Transposable elements are regulated by context-specific patterns of chromatin marks in mouse embryonic stem cells

The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this r...

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Published inNature communications Vol. 10; no. 1; pp. 34 - 13
Main Authors He, Jiangping, Fu, Xiuling, Zhang, Meng, He, Fangfang, Li, Wenjuan, Abdul, Mazid Md, Zhou, Jianguo, Sun, Li, Chang, Chen, Li, Yuhao, Liu, He, Wu, Kaixin, Babarinde, Isaac A., Zhuang, Qiang, Loh, Yuin-Han, Chen, Jiekai, Esteban, Miguel A., Hutchins, Andrew P.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 03.01.2019
Nature Publishing Group
Nature Portfolio
Subjects
13
13/1
13/89
38
38/39
45
45/100
45/15
45/88
45/91
631/208/176
631/208/177
631/208/212
631/532/2117
Accessibility
Animals
Cell Line
Chromatin
Chromatin - genetics
Chromatin - metabolism
Complexity
Deregulation
DNA Methylation - genetics
DNA Transposable Elements - genetics
Embryo cells
Embryos
Epigenesis, Genetic
Epigenetics
Gene Knockdown Techniques
Genomes
Hazards
Histone Code
Histones - genetics
Histones - metabolism
Humanities and Social Sciences
Mice
Mouse Embryonic Stem Cells
multidisciplinary
Science
Science (multidisciplinary)
Stem cell transplantation
Stem cells
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-018-08006-y

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Abstract The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1 , Ncor2 , Rnf2 , Kat5 , Prmt5 , Uhrf1 , and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs. Transposable elements (TEs) fulfill essential but poorly understood roles in genome organization and gene expression control. Here the authors show that the regulation of TEs occurs through overlapping epigenetic mechanisms that control the expression and chromatin signatures at TEs.
AbstractList The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1 , Ncor2 , Rnf2 , Kat5 , Prmt5 , Uhrf1 , and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs. Transposable elements (TEs) fulfill essential but poorly understood roles in genome organization and gene expression control. Here the authors show that the regulation of TEs occurs through overlapping epigenetic mechanisms that control the expression and chromatin signatures at TEs.
The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1, Ncor2, Rnf2, Kat5, Prmt5, Uhrf1, and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs.
The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1, Ncor2, Rnf2, Kat5, Prmt5, Uhrf1, and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs.
Transposable elements (TEs) fulfill essential but poorly understood roles in genome organization and gene expression control. Here the authors show that the regulation of TEs occurs through overlapping epigenetic mechanisms that control the expression and chromatin signatures at TEs.
The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1 , Ncor2 , Rnf2 , Kat5 , Prmt5 , Uhrf1 , and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs.
The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1, Ncor2, Rnf2, Kat5, Prmt5, Uhrf1, and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs.The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions, they are a potential danger to genomic stability and are carefully regulated by the epigenetic system. However, the full complexity of this regulatory system is not understood. Here, using mouse embryonic stem cells, we show that TEs are suppressed by heterochromatic marks like H3K9me3, and are also labelled by all major types of chromatin modification in complex patterns, including bivalent activatory and repressive marks. We identified 29 epigenetic modifiers that significantly deregulated at least one type of TE. The loss of Setdb1, Ncor2, Rnf2, Kat5, Prmt5, Uhrf1, and Rrp8 caused widespread changes in TE expression and chromatin accessibility. These effects were context-specific, with different chromatin modifiers regulating the expression and chromatin accessibility of specific subsets of TEs. Our work reveals the complex patterns of epigenetic regulation of TEs.
ArticleNumber 34
Author Fu, Xiuling
Liu, He
Li, Wenjuan
He, Fangfang
Abdul, Mazid Md
Wu, Kaixin
Chang, Chen
Chen, Jiekai
Zhou, Jianguo
Babarinde, Isaac A.
Zhuang, Qiang
Hutchins, Andrew P.
Sun, Li
Loh, Yuin-Han
Zhang, Meng
Esteban, Miguel A.
He, Jiangping
Li, Yuhao
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Joint School of Life Sciences, Guangzhou Medical University and Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Regenerative Medicine and Health-Guangdong Laboratory (GRMH-GDL), University of Chinese Academy of Sciences
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  organization: Department of Biology, Southern University of Science and Technology
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Joint School of Life Sciences, Guangzhou Medical University and Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Regenerative Medicine and Health-Guangdong Laboratory (GRMH-GDL), University of Chinese Academy of Sciences, Laboratory of RNA, Chromatin, and Human Disease, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Joint School of Life Sciences, Guangzhou Medical University and Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Regenerative Medicine and Health-Guangdong Laboratory (GRMH-GDL), University of Chinese Academy of Sciences, Laboratory of RNA, Chromatin, and Human Disease, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Joint School of Life Sciences, Guangzhou Medical University and Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Regenerative Medicine and Health-Guangdong Laboratory (GRMH-GDL), Laboratory of RNA, Chromatin, and Human Disease, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences
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  organization: Department of Biology, Southern University of Science and Technology
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  organization: Department of Biology, Southern University of Science and Technology
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  organization: Department of Biology, Southern University of Science and Technology
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences
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  organization: Key Laboratory of Regenerative Biology of the Chinese Academy of Sciences and Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences
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  organization: Department of Biology, Southern University of Science and Technology
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  givenname: Qiang
  surname: Zhuang
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  organization: Department of Biology, Southern University of Science and Technology, State Key Laboratory of Medicinal Chemical Biology and College of Life Sciences, Nankai University
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  givenname: Yuin-Han
  surname: Loh
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  organization: Epigenetics and Cell Fates Laboratory, ASTAR Institute of Molecular and Cell Biology, Department of Biological Sciences, National University of Singapore
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  surname: Chen
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  givenname: Andrew P.
  orcidid: 0000-0001-7784-2255
  surname: Hutchins
  fullname: Hutchins, Andrew P.
  email: andrewh@sustc.edu.cn
  organization: Department of Biology, Southern University of Science and Technology
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30604769$$D View this record in MEDLINE/PubMed
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Snippet The majority of mammalian genomes are devoted to transposable elements (TEs). Whilst TEs are increasingly recognized for their important biological functions,...
Transposable elements (TEs) fulfill essential but poorly understood roles in genome organization and gene expression control. Here the authors show that the...
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Accessibility
Animals
Cell Line
Chromatin
Chromatin - genetics
Chromatin - metabolism
Complexity
Deregulation
DNA Methylation - genetics
DNA Transposable Elements - genetics
Embryo cells
Embryos
Epigenesis, Genetic
Epigenetics
Gene Knockdown Techniques
Genomes
Hazards
Histone Code
Histones - genetics
Histones - metabolism
Humanities and Social Sciences
Mice
Mouse Embryonic Stem Cells
multidisciplinary
Science
Science (multidisciplinary)
Stem cell transplantation
Stem cells
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Title Transposable elements are regulated by context-specific patterns of chromatin marks in mouse embryonic stem cells
URI https://link.springer.com/article/10.1038/s41467-018-08006-y
https://www.ncbi.nlm.nih.gov/pubmed/30604769
https://www.proquest.com/docview/2163007704
https://www.proquest.com/docview/2163012180
https://pubmed.ncbi.nlm.nih.gov/PMC6318327
https://doaj.org/article/514209f5475741538fad4a2b8992fecb
Volume 10
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