Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST
X-chromosome inactivation is a striking example of epigenetic silencing in which expression of the long non-coding RNA XIST initiates the heterochromatinization and silencing of one of the pair of X chromosomes in mammalian females. To understand how the RNA can establish silencing across millions o...
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| creator | Kelsey, Angela D Yang, Christine Leung, Danny Minks, Jakub Dixon-McDougall, Thomas Baldry, Sarah E L Bogutz, Aaron B Lefebvre, Louis Brown, Carolyn J |
| description | X-chromosome inactivation is a striking example of epigenetic silencing in which expression of the long non-coding RNA XIST initiates the heterochromatinization and silencing of one of the pair of X chromosomes in mammalian females. To understand how the RNA can establish silencing across millions of basepairs of DNA we have modelled the process by inducing expression of XIST from nine different locations in human HT1080 cells.
Localization of XIST, depletion of Cot-1 RNA, perinuclear localization, and ubiquitination of H2A occurs at all sites examined, while recruitment of H3K9me3 was not observed. Recruitment of the heterochromatic features SMCHD1, macroH2A, H3K27me3, and H4K20me1 occurs independently of each other in an integration site-dependent manner. Silencing of flanking reporter genes occurs at all sites, but the spread of silencing to flanking endogenous human genes is variable in extent of silencing as well as extent of spread, with silencing able to skip regions. The spread of H3K27me3 and loss of H3K27ac correlates with the pre-existing levels of the modifications, and overall the extent of silencing correlates with the ability to recruit additional heterochromatic features.
The non-coding RNA XIST functions as a cis-acting silencer when expressed from nine different locations throughout the genome. A hierarchy among the features of heterochromatin reveals the importance of interaction with the local chromatin neighborhood for optimal spread of silencing, as well as the independent yet cooperative nature of the establishment of heterochromatin by the non-coding XIST RNA. |
| doi_str_mv | 10.1186/s13059-015-0774-2 |
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Localization of XIST, depletion of Cot-1 RNA, perinuclear localization, and ubiquitination of H2A occurs at all sites examined, while recruitment of H3K9me3 was not observed. Recruitment of the heterochromatic features SMCHD1, macroH2A, H3K27me3, and H4K20me1 occurs independently of each other in an integration site-dependent manner. Silencing of flanking reporter genes occurs at all sites, but the spread of silencing to flanking endogenous human genes is variable in extent of silencing as well as extent of spread, with silencing able to skip regions. The spread of H3K27me3 and loss of H3K27ac correlates with the pre-existing levels of the modifications, and overall the extent of silencing correlates with the ability to recruit additional heterochromatic features.
The non-coding RNA XIST functions as a cis-acting silencer when expressed from nine different locations throughout the genome. A hierarchy among the features of heterochromatin reveals the importance of interaction with the local chromatin neighborhood for optimal spread of silencing, as well as the independent yet cooperative nature of the establishment of heterochromatin by the non-coding XIST RNA.</description><identifier>ISSN: 1474-760X</identifier><identifier>ISSN: 1474-7596</identifier><identifier>EISSN: 1474-760X</identifier><identifier>DOI: 10.1186/s13059-015-0774-2</identifier><identifier>PMID: 26429547</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Base pairs ; Chromatin ; Chromosomes ; Chromosomes, Human, X - genetics ; Deoxyribonucleic acid ; DNA ; DNA methylation ; Epigenesis, Genetic ; Epigenetic inheritance ; Female ; Gene Expression Regulation, Developmental ; Gene Silencing ; Gene therapy ; Genes ; Genome, Human ; Genomes ; Heterochromatin ; Heterochromatin - genetics ; Humans ; Localization ; Mammals ; Methods ; Non-coding RNA ; Physiological aspects ; Regulatory sequences ; RNA ; RNA, Long Noncoding - genetics ; RNA-mediated interference ; Stem cells ; Ubiquitination ; X Chromosome Inactivation - genetics ; X chromosomes ; X-chromosome inactivation</subject><ispartof>Genome Biology, 2015-10, Vol.16 (1), p.208-208, Article 208</ispartof><rights>COPYRIGHT 2015 BioMed Central Ltd.</rights><rights>2015. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Kelsey et al. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c628t-16971c0c0d762fba43edb22da2bcf2e7d7840218986f6377cc42d0770a2fd0313</citedby><cites>FETCH-LOGICAL-c628t-16971c0c0d762fba43edb22da2bcf2e7d7840218986f6377cc42d0770a2fd0313</cites><orcidid>0000-0002-8959-0101</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/PMC4591629/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4591629/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26429547$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kelsey, Angela D</creatorcontrib><creatorcontrib>Yang, Christine</creatorcontrib><creatorcontrib>Leung, Danny</creatorcontrib><creatorcontrib>Minks, Jakub</creatorcontrib><creatorcontrib>Dixon-McDougall, Thomas</creatorcontrib><creatorcontrib>Baldry, Sarah E L</creatorcontrib><creatorcontrib>Bogutz, Aaron B</creatorcontrib><creatorcontrib>Lefebvre, Louis</creatorcontrib><creatorcontrib>Brown, Carolyn J</creatorcontrib><title>Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST</title><title>Genome Biology</title><addtitle>Genome Biol</addtitle><description>X-chromosome inactivation is a striking example of epigenetic silencing in which expression of the long non-coding RNA XIST initiates the heterochromatinization and silencing of one of the pair of X chromosomes in mammalian females. To understand how the RNA can establish silencing across millions of basepairs of DNA we have modelled the process by inducing expression of XIST from nine different locations in human HT1080 cells.
Localization of XIST, depletion of Cot-1 RNA, perinuclear localization, and ubiquitination of H2A occurs at all sites examined, while recruitment of H3K9me3 was not observed. Recruitment of the heterochromatic features SMCHD1, macroH2A, H3K27me3, and H4K20me1 occurs independently of each other in an integration site-dependent manner. Silencing of flanking reporter genes occurs at all sites, but the spread of silencing to flanking endogenous human genes is variable in extent of silencing as well as extent of spread, with silencing able to skip regions. The spread of H3K27me3 and loss of H3K27ac correlates with the pre-existing levels of the modifications, and overall the extent of silencing correlates with the ability to recruit additional heterochromatic features.
The non-coding RNA XIST functions as a cis-acting silencer when expressed from nine different locations throughout the genome. A hierarchy among the features of heterochromatin reveals the importance of interaction with the local chromatin neighborhood for optimal spread of silencing, as well as the independent yet cooperative nature of the establishment of heterochromatin by the non-coding XIST RNA.</description><subject>Analysis</subject><subject>Base pairs</subject><subject>Chromatin</subject><subject>Chromosomes</subject><subject>Chromosomes, Human, X - genetics</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetic inheritance</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Silencing</subject><subject>Gene therapy</subject><subject>Genes</subject><subject>Genome, Human</subject><subject>Genomes</subject><subject>Heterochromatin</subject><subject>Heterochromatin - genetics</subject><subject>Humans</subject><subject>Localization</subject><subject>Mammals</subject><subject>Methods</subject><subject>Non-coding RNA</subject><subject>Physiological aspects</subject><subject>Regulatory sequences</subject><subject>RNA</subject><subject>RNA, Long Noncoding - genetics</subject><subject>RNA-mediated interference</subject><subject>Stem cells</subject><subject>Ubiquitination</subject><subject>X Chromosome Inactivation - genetics</subject><subject>X chromosomes</subject><subject>X-chromosome inactivation</subject><issn>1474-760X</issn><issn>1474-7596</issn><issn>1474-760X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>KPI</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNpdUk1v1DAQjRCIlsIP4IIscYFDisdx7PiCtKqArloBgiL1Zjn-yLok9jZOEO2vr6MtVRf54BnPezN-o1cUrwEfAzTsQ4IK16LEUJeYc1qSJ8Uh0Bxwhi-fPooPihcpXWEMghL2vDggjBJRU35YdOthq_SEokOuV-G3Dx3SmzEOMcVB9SjZ69kGbROKAfVRq97fqsnnRAWDku9zceG0N2jaWLSZBxVQiKHU0SzvP76u0OX658XL4plTfbKv7u-j4tfnTxcnp-X5ty_rk9V5qRlpphKY4KCxxoYz4lpFK2taQowirXbEcsMbigk0omGOVZxrTYnJ2rEizuAKqqPi467vdm4Ha7QN06h6uR39oMYbGZWX-5XgN7KLfyStBTAicoN39w3GmKWnSQ4-advn5dg4Jwk8T4caRJ2hb_-DXsV5DFmeJATzuhIMlh8d71Cd6q30wcU8V-dj7OB1DNblJcpVTaEWFaU4E97vETJmsn-nTs0pybPv630s7LB6jCmN1j0oBSwXj8idR2T2iFw8IknmvHm8ogfGP1NUd_DUtsQ</recordid><startdate>20151002</startdate><enddate>20151002</enddate><creator>Kelsey, Angela D</creator><creator>Yang, Christine</creator><creator>Leung, Danny</creator><creator>Minks, Jakub</creator><creator>Dixon-McDougall, Thomas</creator><creator>Baldry, Sarah E L</creator><creator>Bogutz, Aaron B</creator><creator>Lefebvre, Louis</creator><creator>Brown, Carolyn J</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>KPI</scope><scope>IAO</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8959-0101</orcidid></search><sort><creationdate>20151002</creationdate><title>Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST</title><author>Kelsey, Angela D ; Yang, Christine ; Leung, Danny ; Minks, Jakub ; Dixon-McDougall, Thomas ; Baldry, Sarah E L ; Bogutz, Aaron B ; Lefebvre, Louis ; Brown, Carolyn J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c628t-16971c0c0d762fba43edb22da2bcf2e7d7840218986f6377cc42d0770a2fd0313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Analysis</topic><topic>Base pairs</topic><topic>Chromatin</topic><topic>Chromosomes</topic><topic>Chromosomes, Human, X - genetics</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetic inheritance</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Silencing</topic><topic>Gene therapy</topic><topic>Genes</topic><topic>Genome, Human</topic><topic>Genomes</topic><topic>Heterochromatin</topic><topic>Heterochromatin - genetics</topic><topic>Humans</topic><topic>Localization</topic><topic>Mammals</topic><topic>Methods</topic><topic>Non-coding RNA</topic><topic>Physiological aspects</topic><topic>Regulatory sequences</topic><topic>RNA</topic><topic>RNA, Long Noncoding - genetics</topic><topic>RNA-mediated interference</topic><topic>Stem cells</topic><topic>Ubiquitination</topic><topic>X Chromosome Inactivation - genetics</topic><topic>X chromosomes</topic><topic>X-chromosome inactivation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kelsey, Angela D</creatorcontrib><creatorcontrib>Yang, Christine</creatorcontrib><creatorcontrib>Leung, Danny</creatorcontrib><creatorcontrib>Minks, Jakub</creatorcontrib><creatorcontrib>Dixon-McDougall, Thomas</creatorcontrib><creatorcontrib>Baldry, Sarah E L</creatorcontrib><creatorcontrib>Bogutz, Aaron B</creatorcontrib><creatorcontrib>Lefebvre, Louis</creatorcontrib><creatorcontrib>Brown, Carolyn J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Global Issues</collection><collection>Gale Academic OneFile</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome Biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kelsey, Angela D</au><au>Yang, Christine</au><au>Leung, Danny</au><au>Minks, Jakub</au><au>Dixon-McDougall, Thomas</au><au>Baldry, Sarah E L</au><au>Bogutz, Aaron B</au><au>Lefebvre, Louis</au><au>Brown, Carolyn J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST</atitle><jtitle>Genome Biology</jtitle><addtitle>Genome Biol</addtitle><date>2015-10-02</date><risdate>2015</risdate><volume>16</volume><issue>1</issue><spage>208</spage><epage>208</epage><pages>208-208</pages><artnum>208</artnum><issn>1474-760X</issn><issn>1474-7596</issn><eissn>1474-760X</eissn><abstract>X-chromosome inactivation is a striking example of epigenetic silencing in which expression of the long non-coding RNA XIST initiates the heterochromatinization and silencing of one of the pair of X chromosomes in mammalian females. To understand how the RNA can establish silencing across millions of basepairs of DNA we have modelled the process by inducing expression of XIST from nine different locations in human HT1080 cells.
Localization of XIST, depletion of Cot-1 RNA, perinuclear localization, and ubiquitination of H2A occurs at all sites examined, while recruitment of H3K9me3 was not observed. Recruitment of the heterochromatic features SMCHD1, macroH2A, H3K27me3, and H4K20me1 occurs independently of each other in an integration site-dependent manner. Silencing of flanking reporter genes occurs at all sites, but the spread of silencing to flanking endogenous human genes is variable in extent of silencing as well as extent of spread, with silencing able to skip regions. The spread of H3K27me3 and loss of H3K27ac correlates with the pre-existing levels of the modifications, and overall the extent of silencing correlates with the ability to recruit additional heterochromatic features.
The non-coding RNA XIST functions as a cis-acting silencer when expressed from nine different locations throughout the genome. A hierarchy among the features of heterochromatin reveals the importance of interaction with the local chromatin neighborhood for optimal spread of silencing, as well as the independent yet cooperative nature of the establishment of heterochromatin by the non-coding XIST RNA.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>26429547</pmid><doi>10.1186/s13059-015-0774-2</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-8959-0101</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Base pairs Chromatin Chromosomes Chromosomes, Human, X - genetics Deoxyribonucleic acid DNA DNA methylation Epigenesis, Genetic Epigenetic inheritance Female Gene Expression Regulation, Developmental Gene Silencing Gene therapy Genes Genome, Human Genomes Heterochromatin Heterochromatin - genetics Humans Localization Mammals Methods Non-coding RNA Physiological aspects Regulatory sequences RNA RNA, Long Noncoding - genetics RNA-mediated interference Stem cells Ubiquitination X Chromosome Inactivation - genetics X chromosomes X-chromosome inactivation |
| title | Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST |
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