Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment.
Identifieur interne : 000C08 ( PubMed/Corpus ); précédent : 000C07; suivant : 000C09Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment.
Auteurs : Justin J-L Wong ; Dadi Gao ; Trung V. Nguyen ; Chau-To Kwok ; Michelle Van Geldermalsen ; Rob Middleton ; Natalia Pinello ; Annora Thoeng ; Rajini Nagarajah ; Jeff Holst ; William Ritchie ; John E J. RaskoSource :
- Nature communications [ 2041-1723 ] ; 2017.
Abstract
While intron retention (IR) is considered a widely conserved and distinct mechanism of gene expression control, its regulation is poorly understood. Here we show that DNA methylation directly regulates IR. We also find reduced occupancy of MeCP2 near the splice junctions of retained introns, mirroring the reduced DNA methylation at these sites. Accordingly, MeCP2 depletion in tissues and cells enhances IR. By analysing the MeCP2 interactome using mass spectrometry and RNA co-precipitation, we demonstrate that decreased MeCP2 binding near splice junctions facilitates IR via reduced recruitment of splicing factors, including Tra2b, and increased RNA polymerase II stalling. These results suggest an association between IR and a slower rate of transcription elongation, which reflects inefficient splicing factor recruitment. In summary, our results reinforce the interdependency between alternative splicing involving IR and epigenetic controls of gene expression.
DOI: 10.1038/ncomms15134
PubMed: 28480880
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pubmed:28480880Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment.</title><author><name sortKey="Wong, Justin J L" sort="Wong, Justin J L" uniqKey="Wong J" first="Justin J-L" last="Wong">Justin J-L Wong</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Gao, Dadi" sort="Gao, Dadi" uniqKey="Gao D" first="Dadi" last="Gao">Dadi Gao</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Nguyen, Trung V" sort="Nguyen, Trung V" uniqKey="Nguyen T" first="Trung V" last="Nguyen">Trung V. Nguyen</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Kwok, Chau To" sort="Kwok, Chau To" uniqKey="Kwok C" first="Chau-To" last="Kwok">Chau-To Kwok</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Van Geldermalsen, Michelle" sort="Van Geldermalsen, Michelle" uniqKey="Van Geldermalsen M" first="Michelle" last="Van Geldermalsen">Michelle Van Geldermalsen</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Middleton, Rob" sort="Middleton, Rob" uniqKey="Middleton R" first="Rob" last="Middleton">Rob Middleton</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Pinello, Natalia" sort="Pinello, Natalia" uniqKey="Pinello N" first="Natalia" last="Pinello">Natalia Pinello</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Thoeng, Annora" sort="Thoeng, Annora" uniqKey="Thoeng A" first="Annora" last="Thoeng">Annora Thoeng</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Nagarajah, Rajini" sort="Nagarajah, Rajini" uniqKey="Nagarajah R" first="Rajini" last="Nagarajah">Rajini Nagarajah</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Holst, Jeff" sort="Holst, Jeff" uniqKey="Holst J" first="Jeff" last="Holst">Jeff Holst</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Ritchie, William" sort="Ritchie, William" uniqKey="Ritchie W" first="William" last="Ritchie">William Ritchie</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Rasko, John E J" sort="Rasko, John E J" uniqKey="Rasko J" first="John E J" last="Rasko">John E J. Rasko</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28480880</idno><idno type="pmid">28480880</idno><idno type="doi">10.1038/ncomms15134</idno><idno type="wicri:Area/PubMed/Corpus">000C08</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000C08</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment.</title><author><name sortKey="Wong, Justin J L" sort="Wong, Justin J L" uniqKey="Wong J" first="Justin J-L" last="Wong">Justin J-L Wong</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Gao, Dadi" sort="Gao, Dadi" uniqKey="Gao D" first="Dadi" last="Gao">Dadi Gao</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Nguyen, Trung V" sort="Nguyen, Trung V" uniqKey="Nguyen T" first="Trung V" last="Nguyen">Trung V. Nguyen</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Kwok, Chau To" sort="Kwok, Chau To" uniqKey="Kwok C" first="Chau-To" last="Kwok">Chau-To Kwok</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Van Geldermalsen, Michelle" sort="Van Geldermalsen, Michelle" uniqKey="Van Geldermalsen M" first="Michelle" last="Van Geldermalsen">Michelle Van Geldermalsen</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Middleton, Rob" sort="Middleton, Rob" uniqKey="Middleton R" first="Rob" last="Middleton">Rob Middleton</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Pinello, Natalia" sort="Pinello, Natalia" uniqKey="Pinello N" first="Natalia" last="Pinello">Natalia Pinello</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Thoeng, Annora" sort="Thoeng, Annora" uniqKey="Thoeng A" first="Annora" last="Thoeng">Annora Thoeng</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Nagarajah, Rajini" sort="Nagarajah, Rajini" uniqKey="Nagarajah R" first="Rajini" last="Nagarajah">Rajini Nagarajah</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Holst, Jeff" sort="Holst, Jeff" uniqKey="Holst J" first="Jeff" last="Holst">Jeff Holst</name><affiliation><nlm:affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Ritchie, William" sort="Ritchie, William" uniqKey="Ritchie W" first="William" last="Ritchie">William Ritchie</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Rasko, John E J" sort="Rasko, John E J" uniqKey="Rasko J" first="John E J" last="Rasko">John E J. Rasko</name><affiliation><nlm:affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Nature communications</title><idno type="eISSN">2041-1723</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">While intron retention (IR) is considered a widely conserved and distinct mechanism of gene expression control, its regulation is poorly understood. Here we show that DNA methylation directly regulates IR. We also find reduced occupancy of MeCP2 near the splice junctions of retained introns, mirroring the reduced DNA methylation at these sites. Accordingly, MeCP2 depletion in tissues and cells enhances IR. By analysing the MeCP2 interactome using mass spectrometry and RNA co-precipitation, we demonstrate that decreased MeCP2 binding near splice junctions facilitates IR via reduced recruitment of splicing factors, including Tra2b, and increased RNA polymerase II stalling. These results suggest an association between IR and a slower rate of transcription elongation, which reflects inefficient splicing factor recruitment. In summary, our results reinforce the interdependency between alternative splicing involving IR and epigenetic controls of gene expression.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">28480880</PMID><DateCreated><Year>2017</Year><Month>05</Month><Day>08</Day></DateCreated><DateRevised><Year>2017</Year><Month>05</Month><Day>25</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2041-1723</ISSN><JournalIssue CitedMedium="Internet"><Volume>8</Volume><PubDate><Year>2017</Year><Month>May</Month><Day>08</Day></PubDate></JournalIssue><Title>Nature communications</Title><ISOAbbreviation>Nat Commun</ISOAbbreviation></Journal><ArticleTitle>Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment.</ArticleTitle><Pagination><MedlinePgn>15134</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/ncomms15134</ELocationID><Abstract><AbstractText>While intron retention (IR) is considered a widely conserved and distinct mechanism of gene expression control, its regulation is poorly understood. Here we show that DNA methylation directly regulates IR. We also find reduced occupancy of MeCP2 near the splice junctions of retained introns, mirroring the reduced DNA methylation at these sites. Accordingly, MeCP2 depletion in tissues and cells enhances IR. By analysing the MeCP2 interactome using mass spectrometry and RNA co-precipitation, we demonstrate that decreased MeCP2 binding near splice junctions facilitates IR via reduced recruitment of splicing factors, including Tra2b, and increased RNA polymerase II stalling. These results suggest an association between IR and a slower rate of transcription elongation, which reflects inefficient splicing factor recruitment. In summary, our results reinforce the interdependency between alternative splicing involving IR and epigenetic controls of gene expression.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wong</LastName><ForeName>Justin J-L</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Gene Regulation in Cancer Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gao</LastName><ForeName>Dadi</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Bioinformatics Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nguyen</LastName><ForeName>Trung V</ForeName><Initials>TV</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Gene Regulation in Cancer Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kwok</LastName><ForeName>Chau-To</ForeName><Initials>CT</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Gene Regulation in Cancer Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Geldermalsen</LastName><ForeName>Michelle</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Origins of Cancer Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Middleton</LastName><ForeName>Rob</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Bioinformatics Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pinello</LastName><ForeName>Natalia</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Gene Regulation in Cancer Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thoeng</LastName><ForeName>Annora</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nagarajah</LastName><ForeName>Rajini</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Holst</LastName><ForeName>Jeff</ForeName><Initials>J</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0377-9318</Identifier><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Origins of Cancer Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ritchie</LastName><ForeName>William</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Bioinformatics Laboratory, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>CNRS, UMR 5203, 34094 Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rasko</LastName><ForeName>John E J</ForeName><Initials>JEJ</Initials><AffiliationInfo><Affiliation>Gene &Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Sydney Medical School, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Cell and Molecular Therapies, Royal Prince Alfred Hospital, Camperdown, New South Wales 2050, Australia.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2017</Year><Month>05</Month><Day>08</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Nat Commun</MedlineTA><NlmUniqueID>101528555</NlmUniqueID><ISSNLinking>2041-1723</ISSNLinking></MedlineJournalInfo><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Biosci Rep. 2011 Oct;31(5):333-43</RefSource><PMID Version="1">21070191</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Cancer Treat Rev. 2011 Apr;37(2):160-7</RefSource><PMID Version="1">20591575</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Trends Genet. 2012 Apr;28(4):147-54</RefSource><PMID Version="1">22397991</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Nat 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Version="1">23582333</PMID></CommentsCorrections></CommentsCorrectionsList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>09</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2017</Year><Month>03</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>5</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>5</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>5</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28480880</ArticleId><ArticleId IdType="pii">ncomms15134</ArticleId><ArticleId IdType="doi">10.1038/ncomms15134</ArticleId><ArticleId 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