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N6-methyldeoxyadenosine directs nucleosome positioning in Tetrahymena DNA
Background N6-methyldeoxyadenosine (6mA or m6dA) was shown more than 40 years ago in simple eukaryotes. Recent studies revealed the presence of 6mA in more prevalent eukaryotes, even in vertebrates. However, functional characterizations have been limited. Results We use Tetrahymena thermophila as a...
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Published in: | Genome Biology 2018-11, Vol.19 (1), p.200-200, Article 200 |
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creator | Luo, Guan-Zheng Hao, Ziyang Luo, Liangzhi Shen, Mingren Sparvoli, Daniela Zheng, Yuqing Zhang, Zijie Weng, Xiaocheng Chen, Kai Cui, Qiang Turkewitz, Aaron P. He, Chuan |
description | Background N6-methyldeoxyadenosine (6mA or m6dA) was shown more than 40 years ago in simple eukaryotes. Recent studies revealed the presence of 6mA in more prevalent eukaryotes, even in vertebrates. However, functional characterizations have been limited. Results We use Tetrahymena thermophila as a model organism to examine the effects of 6mA on nucleosome positioning. Independent methods reveal the enrichment of 6mA near and after transcription start sites with a periodic pattern and anti-correlation relationship with the positions of nucleosomes. The distribution pattern can be recapitulated by in vitro nucleosome assembly on native Tetrahymena genomic DNA but not on DNA without 6mA. Model DNA containing artificially installed 6mA resists nucleosome assembling compared to unmodified DNA in vitro. Computational simulation indicates that 6mA increases dsDNA rigidity, which disfavors nucleosome wrapping. Knockout of a potential 6mA methyltransferase leads to a transcriptome-wide change of gene expression. Conclusions These findings uncover a mechanism by which DNA 6mA assists to shape the nucleosome positioning and potentially affects gene expression. |
doi_str_mv | 10.1186/s13059-018-1573-3 |
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Recent studies revealed the presence of 6mA in more prevalent eukaryotes, even in vertebrates. However, functional characterizations have been limited. Results We use Tetrahymena thermophila as a model organism to examine the effects of 6mA on nucleosome positioning. Independent methods reveal the enrichment of 6mA near and after transcription start sites with a periodic pattern and anti-correlation relationship with the positions of nucleosomes. The distribution pattern can be recapitulated by in vitro nucleosome assembly on native Tetrahymena genomic DNA but not on DNA without 6mA. Model DNA containing artificially installed 6mA resists nucleosome assembling compared to unmodified DNA in vitro. Computational simulation indicates that 6mA increases dsDNA rigidity, which disfavors nucleosome wrapping. Knockout of a potential 6mA methyltransferase leads to a transcriptome-wide change of gene expression. Conclusions These findings uncover a mechanism by which DNA 6mA assists to shape the nucleosome positioning and potentially affects gene expression.</description><identifier>ISSN: 1474-760X</identifier><identifier>ISSN: 1474-7596</identifier><identifier>EISSN: 1474-760X</identifier><identifier>DOI: 10.1186/s13059-018-1573-3</identifier><identifier>PMID: 30454035</identifier><language>eng</language><publisher>London: BioMed Central</publisher><subject>Computer applications ; Deoxyribonucleic acid ; DNA ; DNA methylation ; Enzymes ; Epigenetics ; Eukaryotes ; Gene expression ; Genomes ; Integrated software ; Methyltransferase ; N6-methyladenosine ; Nucleosomes ; Organisms ; Prokaryotes ; Tetrahymena ; Transcription</subject><ispartof>Genome Biology, 2018-11, Vol.19 (1), p.200-200, Article 200</ispartof><rights>2018. 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>The Author(s). 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3843-88e9289d953a3b8174822f5cd9bf2a40a47473851195fbde71ab170723e98f5d3</citedby><cites>FETCH-LOGICAL-c3843-88e9289d953a3b8174822f5cd9bf2a40a47473851195fbde71ab170723e98f5d3</cites><orcidid>0000-0002-6797-9319</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/PMC6245762/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2207186475?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793</link.rule.ids></links><search><creatorcontrib>Luo, Guan-Zheng</creatorcontrib><creatorcontrib>Hao, Ziyang</creatorcontrib><creatorcontrib>Luo, Liangzhi</creatorcontrib><creatorcontrib>Shen, Mingren</creatorcontrib><creatorcontrib>Sparvoli, Daniela</creatorcontrib><creatorcontrib>Zheng, Yuqing</creatorcontrib><creatorcontrib>Zhang, Zijie</creatorcontrib><creatorcontrib>Weng, Xiaocheng</creatorcontrib><creatorcontrib>Chen, Kai</creatorcontrib><creatorcontrib>Cui, Qiang</creatorcontrib><creatorcontrib>Turkewitz, Aaron P.</creatorcontrib><creatorcontrib>He, Chuan</creatorcontrib><title>N6-methyldeoxyadenosine directs nucleosome positioning in Tetrahymena DNA</title><title>Genome Biology</title><description>Background N6-methyldeoxyadenosine (6mA or m6dA) was shown more than 40 years ago in simple eukaryotes. Recent studies revealed the presence of 6mA in more prevalent eukaryotes, even in vertebrates. However, functional characterizations have been limited. Results We use Tetrahymena thermophila as a model organism to examine the effects of 6mA on nucleosome positioning. Independent methods reveal the enrichment of 6mA near and after transcription start sites with a periodic pattern and anti-correlation relationship with the positions of nucleosomes. The distribution pattern can be recapitulated by in vitro nucleosome assembly on native Tetrahymena genomic DNA but not on DNA without 6mA. Model DNA containing artificially installed 6mA resists nucleosome assembling compared to unmodified DNA in vitro. Computational simulation indicates that 6mA increases dsDNA rigidity, which disfavors nucleosome wrapping. Knockout of a potential 6mA methyltransferase leads to a transcriptome-wide change of gene expression. 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Hao, Ziyang ; Luo, Liangzhi ; Shen, Mingren ; Sparvoli, Daniela ; Zheng, Yuqing ; Zhang, Zijie ; Weng, Xiaocheng ; Chen, Kai ; Cui, Qiang ; Turkewitz, Aaron P. ; He, Chuan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3843-88e9289d953a3b8174822f5cd9bf2a40a47473851195fbde71ab170723e98f5d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Computer applications</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>Enzymes</topic><topic>Epigenetics</topic><topic>Eukaryotes</topic><topic>Gene expression</topic><topic>Genomes</topic><topic>Integrated software</topic><topic>Methyltransferase</topic><topic>N6-methyladenosine</topic><topic>Nucleosomes</topic><topic>Organisms</topic><topic>Prokaryotes</topic><topic>Tetrahymena</topic><topic>Transcription</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Luo, Guan-Zheng</creatorcontrib><creatorcontrib>Hao, Ziyang</creatorcontrib><creatorcontrib>Luo, Liangzhi</creatorcontrib><creatorcontrib>Shen, Mingren</creatorcontrib><creatorcontrib>Sparvoli, Daniela</creatorcontrib><creatorcontrib>Zheng, Yuqing</creatorcontrib><creatorcontrib>Zhang, Zijie</creatorcontrib><creatorcontrib>Weng, Xiaocheng</creatorcontrib><creatorcontrib>Chen, Kai</creatorcontrib><creatorcontrib>Cui, Qiang</creatorcontrib><creatorcontrib>Turkewitz, Aaron P.</creatorcontrib><creatorcontrib>He, Chuan</creatorcontrib><collection>CrossRef</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)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: 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 (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database (Proquest) (PQ_SDU_P3)</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>Luo, Guan-Zheng</au><au>Hao, Ziyang</au><au>Luo, Liangzhi</au><au>Shen, Mingren</au><au>Sparvoli, Daniela</au><au>Zheng, Yuqing</au><au>Zhang, Zijie</au><au>Weng, Xiaocheng</au><au>Chen, Kai</au><au>Cui, Qiang</au><au>Turkewitz, Aaron P.</au><au>He, Chuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>N6-methyldeoxyadenosine directs nucleosome positioning in Tetrahymena DNA</atitle><jtitle>Genome Biology</jtitle><date>2018-11-19</date><risdate>2018</risdate><volume>19</volume><issue>1</issue><spage>200</spage><epage>200</epage><pages>200-200</pages><artnum>200</artnum><issn>1474-760X</issn><issn>1474-7596</issn><eissn>1474-760X</eissn><abstract>Background N6-methyldeoxyadenosine (6mA or m6dA) was shown more than 40 years ago in simple eukaryotes. Recent studies revealed the presence of 6mA in more prevalent eukaryotes, even in vertebrates. However, functional characterizations have been limited. Results We use Tetrahymena thermophila as a model organism to examine the effects of 6mA on nucleosome positioning. Independent methods reveal the enrichment of 6mA near and after transcription start sites with a periodic pattern and anti-correlation relationship with the positions of nucleosomes. The distribution pattern can be recapitulated by in vitro nucleosome assembly on native Tetrahymena genomic DNA but not on DNA without 6mA. Model DNA containing artificially installed 6mA resists nucleosome assembling compared to unmodified DNA in vitro. Computational simulation indicates that 6mA increases dsDNA rigidity, which disfavors nucleosome wrapping. Knockout of a potential 6mA methyltransferase leads to a transcriptome-wide change of gene expression. Conclusions These findings uncover a mechanism by which DNA 6mA assists to shape the nucleosome positioning and potentially affects gene expression.</abstract><cop>London</cop><pub>BioMed Central</pub><pmid>30454035</pmid><doi>10.1186/s13059-018-1573-3</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-6797-9319</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Computer applications Deoxyribonucleic acid DNA DNA methylation Enzymes Epigenetics Eukaryotes Gene expression Genomes Integrated software Methyltransferase N6-methyladenosine Nucleosomes Organisms Prokaryotes Tetrahymena Transcription |
title | N6-methyldeoxyadenosine directs nucleosome positioning in Tetrahymena DNA |
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