Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos

Genomic imprinting regulates parental-specific expression of particular genes and is required for normal mammalian development. How imprinting is established during development is, however, largely unknown. To address this question, we studied the mouse Kcnq1 imprinted cluster at which paternal-spec...

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Published in:	Developmental cell Vol. 15; no. 5; p. 668
Main Authors:	Terranova, Rémi, Yokobayashi, Shihori, Stadler, Michael B, Otte, Arie P, van Lohuizen, Maarten, Orkin, Stuart H, Peters, Antoine H F M
Format:	Journal Article
Language:	English
Published:	United States 01.11.2008
Subjects:	Animals Cell Nucleus - genetics Cell Nucleus - metabolism Chromatin Assembly and Disassembly DNA-Binding Proteins - metabolism Embryo, Mammalian - metabolism Enhancer of Zeste Homolog 2 Protein Female Genomic Imprinting Histone-Lysine N-Methyltransferase - metabolism Male Mice Polycomb Repressive Complex 1 Polycomb Repressive Complex 2 Repressor Proteins - metabolism RNA, Long Noncoding RNA, Untranslated - metabolism Ubiquitin-Protein Ligases - metabolism
ISSN:	1878-1551, 1878-1551
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Abstract	Genomic imprinting regulates parental-specific expression of particular genes and is required for normal mammalian development. How imprinting is established during development is, however, largely unknown. To address this question, we studied the mouse Kcnq1 imprinted cluster at which paternal-specific silencing depends on expression of the noncoding RNA Kcnq1ot1. We show that Kcnq1ot1 is expressed from the zygote stage onward and rapidly associates with chromatin marked by Polycomb group (PcG) proteins and repressive histone modifications, forming a discrete repressive nuclear compartment devoid of RNA polymerase II, a configuration also observed at the Igf2r imprinted cluster. In this compartment, the paternal Kcnq1 cluster exists in a three-dimensionally contracted state. In vivo the PcG proteins Ezh2 and Rnf2 are independently required for genomic contraction and imprinted silencing. We propose that the formation of a parental-specific higher-order chromatin organization renders imprint clusters competent for monoallelic silencing and assign a central role to PcG proteins in this process.
AbstractList	Genomic imprinting regulates parental-specific expression of particular genes and is required for normal mammalian development. How imprinting is established during development is, however, largely unknown. To address this question, we studied the mouse Kcnq1 imprinted cluster at which paternal-specific silencing depends on expression of the noncoding RNA Kcnq1ot1. We show that Kcnq1ot1 is expressed from the zygote stage onward and rapidly associates with chromatin marked by Polycomb group (PcG) proteins and repressive histone modifications, forming a discrete repressive nuclear compartment devoid of RNA polymerase II, a configuration also observed at the Igf2r imprinted cluster. In this compartment, the paternal Kcnq1 cluster exists in a three-dimensionally contracted state. In vivo the PcG proteins Ezh2 and Rnf2 are independently required for genomic contraction and imprinted silencing. We propose that the formation of a parental-specific higher-order chromatin organization renders imprint clusters competent for monoallelic silencing and assign a central role to PcG proteins in this process. Genomic imprinting regulates parental-specific expression of particular genes and is required for normal mammalian development. How imprinting is established during development is, however, largely unknown. To address this question, we studied the mouse Kcnq1 imprinted cluster at which paternal-specific silencing depends on expression of the noncoding RNA Kcnq1ot1. We show that Kcnq1ot1 is expressed from the zygote stage onward and rapidly associates with chromatin marked by Polycomb group (PcG) proteins and repressive histone modifications, forming a discrete repressive nuclear compartment devoid of RNA polymerase II, a configuration also observed at the Igf2r imprinted cluster. In this compartment, the paternal Kcnq1 cluster exists in a three-dimensionally contracted state. In vivo the PcG proteins Ezh2 and Rnf2 are independently required for genomic contraction and imprinted silencing. We propose that the formation of a parental-specific higher-order chromatin organization renders imprint clusters competent for monoallelic silencing and assign a central role to PcG proteins in this process.Genomic imprinting regulates parental-specific expression of particular genes and is required for normal mammalian development. How imprinting is established during development is, however, largely unknown. To address this question, we studied the mouse Kcnq1 imprinted cluster at which paternal-specific silencing depends on expression of the noncoding RNA Kcnq1ot1. We show that Kcnq1ot1 is expressed from the zygote stage onward and rapidly associates with chromatin marked by Polycomb group (PcG) proteins and repressive histone modifications, forming a discrete repressive nuclear compartment devoid of RNA polymerase II, a configuration also observed at the Igf2r imprinted cluster. In this compartment, the paternal Kcnq1 cluster exists in a three-dimensionally contracted state. In vivo the PcG proteins Ezh2 and Rnf2 are independently required for genomic contraction and imprinted silencing. We propose that the formation of a parental-specific higher-order chromatin organization renders imprint clusters competent for monoallelic silencing and assign a central role to PcG proteins in this process.
Author	Otte, Arie P van Lohuizen, Maarten Stadler, Michael B Yokobayashi, Shihori Peters, Antoine H F M Orkin, Stuart H Terranova, Rémi
Author_xml	– sequence: 1 givenname: Rémi surname: Terranova fullname: Terranova, Rémi organization: Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland – sequence: 2 givenname: Shihori surname: Yokobayashi fullname: Yokobayashi, Shihori – sequence: 3 givenname: Michael B surname: Stadler fullname: Stadler, Michael B – sequence: 4 givenname: Arie P surname: Otte fullname: Otte, Arie P – sequence: 5 givenname: Maarten surname: van Lohuizen fullname: van Lohuizen, Maarten – sequence: 6 givenname: Stuart H surname: Orkin fullname: Orkin, Stuart H – sequence: 7 givenname: Antoine H F M surname: Peters fullname: Peters, Antoine H F M
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SubjectTerms	Animals Cell Nucleus - genetics Cell Nucleus - metabolism Chromatin Assembly and Disassembly DNA-Binding Proteins - metabolism Embryo, Mammalian - metabolism Enhancer of Zeste Homolog 2 Protein Female Genomic Imprinting Histone-Lysine N-Methyltransferase - metabolism Male Mice Polycomb Repressive Complex 1 Polycomb Repressive Complex 2 Repressor Proteins - metabolism RNA, Long Noncoding RNA, Untranslated - metabolism Ubiquitin-Protein Ligases - metabolism
Title	Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos
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