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Linear decay of retrotransposon antisense bias across genes is contingent upon tissue specificity
Retrotransposons comprise approximately half of the human genome and contribute to chromatin structure, regulatory motifs, and protein-coding sequences. Since retrotransposon insertions can disrupt functional genetic elements as well as introduce new sequence motifs to a region, they have the potent...
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Published in: | PloS one 2013-11, Vol.8 (11), p.e79402-e79402 |
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description | Retrotransposons comprise approximately half of the human genome and contribute to chromatin structure, regulatory motifs, and protein-coding sequences. Since retrotransposon insertions can disrupt functional genetic elements as well as introduce new sequence motifs to a region, they have the potential to affect the function of genes that harbour insertions as well as those nearby. Partly as a result of these effects, the distribution of retrotransposons across the genome is non-uniform and there are observed imbalances in the orientation of insertions with respect to the transcriptional direction of the containing gene. Although some of the factors underlying the observed distributions are understood, much of the variability remains unexplained. Detailed characterization of retrotransposon density in genes could help inform predictions of the functional consequence of de novo as well as polymorphic insertions. In order to characterize the relationship between genes and inserted elements, we have examined the distribution of retrotransposons and their internal motifs within tissue-specific and housekeeping genes. We have identified that the previously established retrotransposon antisense bias decays at a linear rate across genes, resulting in an equal density of sense and antisense retrotransposons near the 3'-UTR. In addition, the decay of antisense bias across genes is less pronounced among tissue-specific genes. Our results provide support for the scenario in which this linear decay in antisense bias is established by natural selection shortly after retrotransposon integration, and that total antisense bias observed is above and beyond any bias introduced by the integration process itself. Finally, we provide an example of a retrotransposon acting as an eQTL on a coincident gene, highlighting one of several possible avenues through which insertions may modulate gene function. |
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Since retrotransposon insertions can disrupt functional genetic elements as well as introduce new sequence motifs to a region, they have the potential to affect the function of genes that harbour insertions as well as those nearby. Partly as a result of these effects, the distribution of retrotransposons across the genome is non-uniform and there are observed imbalances in the orientation of insertions with respect to the transcriptional direction of the containing gene. Although some of the factors underlying the observed distributions are understood, much of the variability remains unexplained. Detailed characterization of retrotransposon density in genes could help inform predictions of the functional consequence of de novo as well as polymorphic insertions. In order to characterize the relationship between genes and inserted elements, we have examined the distribution of retrotransposons and their internal motifs within tissue-specific and housekeeping genes. We have identified that the previously established retrotransposon antisense bias decays at a linear rate across genes, resulting in an equal density of sense and antisense retrotransposons near the 3'-UTR. In addition, the decay of antisense bias across genes is less pronounced among tissue-specific genes. Our results provide support for the scenario in which this linear decay in antisense bias is established by natural selection shortly after retrotransposon integration, and that total antisense bias observed is above and beyond any bias introduced by the integration process itself. Finally, we provide an example of a retrotransposon acting as an eQTL on a coincident gene, highlighting one of several possible avenues through which insertions may modulate gene function.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0079402</identifier><identifier>PMID: 24244495</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3' Untranslated regions ; 5' Untranslated Regions ; Alu Elements - genetics ; Antisense RNA ; Bias ; Binding sites ; Chromatin ; Decay ; DNA methylation ; Evolution ; Evolution, Molecular ; Exons ; Gene expression ; Gene Frequency ; Gene sequencing ; Genes ; Genetic aspects ; Genomes ; Genomics ; Humans ; Integration ; Long Interspersed Nucleotide Elements - genetics ; Natural selection ; Nucleotide Motifs ; Organ Specificity - genetics ; Polymorphism, Genetic ; Protein structure ; Quantitative Trait Loci ; Retroelements - genetics ; RNA, Antisense ; Transcription ; Transcription (Genetics) ; Transposons</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e79402-e79402</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Linker, Hedges. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Linker, Hedges 2013 Linker, Hedges</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-4a5d129fd8d6151573326f4a427a5c2cb01e343ab37e26d3205728f2c49080b73</citedby><cites>FETCH-LOGICAL-c692t-4a5d129fd8d6151573326f4a427a5c2cb01e343ab37e26d3205728f2c49080b73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1458577074/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1458577074?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24244495$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kashkush, Khalil</contributor><creatorcontrib>Linker, Sara</creatorcontrib><creatorcontrib>Hedges, Dale J</creatorcontrib><title>Linear decay of retrotransposon antisense bias across genes is contingent upon tissue specificity</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Retrotransposons comprise approximately half of the human genome and contribute to chromatin structure, regulatory motifs, and protein-coding sequences. Since retrotransposon insertions can disrupt functional genetic elements as well as introduce new sequence motifs to a region, they have the potential to affect the function of genes that harbour insertions as well as those nearby. Partly as a result of these effects, the distribution of retrotransposons across the genome is non-uniform and there are observed imbalances in the orientation of insertions with respect to the transcriptional direction of the containing gene. Although some of the factors underlying the observed distributions are understood, much of the variability remains unexplained. Detailed characterization of retrotransposon density in genes could help inform predictions of the functional consequence of de novo as well as polymorphic insertions. In order to characterize the relationship between genes and inserted elements, we have examined the distribution of retrotransposons and their internal motifs within tissue-specific and housekeeping genes. We have identified that the previously established retrotransposon antisense bias decays at a linear rate across genes, resulting in an equal density of sense and antisense retrotransposons near the 3'-UTR. In addition, the decay of antisense bias across genes is less pronounced among tissue-specific genes. Our results provide support for the scenario in which this linear decay in antisense bias is established by natural selection shortly after retrotransposon integration, and that total antisense bias observed is above and beyond any bias introduced by the integration process itself. Finally, we provide an example of a retrotransposon acting as an eQTL on a coincident gene, highlighting one of several possible avenues through which insertions may modulate gene function.</description><subject>3' Untranslated regions</subject><subject>5' Untranslated Regions</subject><subject>Alu Elements - genetics</subject><subject>Antisense RNA</subject><subject>Bias</subject><subject>Binding sites</subject><subject>Chromatin</subject><subject>Decay</subject><subject>DNA methylation</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Exons</subject><subject>Gene expression</subject><subject>Gene Frequency</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Humans</subject><subject>Integration</subject><subject>Long Interspersed Nucleotide Elements - genetics</subject><subject>Natural selection</subject><subject>Nucleotide Motifs</subject><subject>Organ Specificity - genetics</subject><subject>Polymorphism, Genetic</subject><subject>Protein structure</subject><subject>Quantitative Trait Loci</subject><subject>Retroelements - genetics</subject><subject>RNA, Antisense</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Transposons</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0trGzEQx5fS0qRpv0FpBYXSHuzqudJeCiH0YTAE-rqKWa3WVlhLjrRb6m9f2d4Eb8mh6KDH_OYvzYymKF4SPCdMkg83YYgeuvk2eDvHWFYc00fFOakYnZUUs8cn67PiWUo3GAumyvJpcUY55ZxX4ryApfMWImqsgR0KLYq2j6GP4NM2pOAR-N4l65NFtYOEwMSQElpZbxNyCZmQ7T5vezTkl6AMp8GitLXGtc64fve8eNJCl-yLcb4ofn7-9OPq62x5_WVxdbmcmbKi_YyDaAit2kY1JRFESMZo2XLgVIIw1NSYWMYZ1ExaWjaMYiGpaqnhFVa4luyieH3U3XYh6TE7SRMulJASS56JxZFoAtzobXQbiDsdwOnDQYgrDbF3prNaEdzwtjUVxpSrGivgAkpKiKgkJoRkrY_jbUO9sY3JCYjQTUSnFu_WehV-a6aoYlJlgXejQAy3g0293rhkbNeBt2E4vLsSQlWUZvTNP-jD0Y3UCnIAzrf7Kpq9qL7kUtFMEZyp-QNUHo3duFxM27p8PnF4P3HYF9z-6VcwpKQX37_9P3v9a8q-PWHXFrp-nUI39C74NAX5ETz8vGjb-yQTrPedcJcNve8EPXZCdnt1WqB7p7uvz_4C9FwCXw</recordid><startdate>20131114</startdate><enddate>20131114</enddate><creator>Linker, Sara</creator><creator>Hedges, Dale J</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131114</creationdate><title>Linear decay of retrotransposon antisense bias across genes is contingent upon tissue specificity</title><author>Linker, Sara ; Hedges, Dale J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-4a5d129fd8d6151573326f4a427a5c2cb01e343ab37e26d3205728f2c49080b73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>3' Untranslated regions</topic><topic>5' Untranslated Regions</topic><topic>Alu Elements - 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Since retrotransposon insertions can disrupt functional genetic elements as well as introduce new sequence motifs to a region, they have the potential to affect the function of genes that harbour insertions as well as those nearby. Partly as a result of these effects, the distribution of retrotransposons across the genome is non-uniform and there are observed imbalances in the orientation of insertions with respect to the transcriptional direction of the containing gene. Although some of the factors underlying the observed distributions are understood, much of the variability remains unexplained. Detailed characterization of retrotransposon density in genes could help inform predictions of the functional consequence of de novo as well as polymorphic insertions. In order to characterize the relationship between genes and inserted elements, we have examined the distribution of retrotransposons and their internal motifs within tissue-specific and housekeeping genes. We have identified that the previously established retrotransposon antisense bias decays at a linear rate across genes, resulting in an equal density of sense and antisense retrotransposons near the 3'-UTR. In addition, the decay of antisense bias across genes is less pronounced among tissue-specific genes. Our results provide support for the scenario in which this linear decay in antisense bias is established by natural selection shortly after retrotransposon integration, and that total antisense bias observed is above and beyond any bias introduced by the integration process itself. Finally, we provide an example of a retrotransposon acting as an eQTL on a coincident gene, highlighting one of several possible avenues through which insertions may modulate gene function.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24244495</pmid><doi>10.1371/journal.pone.0079402</doi><tpages>e79402</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 3' Untranslated regions 5' Untranslated Regions Alu Elements - genetics Antisense RNA Bias Binding sites Chromatin Decay DNA methylation Evolution Evolution, Molecular Exons Gene expression Gene Frequency Gene sequencing Genes Genetic aspects Genomes Genomics Humans Integration Long Interspersed Nucleotide Elements - genetics Natural selection Nucleotide Motifs Organ Specificity - genetics Polymorphism, Genetic Protein structure Quantitative Trait Loci Retroelements - genetics RNA, Antisense Transcription Transcription (Genetics) Transposons |
title | Linear decay of retrotransposon antisense bias across genes is contingent upon tissue specificity |
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