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Major waves of H2A.Z incorporation during mouse oogenesis and preimplantation embryo development

ABSTRACT: Epigenomes of mammalian oocytes and embryos undergo major transitions essential for successful development. Here, we provide genome-wide maps of histone variant H2A.Z during twelve stages of mouse oogenesis and preimplantation embryo development and relate it to histone marks and genomic features. This revealed that major waves of H2A.Z incorporation occur early in growing oocytes, forming distinct patterns of maternal, embryonic, and persistent H2A.Z enrichment. Late maternal enrichment is inherited by the zygote, and precedes reduced formation of lamina associated domains and early replication in the maternal genome of 2-cell embryos. Persistent H2A.Z enrichment is strongly associated with CpG islands and H3K4me3 near transcription start sites of active genes, but thousands of maternal and embryonic H2A.Z incorporation sites exist elsewhere, frequently at transposable elements. The persisting H2A.Z enrichments across related developmental stages enable preservation of epigenetic information despite major concurrent changes in H3K4me3, H3K27me3, and DNA methylation. Altogether, this advances our understanding of how histone variants contribute to epigenetic reprogramming during mammalian oogenesis and early development.

ORGANISM(S): Mus musculus

PROVIDER: GSE293415 | GEO | 2025/11/04

REPOSITORIES: GEO

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Project description:In mammals, totipotent pre-implantation embryos are formed by fusion of highly differentiated oocytes and spermatozoa. Acquisition of totipotency concurs with remodeling of chromatin states of parental genomes (M-bM-^@M-^\epigenetic reprogrammingM-bM-^@M-^]), changes in maternally contributed transcriptome and proteome, and zygotic genome activation. Genomes of mature germ cells are more proficient in supporting embryonic development than those of somatic cells. It is currently unknown whether transgenerational inheritance of chromatin states present in mature gametes underlies the efficacy of early embryonic development after natural conception. Here, we show that Ring1 and Rnf2, two core components of the Polycomb Repressive Complex 1 (PRC1), serve redundant gene regulatory functions during oogenesis that are required to support embryonic development beyond the two-cell stage. Numerous developmental regulatory genes that are established Polycomb targets in various somatic cell types are de-repressed in Ring1/Rnf2 double mutant (dm) fully grown germinal vesicle (GV) oocytes. Translation of tested aberrant maternal transcripts is, however, delayed until after fertilization. Exchange of maternal pro-nuclei between control and Ring1/Rnf2 maternally dm early zygotes demonstrates an essential role for Ring1 and Rnf2 during oogenesis in defining cytoplasmic and nuclear maternal contributions that are both essential for proper initiation of embryonic development. A large number of genes up-regulated in Ring1/Rnf2 dm GV oocytes harbor PRC2-mediated histone H3 lysine 27 trimethylation (H3K27me3) in spermatozoa and in embryonic stem cells (ESCs), and are repressed during normal oogenesis and early embryogenesis. These data strongly support the model that Polycomb acts in the female and male germline to silence differentiation inducing genes and to program chromatin states, thereby sustaining developmental potential across generations. Expression profiling of fully grown mouse GV oocytes was performed with the following genotypes: Ring1+/+Rnf2F/F (control), Ring1-/-Rnf2F/F (Ring1 mutant), Ring1+/+Rnf2F/FZp3-cre (Rnf2 mutant) and Ring1-/-Rnf2F/FZp3-cre (Ring1/Rnf2 double mutant). 12 samples were analyzed: 3 biological replicates of each of the 4 genotypes (Ring1+/+Rnf2F/F (control), Ring1-/-Rnf2F/F (Ring1 mutant), Ring1+/+Rnf2F/FZp3-cre (Rnf2 mutant) and Ring1-/-Rnf2F/FZp3-cre (Ring1/Rnf2 double mutant)). Each sample contains 50 GV oocytes.

Project description:In mammals, totipotent pre-implantation embryos are formed by fusion of highly differentiated oocytes and spermatozoa. Acquisition of totipotency concurs with remodeling of chromatin states of parental genomes (âepigenetic reprogrammingâ), changes in maternally contributed transcriptome and proteome, and zygotic genome activation. Genomes of mature germ cells are more proficient in supporting embryonic development than those of somatic cells. It is currently unknown whether transgenerational inheritance of chromatin states present in mature gametes underlies the efficacy of early embryonic development after natural conception. Here, we show that Ring1 and Rnf2, two core components of the Polycomb Repressive Complex 1 (PRC1), serve redundant gene regulatory functions during oogenesis that are required to support embryonic development beyond the two-cell stage. Numerous developmental regulatory genes that are established Polycomb targets in various somatic cell types are de-repressed in Ring1/Rnf2 double mutant (dm) fully grown germinal vesicle (GV) oocytes. Translation of tested aberrant maternal transcripts is, however, delayed until after fertilization. Exchange of maternal pro-nuclei between control and Ring1/Rnf2 maternally dm early zygotes demonstrates an essential role for Ring1 and Rnf2 during oogenesis in defining cytoplasmic and nuclear maternal contributions that are both essential for proper initiation of embryonic development. A large number of genes up-regulated in Ring1/Rnf2 dm GV oocytes harbor PRC2-mediated histone H3 lysine 27 trimethylation (H3K27me3) in spermatozoa and in embryonic stem cells (ESCs), and are repressed during normal oogenesis and early embryogenesis. These data strongly support the model that Polycomb acts in the female and male germline to silence differentiation inducing genes and to program chromatin states, thereby sustaining developmental potential across generations. Expression profiling of late 2-cell embryos was performed with the following genotypes: maternal Ring1-Rnf+ (control), maternal Ring1-Rnf2- (maternal Ring1/Rnf2 double mutant). These embryos were obtained by crossing Ring1-/-Rnf2F/F control females or Ring1-/-Rnf2F/F Zp3-cre expreimental females, respectively, to Ring1+/+Rnf2F/F control males. To distinguish between maternal transcripts present in the 2-cell embryo and newly (embryonicaly) transcribed transcripts, embryos from both genotypes were either not treated (expression profiling therefore shows all maternal and embryonic transcripts) or alpha-amanitin treated (alpha-amanitin inhibits de novo transcription, therefore expression profiling of treated embryos will only show maternal transcripts). 11 samples were analyzed: 3 biological replicates (except alpha-amanitin treated maternal Ring1/Rnf2 double mutant, where only 2 replicates were analyzed) of each genotype and treatment group were analyzed. Each sample contains 40 late 2-cell embryos.

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Major waves of H2A.Z incorporation during mouse oogenesis and preimplantation embryo development

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