Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms
The "arms race" relationship between transposable elements (TEs) and their host has promoted a series of epigenetic silencing mechanisms directed against TEs. Retrotransposons, a class of TEs, are often located in repressed regions and are thought to induce heterochromatin formation and sp...
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| creator | Rebollo, Rita Karimi, Mohammad M Bilenky, Misha Gagnier, Liane Miceli-Royer, Katharine Zhang, Ying Goyal, Preeti Keane, Thomas M Jones, Steven Hirst, Martin Lorincz, Matthew C Mager, Dixie L |
| description | The "arms race" relationship between transposable elements (TEs) and their host has promoted a series of epigenetic silencing mechanisms directed against TEs. Retrotransposons, a class of TEs, are often located in repressed regions and are thought to induce heterochromatin formation and spreading. However, direct evidence for TE-induced local heterochromatin in mammals is surprisingly scarce. To examine this phenomenon, we chose two mouse embryonic stem (ES) cell lines that possess insertionally polymorphic retrotransposons (IAP, ETn/MusD, and LINE elements) at specific loci in one cell line but not the other. Employing ChIP-seq data for these cell lines, we show that IAP elements robustly induce H3K9me3 and H4K20me3 marks in flanking genomic DNA. In contrast, such heterochromatin is not induced by LINE copies and only by a minority of polymorphic ETn/MusD copies. DNA methylation is independent of the presence of IAP copies, since it is present in flanking regions of both full and empty sites. Finally, such spreading into genes appears to be rare, since the transcriptional start sites of very few genes are less than one Kb from an IAP. However, the B3galtl gene is subject to transcriptional silencing via IAP-induced heterochromatin. Hence, although rare, IAP-induced local heterochromatin spreading into nearby genes may influence expression and, in turn, host fitness. |
| doi_str_mv | 10.1371/journal.pgen.1002301 |
| format | Article |
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Retrotransposons, a class of TEs, are often located in repressed regions and are thought to induce heterochromatin formation and spreading. However, direct evidence for TE-induced local heterochromatin in mammals is surprisingly scarce. To examine this phenomenon, we chose two mouse embryonic stem (ES) cell lines that possess insertionally polymorphic retrotransposons (IAP, ETn/MusD, and LINE elements) at specific loci in one cell line but not the other. Employing ChIP-seq data for these cell lines, we show that IAP elements robustly induce H3K9me3 and H4K20me3 marks in flanking genomic DNA. In contrast, such heterochromatin is not induced by LINE copies and only by a minority of polymorphic ETn/MusD copies. DNA methylation is independent of the presence of IAP copies, since it is present in flanking regions of both full and empty sites. Finally, such spreading into genes appears to be rare, since the transcriptional start sites of very few genes are less than one Kb from an IAP. However, the B3galtl gene is subject to transcriptional silencing via IAP-induced heterochromatin. Hence, although rare, IAP-induced local heterochromatin spreading into nearby genes may influence expression and, in turn, host fitness.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1002301</identifier><identifier>PMID: 21980304</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology ; Cell Line ; Chromatin Immunoprecipitation ; Deoxyribonucleic acid ; DNA ; DNA methylation ; Embryonic Stem Cells - cytology ; Epigenesis, Genetic - genetics ; Gene Expression Regulation ; Gene Silencing ; Genetics ; Glycosyltransferases - genetics ; Glycosyltransferases - metabolism ; Heterochromatin - genetics ; Heterochromatin - metabolism ; Life Sciences ; Long Interspersed Nucleotide Elements - genetics ; Medical research ; Mice ; Mutagenesis, Insertional - genetics ; Polymorphism, Genetic ; Proteins ; Retroelements - genetics ; Stem cells</subject><ispartof>PLoS genetics, 2011-09, Vol.7 (9), p.e1002301-14</ispartof><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Rebollo et al. 2011</rights><rights>2011 Rebollo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, et al. (2011) Retrotransposon-Induced Heterochromatin Spreading in the Mouse Revealed by Insertional Polymorphisms. 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Hence, although rare, IAP-induced local heterochromatin spreading into nearby genes may influence expression and, in turn, host fitness.</description><subject>Animals</subject><subject>Biology</subject><subject>Cell Line</subject><subject>Chromatin Immunoprecipitation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>Embryonic Stem Cells - cytology</subject><subject>Epigenesis, Genetic - genetics</subject><subject>Gene Expression Regulation</subject><subject>Gene Silencing</subject><subject>Genetics</subject><subject>Glycosyltransferases - genetics</subject><subject>Glycosyltransferases - metabolism</subject><subject>Heterochromatin - genetics</subject><subject>Heterochromatin - metabolism</subject><subject>Life Sciences</subject><subject>Long Interspersed Nucleotide Elements - genetics</subject><subject>Medical research</subject><subject>Mice</subject><subject>Mutagenesis, Insertional - genetics</subject><subject>Polymorphism, Genetic</subject><subject>Proteins</subject><subject>Retroelements - genetics</subject><subject>Stem cells</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNpdUk1r3DAQNaWl-Wj_QWl97cFbySOvpEshhOYDFgohPQtZGq292JKRvAv776PNbkLSk6SZ957eDK8ovlGyoMDpr03YRq-HxbRGv6CE1EDoh-KcNg1UnBH28c39rLhIaUMINELyz8VZTaUgQNh5YR9wjmGO2qcppOCr3tutQVt2OGMMpoth1HPvyzRF1Lb36zI_5g7LMWwTlhF3qIeMb_e5kTDOfciuyikM-zHEqevTmL4Un5weEn49nZfFv5s_j9d31erv7f311aoyjeRz1WprnBNMEApONkxYK-WSt_lheWsNGGccW0J2D5Jy1ta2xuwVWsqYNQQuix9H3WkISZ0WlBQFCg2TkoqMuD8ibNAbNcV-1HGvgu7VcyHEtdJ5BDOgEmBZwzlg7TjTgkiClmcrFGoHRMqs9fv027Yd0Rr0eY3DO9H3Hd93ah12CrIRIpos8PMo0P1Hu7taqUON1MuG1ozsaMayI9bEkFJE90qgRB3y8DKuOuRBnfKQad_fenwlvQQAngAjw7bg</recordid><startdate>20110901</startdate><enddate>20110901</enddate><creator>Rebollo, Rita</creator><creator>Karimi, Mohammad M</creator><creator>Bilenky, Misha</creator><creator>Gagnier, Liane</creator><creator>Miceli-Royer, Katharine</creator><creator>Zhang, Ying</creator><creator>Goyal, Preeti</creator><creator>Keane, Thomas M</creator><creator>Jones, Steven</creator><creator>Hirst, Martin</creator><creator>Lorincz, Matthew C</creator><creator>Mager, Dixie L</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-8138-5082</orcidid></search><sort><creationdate>20110901</creationdate><title>Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms</title><author>Rebollo, Rita ; 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Retrotransposons, a class of TEs, are often located in repressed regions and are thought to induce heterochromatin formation and spreading. However, direct evidence for TE-induced local heterochromatin in mammals is surprisingly scarce. To examine this phenomenon, we chose two mouse embryonic stem (ES) cell lines that possess insertionally polymorphic retrotransposons (IAP, ETn/MusD, and LINE elements) at specific loci in one cell line but not the other. Employing ChIP-seq data for these cell lines, we show that IAP elements robustly induce H3K9me3 and H4K20me3 marks in flanking genomic DNA. In contrast, such heterochromatin is not induced by LINE copies and only by a minority of polymorphic ETn/MusD copies. DNA methylation is independent of the presence of IAP copies, since it is present in flanking regions of both full and empty sites. Finally, such spreading into genes appears to be rare, since the transcriptional start sites of very few genes are less than one Kb from an IAP. However, the B3galtl gene is subject to transcriptional silencing via IAP-induced heterochromatin. Hence, although rare, IAP-induced local heterochromatin spreading into nearby genes may influence expression and, in turn, host fitness.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21980304</pmid><doi>10.1371/journal.pgen.1002301</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-8138-5082</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biology Cell Line Chromatin Immunoprecipitation Deoxyribonucleic acid DNA DNA methylation Embryonic Stem Cells - cytology Epigenesis, Genetic - genetics Gene Expression Regulation Gene Silencing Genetics Glycosyltransferases - genetics Glycosyltransferases - metabolism Heterochromatin - genetics Heterochromatin - metabolism Life Sciences Long Interspersed Nucleotide Elements - genetics Medical research Mice Mutagenesis, Insertional - genetics Polymorphism, Genetic Proteins Retroelements - genetics Stem cells |
| title | Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms |
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