The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway
The exosome and its nuclear specific subunit Rrp6 form a 3'-5' exonuclease complex that regulates diverse aspects of RNA biology including 3' end processing and degradation of a variety of noncoding RNAs (ncRNAs) and unstable transcripts. Known targets of the nuclear exosome include s...
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| creator | Fox, Melanie J Gao, Hongyu Smith-Kinnaman, Whitney R Liu, Yunlong Mosley, Amber L |
| description | The exosome and its nuclear specific subunit Rrp6 form a 3'-5' exonuclease complex that regulates diverse aspects of RNA biology including 3' end processing and degradation of a variety of noncoding RNAs (ncRNAs) and unstable transcripts. Known targets of the nuclear exosome include short ( |
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Known targets of the nuclear exosome include short (<1000 bp) RNAPII transcripts such as small noncoding RNAs (snRNAs), cryptic unstable transcripts (CUTs), and some stable unannotated transcripts (SUTs) that are terminated by an Nrd1, Nab3, and Sen1 (NNS) dependent mechanism. NNS-dependent termination is coupled to RNA 3' end processing and/or degradation by the Rrp6/exosome in yeast. Recent work suggests Nrd1 is necessary for transcriptome surveillance, regulating promoter directionality and suppressing antisense transcription independently of, or prior to, Rrp6 activity. It remains unclear whether Rrp6 is directly involved in termination; however, Rrp6 has been implicated in the 3' end processing and degradation of ncRNA transcripts including CUTs. To determine the role of Rrp6 in NNS termination globally, we performed RNA sequencing (RNA-Seq) on total RNA and perform ChIP-exo analysis of RNA Polymerase II (RNAPII) localization. Deletion of RRP6 promotes hyper-elongation of multiple NNS-dependent transcripts resulting from both improperly processed 3' RNA ends and faulty transcript termination at specific target genes. The defects in RNAPII termination cause transcriptome-wide changes in mRNA expression through transcription interference and/or antisense repression, similar to previously reported effects of depleting Nrd1 from the nucleus. Elongated transcripts were identified within all classes of known NNS targets with the largest changes in transcription termination occurring at CUTs. Interestingly, the extended transcripts that we have detected in our studies show remarkable similarity to Nrd1-unterminated transcripts at many locations, suggesting that Rrp6 acts with the NNS complex globally to promote transcription termination in addition to 3' end RNA processing and/or degradation at specific targets.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1004999</identifier><identifier>PMID: 25680078</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>DNA Helicases - genetics ; Exosome Multienzyme Ribonuclease Complex - genetics ; Exosomes - genetics ; Exosomes - metabolism ; Gene expression ; Gene Expression Regulation, Fungal ; Identification and classification ; Methods ; Nuclear Proteins - genetics ; Nuclear Proteins - metabolism ; Physiological aspects ; Proteins ; RNA Helicases - genetics ; RNA Polymerase II - genetics ; RNA polymerases ; RNA sequencing ; RNA, Untranslated - genetics ; RNA-Binding Proteins - genetics ; RNA-Binding Proteins - metabolism ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Studies ; Surveillance ; Transcription, Genetic ; Transcriptome - genetics ; Yeast</subject><ispartof>PLoS genetics, 2015-02, Vol.11 (2), p.e1004999-e1004999</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Fox et al 2015 Fox et al</rights><rights>2015 Public Library of Science. 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: Fox MJ, Gao H, Smith-Kinnaman WR, Liu Y, Mosley AL (2015) The Exosome Component Rrp6 Is Required for RNA Polymerase II Termination at Specific Targets of the Nrd1-Nab3 Pathway. PLoS Genet 11(2): e1004999. doi:10.1371/journal.pgen.1004999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c768t-7893813751a95b2876e9bdf094278b93a91648ac3dc0fd81d64f765c988495803</citedby><cites>FETCH-LOGICAL-c768t-7893813751a95b2876e9bdf094278b93a91648ac3dc0fd81d64f765c988495803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4378619/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4378619/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2104,2930,23873,27931,27932,53798,53800</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25680078$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Corden, Jeffry</contributor><creatorcontrib>Fox, Melanie J</creatorcontrib><creatorcontrib>Gao, Hongyu</creatorcontrib><creatorcontrib>Smith-Kinnaman, Whitney R</creatorcontrib><creatorcontrib>Liu, Yunlong</creatorcontrib><creatorcontrib>Mosley, Amber L</creatorcontrib><title>The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The exosome and its nuclear specific subunit Rrp6 form a 3'-5' exonuclease complex that regulates diverse aspects of RNA biology including 3' end processing and degradation of a variety of noncoding RNAs (ncRNAs) and unstable transcripts. Known targets of the nuclear exosome include short (<1000 bp) RNAPII transcripts such as small noncoding RNAs (snRNAs), cryptic unstable transcripts (CUTs), and some stable unannotated transcripts (SUTs) that are terminated by an Nrd1, Nab3, and Sen1 (NNS) dependent mechanism. NNS-dependent termination is coupled to RNA 3' end processing and/or degradation by the Rrp6/exosome in yeast. Recent work suggests Nrd1 is necessary for transcriptome surveillance, regulating promoter directionality and suppressing antisense transcription independently of, or prior to, Rrp6 activity. It remains unclear whether Rrp6 is directly involved in termination; however, Rrp6 has been implicated in the 3' end processing and degradation of ncRNA transcripts including CUTs. To determine the role of Rrp6 in NNS termination globally, we performed RNA sequencing (RNA-Seq) on total RNA and perform ChIP-exo analysis of RNA Polymerase II (RNAPII) localization. Deletion of RRP6 promotes hyper-elongation of multiple NNS-dependent transcripts resulting from both improperly processed 3' RNA ends and faulty transcript termination at specific target genes. The defects in RNAPII termination cause transcriptome-wide changes in mRNA expression through transcription interference and/or antisense repression, similar to previously reported effects of depleting Nrd1 from the nucleus. Elongated transcripts were identified within all classes of known NNS targets with the largest changes in transcription termination occurring at CUTs. Interestingly, the extended transcripts that we have detected in our studies show remarkable similarity to Nrd1-unterminated transcripts at many locations, suggesting that Rrp6 acts with the NNS complex globally to promote transcription termination in addition to 3' end RNA processing and/or degradation at specific targets.</description><subject>DNA Helicases - genetics</subject><subject>Exosome Multienzyme Ribonuclease Complex - genetics</subject><subject>Exosomes - genetics</subject><subject>Exosomes - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Identification and classification</subject><subject>Methods</subject><subject>Nuclear Proteins - genetics</subject><subject>Nuclear Proteins - metabolism</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>RNA Helicases - genetics</subject><subject>RNA Polymerase II - genetics</subject><subject>RNA polymerases</subject><subject>RNA sequencing</subject><subject>RNA, Untranslated - genetics</subject><subject>RNA-Binding Proteins - genetics</subject><subject>RNA-Binding Proteins - metabolism</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Studies</subject><subject>Surveillance</subject><subject>Transcription, Genetic</subject><subject>Transcriptome - genetics</subject><subject>Yeast</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7rr6D0QDgujFjEnz0eRGGBY_BpZZGFdvQ5qmMxnappukuvPvTZ3ZZQpeKLlISJ73zck5OVn2EsE5wgX6sHOD71Qz7zemmyMIiRDiUXaOKMWzgkDy-GR9lj0LYQchplwUT7OznDIOYcHPs-Fma4C5c8G1BmjX9q4zXQRr3zNgA_DmdrDeVKB2HqxXC9C7Zt8ar4IByyWIxre2U9G6DqgIQm-0ra0GUfmNiQG4GsTkv_IVmq1UiUGv4vaX2j_PntSqCebFcb7Ivn_-dHP5dXZ1_WV5ubia6YLxOCu4wDw9liIlaJnzghlRVjUUJC94KbASiBGuNK40rCuOKkbqglEtOCeCcogvstcH375xQR4zFiRinCLMOROJWB6Iyqmd7L1tld9Lp6z8s-H8RiofrW6MLHmVM5XTWrGS0LwWBWSF4hTriqUoTfL6eLxtKFtT6ZRIr5qJ6fSks1u5cT8lwQVnaAzm3dHAu9vBhChbG7RpGtUZN4xxU0pzkmOU0DcHdKNSaLarXXLUIy4XBHFMMM5JouZ_odKoTGt1KnVt0_5E8H4iSEw0d3GjhhDk8tv6P9jVv7PXP6bs2xN2a1QTt8E1w_jLwhQkB1B7F4I39UOqEZRjj9xXXI49Io89kmSvTsv0ILpvCvwbBsoKKQ</recordid><startdate>20150201</startdate><enddate>20150201</enddate><creator>Fox, Melanie J</creator><creator>Gao, Hongyu</creator><creator>Smith-Kinnaman, Whitney R</creator><creator>Liu, Yunlong</creator><creator>Mosley, Amber 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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150201</creationdate><title>The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway</title><author>Fox, Melanie J ; Gao, Hongyu ; Smith-Kinnaman, Whitney R ; Liu, Yunlong ; Mosley, Amber L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c768t-7893813751a95b2876e9bdf094278b93a91648ac3dc0fd81d64f765c988495803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>DNA Helicases - genetics</topic><topic>Exosome Multienzyme Ribonuclease Complex - genetics</topic><topic>Exosomes - genetics</topic><topic>Exosomes - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Identification and classification</topic><topic>Methods</topic><topic>Nuclear Proteins - genetics</topic><topic>Nuclear Proteins - metabolism</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>RNA Helicases - genetics</topic><topic>RNA Polymerase II - genetics</topic><topic>RNA polymerases</topic><topic>RNA sequencing</topic><topic>RNA, Untranslated - genetics</topic><topic>RNA-Binding Proteins - genetics</topic><topic>RNA-Binding Proteins - metabolism</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Studies</topic><topic>Surveillance</topic><topic>Transcription, Genetic</topic><topic>Transcriptome - genetics</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fox, Melanie J</creatorcontrib><creatorcontrib>Gao, Hongyu</creatorcontrib><creatorcontrib>Smith-Kinnaman, Whitney R</creatorcontrib><creatorcontrib>Liu, Yunlong</creatorcontrib><creatorcontrib>Mosley, Amber L</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: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fox, Melanie J</au><au>Gao, Hongyu</au><au>Smith-Kinnaman, Whitney R</au><au>Liu, Yunlong</au><au>Mosley, Amber L</au><au>Corden, Jeffry</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-02-01</date><risdate>2015</risdate><volume>11</volume><issue>2</issue><spage>e1004999</spage><epage>e1004999</epage><pages>e1004999-e1004999</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The exosome and its nuclear specific subunit Rrp6 form a 3'-5' exonuclease complex that regulates diverse aspects of RNA biology including 3' end processing and degradation of a variety of noncoding RNAs (ncRNAs) and unstable transcripts. Known targets of the nuclear exosome include short (<1000 bp) RNAPII transcripts such as small noncoding RNAs (snRNAs), cryptic unstable transcripts (CUTs), and some stable unannotated transcripts (SUTs) that are terminated by an Nrd1, Nab3, and Sen1 (NNS) dependent mechanism. NNS-dependent termination is coupled to RNA 3' end processing and/or degradation by the Rrp6/exosome in yeast. Recent work suggests Nrd1 is necessary for transcriptome surveillance, regulating promoter directionality and suppressing antisense transcription independently of, or prior to, Rrp6 activity. It remains unclear whether Rrp6 is directly involved in termination; however, Rrp6 has been implicated in the 3' end processing and degradation of ncRNA transcripts including CUTs. To determine the role of Rrp6 in NNS termination globally, we performed RNA sequencing (RNA-Seq) on total RNA and perform ChIP-exo analysis of RNA Polymerase II (RNAPII) localization. Deletion of RRP6 promotes hyper-elongation of multiple NNS-dependent transcripts resulting from both improperly processed 3' RNA ends and faulty transcript termination at specific target genes. The defects in RNAPII termination cause transcriptome-wide changes in mRNA expression through transcription interference and/or antisense repression, similar to previously reported effects of depleting Nrd1 from the nucleus. Elongated transcripts were identified within all classes of known NNS targets with the largest changes in transcription termination occurring at CUTs. Interestingly, the extended transcripts that we have detected in our studies show remarkable similarity to Nrd1-unterminated transcripts at many locations, suggesting that Rrp6 acts with the NNS complex globally to promote transcription termination in addition to 3' end RNA processing and/or degradation at specific targets.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25680078</pmid><doi>10.1371/journal.pgen.1004999</doi><oa>free_for_read</oa></addata></record> |
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| subjects | DNA Helicases - genetics Exosome Multienzyme Ribonuclease Complex - genetics Exosomes - genetics Exosomes - metabolism Gene expression Gene Expression Regulation, Fungal Identification and classification Methods Nuclear Proteins - genetics Nuclear Proteins - metabolism Physiological aspects Proteins RNA Helicases - genetics RNA Polymerase II - genetics RNA polymerases RNA sequencing RNA, Untranslated - genetics RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Studies Surveillance Transcription, Genetic Transcriptome - genetics Yeast |
| title | The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway |
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