Coordinated changes in gene expression, H1 variant distribution and genome 3D conformation in response to H1 depletion
Abstract Up to seven members of the histone H1 family may contribute to chromatin compaction and its regulation in human somatic cells. In breast cancer cells, knock-down of multiple H1 variants deregulates many genes, promotes the appearance of genome-wide accessibility sites and triggers an interf...
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Veröffentlicht in: | Nucleic acids research 2022-04, Vol.50 (7), p.3892-3910 |
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creator | Serna-Pujol, Núria Salinas-Pena, Mónica Mugianesi, Francesca Le Dily, François Marti-Renom, Marc A Jordan, Albert |
description | Abstract
Up to seven members of the histone H1 family may contribute to chromatin compaction and its regulation in human somatic cells. In breast cancer cells, knock-down of multiple H1 variants deregulates many genes, promotes the appearance of genome-wide accessibility sites and triggers an interferon response via activation of heterochromatic repeats. However, how these changes in the expression profile relate to the re-distribution of H1 variants as well as to genome conformational changes have not been yet studied. Here, we combined ChIP-seq of five endogenous H1 variants with Chromosome Conformation Capture analysis in wild-type and H1.2/H1.4 knock-down T47D cells. The results indicate that H1 variants coexist in the genome in two large groups depending on the local GC content and that their distribution is robust with respect to H1 depletion. Despite the small changes in H1 variants distribution, knock-down of H1 translated into more isolated but de-compacted chromatin structures at the scale of topologically associating domains (TADs). Such changes in TAD structure correlated with a coordinated gene expression response of their resident genes. This is the first report describing simultaneous profiling of five endogenous H1 variants and giving functional evidence of genome topology alterations upon H1 depletion in human cancer cells. |
doi_str_mv | 10.1093/nar/gkac226 |
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Up to seven members of the histone H1 family may contribute to chromatin compaction and its regulation in human somatic cells. In breast cancer cells, knock-down of multiple H1 variants deregulates many genes, promotes the appearance of genome-wide accessibility sites and triggers an interferon response via activation of heterochromatic repeats. However, how these changes in the expression profile relate to the re-distribution of H1 variants as well as to genome conformational changes have not been yet studied. Here, we combined ChIP-seq of five endogenous H1 variants with Chromosome Conformation Capture analysis in wild-type and H1.2/H1.4 knock-down T47D cells. The results indicate that H1 variants coexist in the genome in two large groups depending on the local GC content and that their distribution is robust with respect to H1 depletion. Despite the small changes in H1 variants distribution, knock-down of H1 translated into more isolated but de-compacted chromatin structures at the scale of topologically associating domains (TADs). Such changes in TAD structure correlated with a coordinated gene expression response of their resident genes. This is the first report describing simultaneous profiling of five endogenous H1 variants and giving functional evidence of genome topology alterations upon H1 depletion in human cancer cells.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkac226</identifier><identifier>PMID: 35380694</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Base Composition ; Chromatin - genetics ; Chromatin Assembly and Disassembly ; Gene Expression ; Gene regulation, Chromatin and Epigenetics ; Histones - genetics ; Histones - metabolism ; Humans</subject><ispartof>Nucleic acids research, 2022-04, Vol.50 (7), p.3892-3910</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-a87778e56c3ca1054400c7dcc672ac2b9a436af0290ab97e2a966f6b791027283</citedby><cites>FETCH-LOGICAL-c412t-a87778e56c3ca1054400c7dcc672ac2b9a436af0290ab97e2a966f6b791027283</cites><orcidid>0000-0002-0151-4279 ; 0000-0002-8324-7927 ; 0000-0001-8134-7038 ; 0000-0002-3970-8693</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9023279/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9023279/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35380694$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Serna-Pujol, Núria</creatorcontrib><creatorcontrib>Salinas-Pena, Mónica</creatorcontrib><creatorcontrib>Mugianesi, Francesca</creatorcontrib><creatorcontrib>Le Dily, François</creatorcontrib><creatorcontrib>Marti-Renom, Marc A</creatorcontrib><creatorcontrib>Jordan, Albert</creatorcontrib><title>Coordinated changes in gene expression, H1 variant distribution and genome 3D conformation in response to H1 depletion</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Abstract
Up to seven members of the histone H1 family may contribute to chromatin compaction and its regulation in human somatic cells. In breast cancer cells, knock-down of multiple H1 variants deregulates many genes, promotes the appearance of genome-wide accessibility sites and triggers an interferon response via activation of heterochromatic repeats. However, how these changes in the expression profile relate to the re-distribution of H1 variants as well as to genome conformational changes have not been yet studied. Here, we combined ChIP-seq of five endogenous H1 variants with Chromosome Conformation Capture analysis in wild-type and H1.2/H1.4 knock-down T47D cells. The results indicate that H1 variants coexist in the genome in two large groups depending on the local GC content and that their distribution is robust with respect to H1 depletion. Despite the small changes in H1 variants distribution, knock-down of H1 translated into more isolated but de-compacted chromatin structures at the scale of topologically associating domains (TADs). Such changes in TAD structure correlated with a coordinated gene expression response of their resident genes. This is the first report describing simultaneous profiling of five endogenous H1 variants and giving functional evidence of genome topology alterations upon H1 depletion in human cancer cells.</description><subject>Base Composition</subject><subject>Chromatin - genetics</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Gene Expression</subject><subject>Gene regulation, Chromatin and Epigenetics</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Humans</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhi0EotvCiTvyCSGVUH_Fji-V0PJRpEpc4GxNnMnWkNjBTlbw78mySwUXTj68zzzj0UvIM85ec2blVYR8tfsGXgj9gGy41KJSVouHZMMkqyvOVHNGzkv5yhhXvFaPyZmsZcO0VRuy36aUuxBhxo76O4g7LDREusOIFH9MGUsJKb6iN5zuIQeIM-1CmXNol3kNKMTuAKcRqXxLfYp9yiP8jlbNOj6lWJDO6WDocBrwkD0hj3oYCj49vRfky_t3n7c31e2nDx-3b24rr7iYK2iMMQ3W2ksPnNVKMeZN5702Yj24taCkhp4Jy6C1BgVYrXvdGsuZMKKRF-T66J2WdsTOY5wzDG7KYYT80yUI7t8khju3S3tnmZDC2FXw8iTI6fuCZXZjKB6HASKmpTihlRGcG6FX9PKI-pxKydjfr-HMHZpya1Pu1NRKP__7Z_fsn2pW4MURSMv0X9Mv09ae6A</recordid><startdate>20220422</startdate><enddate>20220422</enddate><creator>Serna-Pujol, Núria</creator><creator>Salinas-Pena, Mónica</creator><creator>Mugianesi, Francesca</creator><creator>Le Dily, François</creator><creator>Marti-Renom, Marc A</creator><creator>Jordan, Albert</creator><general>Oxford University Press</general><scope>TOX</scope><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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0151-4279</orcidid><orcidid>https://orcid.org/0000-0002-8324-7927</orcidid><orcidid>https://orcid.org/0000-0001-8134-7038</orcidid><orcidid>https://orcid.org/0000-0002-3970-8693</orcidid></search><sort><creationdate>20220422</creationdate><title>Coordinated changes in gene expression, H1 variant distribution and genome 3D conformation in response to H1 depletion</title><author>Serna-Pujol, Núria ; Salinas-Pena, Mónica ; Mugianesi, Francesca ; Le Dily, François ; Marti-Renom, Marc A ; Jordan, Albert</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-a87778e56c3ca1054400c7dcc672ac2b9a436af0290ab97e2a966f6b791027283</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Base Composition</topic><topic>Chromatin - genetics</topic><topic>Chromatin Assembly and Disassembly</topic><topic>Gene Expression</topic><topic>Gene regulation, Chromatin and Epigenetics</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>Humans</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Serna-Pujol, Núria</creatorcontrib><creatorcontrib>Salinas-Pena, Mónica</creatorcontrib><creatorcontrib>Mugianesi, Francesca</creatorcontrib><creatorcontrib>Le Dily, François</creatorcontrib><creatorcontrib>Marti-Renom, Marc A</creatorcontrib><creatorcontrib>Jordan, Albert</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Serna-Pujol, Núria</au><au>Salinas-Pena, Mónica</au><au>Mugianesi, Francesca</au><au>Le Dily, François</au><au>Marti-Renom, Marc A</au><au>Jordan, Albert</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coordinated changes in gene expression, H1 variant distribution and genome 3D conformation in response to H1 depletion</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2022-04-22</date><risdate>2022</risdate><volume>50</volume><issue>7</issue><spage>3892</spage><epage>3910</epage><pages>3892-3910</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Abstract
Up to seven members of the histone H1 family may contribute to chromatin compaction and its regulation in human somatic cells. In breast cancer cells, knock-down of multiple H1 variants deregulates many genes, promotes the appearance of genome-wide accessibility sites and triggers an interferon response via activation of heterochromatic repeats. However, how these changes in the expression profile relate to the re-distribution of H1 variants as well as to genome conformational changes have not been yet studied. Here, we combined ChIP-seq of five endogenous H1 variants with Chromosome Conformation Capture analysis in wild-type and H1.2/H1.4 knock-down T47D cells. The results indicate that H1 variants coexist in the genome in two large groups depending on the local GC content and that their distribution is robust with respect to H1 depletion. Despite the small changes in H1 variants distribution, knock-down of H1 translated into more isolated but de-compacted chromatin structures at the scale of topologically associating domains (TADs). Such changes in TAD structure correlated with a coordinated gene expression response of their resident genes. This is the first report describing simultaneous profiling of five endogenous H1 variants and giving functional evidence of genome topology alterations upon H1 depletion in human cancer cells.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>35380694</pmid><doi>10.1093/nar/gkac226</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-0151-4279</orcidid><orcidid>https://orcid.org/0000-0002-8324-7927</orcidid><orcidid>https://orcid.org/0000-0001-8134-7038</orcidid><orcidid>https://orcid.org/0000-0002-3970-8693</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Base Composition Chromatin - genetics Chromatin Assembly and Disassembly Gene Expression Gene regulation, Chromatin and Epigenetics Histones - genetics Histones - metabolism Humans |
title | Coordinated changes in gene expression, H1 variant distribution and genome 3D conformation in response to H1 depletion |
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