants, such as deposition of H3.3 to paternal chromatin as well as removal of H2A.Z and macroH2A from maternal chromatin [41,42], takes place soon after fertilization.…”

Section: Tet3-mediated 5mc Oxidation Is Dispensable For Zygotic Gene mentioning

confidence: 99%

Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation

2012

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The methylation state of the paternal genome is rapidly reprogrammed shortly after fertilization. Recent studies have revealed that loss of 5-methylcytosine (5mC) in zygotes correlates with appearance of 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC). This process is mediated by Tet3 and the 5mC oxidation products generated in zygotes are gradually lost during preimplantation development through a replicationdependent dilution process. Despite these findings, the biological significance of Tet3-mediated oxidation of 5mC to 5hmC/5fC/5caC in zygotes is unknown. DNA methylation plays an important role in silencing gene expression including the repression of transposable elements (TEs). Given that the activation of TEs during preimplantation development correlates with loss of DNA methylation, it is believed that paternal DNA demethylation may have an important role in TE activation. Here we examined this hypothesis and found that Tet3-mediated 5mC oxidation does not have a significant contribution to TE activation. We show that the expression of LINE-1 (long interspersed nucleotide element 1) and ERVL (endogenous retroviruses class III) are activated from both paternal and maternal genomes in zygotes. Inhibition of 5mC oxidation by siRNA-mediated depletion of Tet3 affected neither TE activation, nor global transcription in zygotes. Thus, our study provides the first evidence demonstrating that activation of both TEs and global transcription in zygotes are independent of Tet3-mediated 5mC oxidation.

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Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation

Abstract: (2012) Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation, Epigenetics,7:7,[747][748][749][750][751][752][753][754][755][756][757]

Cited by 69 publications

References 60 publications

Changes in Histone H3 Lysine 36 Methylation in Porcine Oocytes and Preimplantation Embryos

Changes in Histone H3 Lysine 36 Methylation in Porcine Oocytes and Preimplantation Embryos

Establishment of regions of genomic activity during theDrosophilamaternal to zygotic transition

Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation

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