Abstract
In eukaryotes, Suv39h H3K9 trimethyltransferases are required for pericentric heterochromatin formation and function. In early mouse preimplantation embryos, however, paternal pericentric heterochromatin lacks Suv39h-mediated H3K9me3 and downstream marks. Here we demonstrate Ezh2-independent targeting of maternally provided polycomb repressive complex 1 (PRC1) components to paternal heterochromatin. In Suv39h2 maternally deficient zygotes, PRC1 also associates with maternal heterochromatin lacking H3K9me3, thereby revealing hierarchy between repressive pathways. In Rnf2 maternally deficient zygotes, the PRC1 complex is disrupted, and levels of pericentric major satellite transcripts are increased at the paternal but not the maternal genome. We conclude that in early embryos, Suv39h-mediated H3K9me3 constitutes the dominant maternal transgenerational signal for pericentric heterochromatin formation. In absence of this signal, PRC1 functions as the default repressive back-up mechanism. Parental epigenetic asymmetry, also observed along cleavage chromosomes, is resolved by the end of the 8-cell stage--concurrent with blastomere polarization--marking the end of the maternal-to-embryonic transition.
Publication types
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Research Support, Non-U.S. Gov't
MeSH terms
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Animals
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Apoptosis / physiology
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Blastomeres / metabolism
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DNA-Binding Proteins / genetics
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DNA-Binding Proteins / physiology
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Embryo, Mammalian / metabolism*
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Embryo, Mammalian / ultrastructure
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Embryonic Development / physiology*
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Enhancer of Zeste Homolog 2 Protein
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Female
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Fluorescent Antibody Technique
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Genomic Imprinting*
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Heterochromatin / physiology*
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Heterochromatin / ultrastructure
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Histone-Lysine N-Methyltransferase / genetics
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Histone-Lysine N-Methyltransferase / physiology
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Integrases / metabolism
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Male
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Methyltransferases / physiology*
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Mice / embryology*
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Mice, Inbred C57BL
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Mice, Knockout
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Oocytes / metabolism
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Polycomb Repressive Complex 1
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Polycomb Repressive Complex 2
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Polycomb-Group Proteins
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Proteins / genetics
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Proteins / physiology
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Repressor Proteins / physiology*
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Reverse Transcriptase Polymerase Chain Reaction
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Transcription, Genetic
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Transgenes / physiology
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Ubiquitin-Protein Ligases
Substances
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DNA-Binding Proteins
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Heterochromatin
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Polycomb-Group Proteins
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Proteins
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Repressor Proteins
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Suv39h1 protein, mouse
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Methyltransferases
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Enhancer of Zeste Homolog 2 Protein
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Ezh2 protein, mouse
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Histone-Lysine N-Methyltransferase
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Polycomb Repressive Complex 2
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Polycomb Repressive Complex 1
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Rnf2 protein, mouse
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Ubiquitin-Protein Ligases
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Cre recombinase
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Integrases