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Dynamic expression of chromatin modifiers during developmental transitions in preimplantation embryos

ABSTRACT: There are two major developmental transitions that take place during the first four days of mouse embryogenesis. The first one is the maternal-to-zygotic transition in the zygote and 2-cell embryo, the second one is the first cell lineage commitment at the 32-cell stage. A number of transcription factors govern zygotic expression and the specification of pluripotent versus trophectoderm cells, while at the same time there are dynamic changes in DNA methylation and chromatin organization. It is not fully understood which chromatin modifying complexes take part in these processes and whether there is a particular spatiotemporal distribution of certain chromatin players in preimplantation development. To address this question, we performed gene expression profiling of single cells from the oocyte to the blastocyst stage. We describe the patterns of expression of over 100 genes involved in histone methylation, DNA methylation and chromatin remodelling. For a number of these genes we observed differential maternal versus zygotic expression. This is particularly the case for homologous genes like Tet1 and Tet3 (zygotic and maternal respectively), or Suv39h1 and Suv39h2 (zygotic and maternal respectively). In contrast to the maternal-to-zygotic switch, most chromatin modifying genes are ubiquitously expressed in the subsequent lineage specification at the 32-cell stage. The few exceptions that showed a differential expression pattern are Kdm1b, Tet1 and Prdm14. Our data suggests that genes coding for histone modifying complexes are ubiquitously expressed in early embryos and that there are maternal and zygotic variants of most of these complexes. Furthermore, the method that we applied, allows the distinction of female versus male embryos based on the expression of Xist (X-linked, expressed in female embryos) and Kdm5d (Y-linked, expressed strongly in male embryo). With the exception of the X- and Y-linked genes, we did not observe sex-specific gene expression patterns of chromatin modifiers or transcription factors.

ORGANISM(S): Mus musculus

PROVIDER: GSE63632 | GEO | 2015/12/01

SECONDARY ACCESSION(S): PRJNA268499

REPOSITORIES: GEO

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Project description:During development histone modifying enzymes are required for cell identity and lineage commitment, however little is known about the regulatory origins of the epigenome during embryonic development. Here we generate a comprehensive set of embryonic epigenome reference maps, which we use to determine the extent to which maternal factors shape chromatin state in Xenopus embryos. Using Î±-amanitin to inhibit zygotic transcription, we find that the majority of H3K4me3 and H3K27me3-enriched regions form a maternally defined epigenetic regulatory space with an underlying logic of hypomethylated islands. This maternal regulatory space extends to a substantial proportion of neurula stage-activated promoters. In contrast, p300-recruitment to distal regulatory regions requires embryonic transcription at most loci. The results show that H3K4me3 and H3K27me3 are part of a regulatory space that exerts an extended maternal control well into post-gastrulation development, and highlight the combinatorial action of maternal and zygotic factors through proximal and distal regulatory sequences. We have performed ChIP-sequencing of eight histone modifications, RNA polymerase II (RNAPII) and the enhancer protein p300 at five stages of development: blastula (st. 9), gastrula (st. 10.5, 12.5), neurula (st. 16) and tailbud (st. 30). These experiments allow identification of enhancers (H3K4me1, p300), promoters (H3K4me3, H3K9ac), transcribed regions (H3K36me3, RNAPII) and repressed and heterochromatic domains (H3K27me3, H3K9me2, H3K9me3, H4K20me3). In addition we generated pre-MBT (st. 8) maps for three histone modifications (H3K4me3, H3K9ac, H3K27me3) and single-base resolution DNA methylome maps using whole genome bisulfite sequencing of blastula and gastrula (st. 9 and 10.5) embryos. To determine the maternal and zygotic contributions to chromatin state, we used alpha-amanitin to block embryonic transcription. Fertilised eggs were injected with 2.3 nl of 2.67 ng/ul alpha-amanitin and developed until the control embryos reached mid-gastrulation. Alpha-amanitin and control embryos were used for RNA-seq and ChIP-seq of RNAPII, H3K4me3, H3K27me3 and p300. For all ChIP-seq samples of the epigenome reference maps and RNAPII ChIP-seq samples of the Î±-amanitin experiments three biological replicates of different chromatin isolations of 45 embryos were pooled. Two biological replicates for H3K4me3 (Î±-amanitin injected: resp. 90 and 56 embryo equivalents (eeq); control: resp. 45 and 67 eeq), H3K27me3 (Î±-amanitin injected: resp. 90 and 180 eeq; control: resp. 45 and 202 eeq) and p300 (Î±-amanitin injected: resp. 112 and 56 eeq; control: resp. 112 and 67 eeq) ChIP-seq samples of the Î±-amanitin experiments were generated. For RNA-seq samples of the Î±-amanitin experiments RNA from 5 embryos from one biological replicate was isolated and depleted of ribosomal RNA

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Dynamic expression of chromatin modifiers during developmental transitions in preimplantation embryos

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