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Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos.

Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P - PLoS ONE (2010)

Bottom Line: The majority of H3K4/K27me3 co-enriched promoters are distinct between the two lineages, primarily due to differences in the distribution of H3K27me3.Derivation of embryonic stem cells leads to significant losses and gains of H3K4/K27me3 co-enriched promoters relative to the ICM, with distinct contributions of (de)methylation events on K4 and K27.Our results show histone trimethylation asymmetry on promoters in the first two developmental lineages, and highlight an epigenetic skewing associated with embryonic stem cell derivation.

View Article: PubMed Central - PubMed

Affiliation: Institute of Basic Medical Sciences, University of Oslo and Norwegian Center for Stem Cell Research, Oslo, Norway.

ABSTRACT
First lineage specification in the mammalian embryo leads to formation of the inner cell mass (ICM) and trophectoderm (TE), which respectively give rise to embryonic and extraembryonic tissues. We show here that this first differentiation event is accompanied by asymmetric distribution of trimethylated histone H3 lysine 27 (H3K27me3) on promoters of signaling and developmentally-regulated genes in the mouse ICM and TE. A genome-wide survey of promoter occupancy by H3K4me3 and H3K27me3 indicates that both compartments harbor promoters enriched in either modification, and promoters co-enriched in trimethylated H3K4 and H3K27 linked to developmental and signaling functions. The majority of H3K4/K27me3 co-enriched promoters are distinct between the two lineages, primarily due to differences in the distribution of H3K27me3. Derivation of embryonic stem cells leads to significant losses and gains of H3K4/K27me3 co-enriched promoters relative to the ICM, with distinct contributions of (de)methylation events on K4 and K27. Our results show histone trimethylation asymmetry on promoters in the first two developmental lineages, and highlight an epigenetic skewing associated with embryonic stem cell derivation.

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Genes with promoters enriched in H3K4me3 and/or H3K27me3 are associated with distinct functional categories.(A) GO term enrichment of genes containing H3K4me3, H3K27me3 or H3K4/K27me3 promoters in the ICM and TE. The twelve most significant GO terms are shown as a function of significance (P-value). (B) GO term representation of all genes containing H3K4/K27me3 promoters in the ICM and TE.
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pone-0009150-g002: Genes with promoters enriched in H3K4me3 and/or H3K27me3 are associated with distinct functional categories.(A) GO term enrichment of genes containing H3K4me3, H3K27me3 or H3K4/K27me3 promoters in the ICM and TE. The twelve most significant GO terms are shown as a function of significance (P-value). (B) GO term representation of all genes containing H3K4/K27me3 promoters in the ICM and TE.

Mentions: Gene ontology (GO) analysis indicated that in both the ICM and TE, H3K4me3 and H3K27me3 genes were enriched in housekeeping and signaling processes, respectively, wheras H3K4/K27me3 genes were predominantly linked to signaling, development/differentiation and transcription regulation functions (Figure 2A; Table S1). These functional categories were corroborated by the analysis of all GO terms identified among genes with promoters co-occupied by trimethylated H3K4 and H3K27 (Figure 2B; Table S2). These functional groups are remarkably similar to those reported in ESCs (see below), arguing that H3K4 and H3K27 trimethylation highlights similar sets of functions in embryonic cells, cultured or in vivo. Functional categories linked to H3K4 and H3K27 trimethylation are thus similar in the ICM and TE, although many genes carrying these modifications are distinct. Trimethylation of H3K4 and H3K27, therefore, delineates a cell identity profile in the ICM and TE.


Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos.

Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P - PLoS ONE (2010)

Genes with promoters enriched in H3K4me3 and/or H3K27me3 are associated with distinct functional categories.(A) GO term enrichment of genes containing H3K4me3, H3K27me3 or H3K4/K27me3 promoters in the ICM and TE. The twelve most significant GO terms are shown as a function of significance (P-value). (B) GO term representation of all genes containing H3K4/K27me3 promoters in the ICM and TE.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2818844&req=5

pone-0009150-g002: Genes with promoters enriched in H3K4me3 and/or H3K27me3 are associated with distinct functional categories.(A) GO term enrichment of genes containing H3K4me3, H3K27me3 or H3K4/K27me3 promoters in the ICM and TE. The twelve most significant GO terms are shown as a function of significance (P-value). (B) GO term representation of all genes containing H3K4/K27me3 promoters in the ICM and TE.
Mentions: Gene ontology (GO) analysis indicated that in both the ICM and TE, H3K4me3 and H3K27me3 genes were enriched in housekeeping and signaling processes, respectively, wheras H3K4/K27me3 genes were predominantly linked to signaling, development/differentiation and transcription regulation functions (Figure 2A; Table S1). These functional categories were corroborated by the analysis of all GO terms identified among genes with promoters co-occupied by trimethylated H3K4 and H3K27 (Figure 2B; Table S2). These functional groups are remarkably similar to those reported in ESCs (see below), arguing that H3K4 and H3K27 trimethylation highlights similar sets of functions in embryonic cells, cultured or in vivo. Functional categories linked to H3K4 and H3K27 trimethylation are thus similar in the ICM and TE, although many genes carrying these modifications are distinct. Trimethylation of H3K4 and H3K27, therefore, delineates a cell identity profile in the ICM and TE.

Bottom Line: The majority of H3K4/K27me3 co-enriched promoters are distinct between the two lineages, primarily due to differences in the distribution of H3K27me3.Derivation of embryonic stem cells leads to significant losses and gains of H3K4/K27me3 co-enriched promoters relative to the ICM, with distinct contributions of (de)methylation events on K4 and K27.Our results show histone trimethylation asymmetry on promoters in the first two developmental lineages, and highlight an epigenetic skewing associated with embryonic stem cell derivation.

View Article: PubMed Central - PubMed

Affiliation: Institute of Basic Medical Sciences, University of Oslo and Norwegian Center for Stem Cell Research, Oslo, Norway.

ABSTRACT
First lineage specification in the mammalian embryo leads to formation of the inner cell mass (ICM) and trophectoderm (TE), which respectively give rise to embryonic and extraembryonic tissues. We show here that this first differentiation event is accompanied by asymmetric distribution of trimethylated histone H3 lysine 27 (H3K27me3) on promoters of signaling and developmentally-regulated genes in the mouse ICM and TE. A genome-wide survey of promoter occupancy by H3K4me3 and H3K27me3 indicates that both compartments harbor promoters enriched in either modification, and promoters co-enriched in trimethylated H3K4 and H3K27 linked to developmental and signaling functions. The majority of H3K4/K27me3 co-enriched promoters are distinct between the two lineages, primarily due to differences in the distribution of H3K27me3. Derivation of embryonic stem cells leads to significant losses and gains of H3K4/K27me3 co-enriched promoters relative to the ICM, with distinct contributions of (de)methylation events on K4 and K27. Our results show histone trimethylation asymmetry on promoters in the first two developmental lineages, and highlight an epigenetic skewing associated with embryonic stem cell derivation.

Show MeSH