Methylated Cytosines Mutate to Transcription Factor Binding Sites that Drive Tetrapod Evolution.
Identifieur interne : 001409 ( PubMed/Curation ); précédent : 001408; suivant : 001410Methylated Cytosines Mutate to Transcription Factor Binding Sites that Drive Tetrapod Evolution.
Auteurs : Ximiao He [États-Unis] ; Desiree Tillo [États-Unis] ; Jeff Vierstra [États-Unis] ; Khund-Sayeed Syed [États-Unis] ; Callie Deng [États-Unis] ; G Jordan Ray [États-Unis] ; John Stamatoyannopoulos [États-Unis] ; Peter C. Fitzgerald [États-Unis] ; Charles Vinson [Israël]Source :
- Genome biology and evolution [ 1759-6653 ] ; 2015.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : 5-Methylcytosine, Cytosine, Transcription Factors.
- chemical , genetics : Dinucleoside Phosphates, Transcription Factors.
- Animals, Binding Sites, Biological Evolution, DNA Methylation, Humans, Mice, Oligonucleotide Array Sequence Analysis, Protein Binding.
Abstract
In mammals, the cytosine in CG dinucleotides is typically methylated producing 5-methylcytosine (5mC), a chemically less stable form of cytosine that can spontaneously deaminate to thymidine resulting in a T•G mismatched base pair. Unlike other eukaryotes that efficiently repair this mismatched base pair back to C•G, in mammals, 5mCG deamination is mutagenic, sometimes producing TG dinucleotides, explaining the depletion of CG dinucleotides in mammalian genomes. It was suggested that new TG dinucleotides generate genetic diversity that may be critical for evolutionary change. We tested this conjecture by examining the DNA sequence properties of regulatory sequences identified by DNase I hypersensitive sites (DHSs) in human and mouse genomes. We hypothesized that the new TG dinucleotides generate transcription factor binding sites (TFBS) that become tissue-specific DHSs (TS-DHSs). We find that 8-mers containing the CG dinucleotide are enriched in DHSs in both species. However, 8-mers containing a TG and no CG dinucleotide are preferentially enriched in TS-DHSs when compared with 8-mers with neither a TG nor a CG dinucleotide. The most enriched 8-mer with a TG and no CG dinucleotide in tissue-specific regulatory regions in both genomes is the AP-1 motif ( TG: A(C)/GT CA: N), and we find evidence that TG dinucleotides in the AP-1 motif arose from CG dinucleotides. Additional TS-DHS-enriched TFBS containing the TG/CA dinucleotide are the E-Box motif (G CA: GC TG: C), the NF-1 motif (GG CATG: CC), and the GR (glucocorticoid receptor) motif (G-A CATG: T-C). Our results support the suggestion that cytosine methylation is mutagenic in tetrapods producing TG dinucleotides that create TFBS that drive evolution.
DOI: 10.1093/gbe/evv205
PubMed: 26507798
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Fitzgerald</name><affiliation wicri:level="2"><nlm:affiliation>Genome Analysis Unit, Genetics Branch, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Genome Analysis Unit, Genetics Branch, National Cancer Institute, National Institutes of Health, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Vinson, Charles" sort="Vinson, Charles" uniqKey="Vinson C" first="Charles" last="Vinson">Charles Vinson</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland vinsonc@mail.nih.gov.</nlm:affiliation><country wicri:rule="url">Israël</country><wicri:regionArea>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda</wicri:regionArea></affiliation></author></analytic><series><title level="j">Genome biology and evolution</title><idno type="eISSN">1759-6653</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>5-Methylcytosine (chemistry)</term><term>Animals</term><term>Binding Sites</term><term>Biological Evolution</term><term>Cytosine (chemistry)</term><term>DNA Methylation</term><term>Dinucleoside Phosphates (genetics)</term><term>Humans</term><term>Mice</term><term>Oligonucleotide Array Sequence Analysis</term><term>Protein Binding</term><term>Transcription Factors (chemistry)</term><term>Transcription Factors (genetics)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>5-Méthyl-cytosine ()</term><term>Animaux</term><term>Cytosine ()</term><term>Dinucléoside phosphates (génétique)</term><term>Facteurs de transcription ()</term><term>Facteurs de transcription (génétique)</term><term>Humains</term><term>Liaison aux protéines</term><term>Méthylation de l'ADN</term><term>Sites de fixation</term><term>Souris</term><term>Séquençage par oligonucléotides en batterie</term><term>Évolution biologique</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>5-Methylcytosine</term><term>Cytosine</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Dinucleoside Phosphates</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Dinucléoside phosphates</term><term>Facteurs de transcription</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Binding Sites</term><term>Biological Evolution</term><term>DNA Methylation</term><term>Humans</term><term>Mice</term><term>Oligonucleotide Array Sequence Analysis</term><term>Protein Binding</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>5-Méthyl-cytosine</term><term>Animaux</term><term>Cytosine</term><term>Facteurs de transcription</term><term>Humains</term><term>Liaison aux protéines</term><term>Méthylation de l'ADN</term><term>Sites de fixation</term><term>Souris</term><term>Séquençage par oligonucléotides en batterie</term><term>Évolution biologique</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In mammals, the cytosine in CG dinucleotides is typically methylated producing 5-methylcytosine (5mC), a chemically less stable form of cytosine that can spontaneously deaminate to thymidine resulting in a T•G mismatched base pair. Unlike other eukaryotes that efficiently repair this mismatched base pair back to C•G, in mammals, 5mCG deamination is mutagenic, sometimes producing TG dinucleotides, explaining the depletion of CG dinucleotides in mammalian genomes. It was suggested that new TG dinucleotides generate genetic diversity that may be critical for evolutionary change. We tested this conjecture by examining the DNA sequence properties of regulatory sequences identified by DNase I hypersensitive sites (DHSs) in human and mouse genomes. We hypothesized that the new TG dinucleotides generate transcription factor binding sites (TFBS) that become tissue-specific DHSs (TS-DHSs). We find that 8-mers containing the CG dinucleotide are enriched in DHSs in both species. However, 8-mers containing a TG and no CG dinucleotide are preferentially enriched in TS-DHSs when compared with 8-mers with neither a TG nor a CG dinucleotide. The most enriched 8-mer with a TG and no CG dinucleotide in tissue-specific regulatory regions in both genomes is the AP-1 motif ( TG: A(C)/GT CA: N), and we find evidence that TG dinucleotides in the AP-1 motif arose from CG dinucleotides. Additional TS-DHS-enriched TFBS containing the TG/CA dinucleotide are the E-Box motif (G CA: GC TG: C), the NF-1 motif (GG CATG: CC), and the GR (glucocorticoid receptor) motif (G-A CATG: T-C). Our results support the suggestion that cytosine methylation is mutagenic in tetrapods producing TG dinucleotides that create TFBS that drive evolution. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26507798</PMID><DateCompleted><Year>2016</Year><Month>09</Month><Day>05</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1759-6653</ISSN><JournalIssue CitedMedium="Internet"><Volume>7</Volume><Issue>11</Issue><PubDate><Year>2015</Year><Month>Oct</Month><Day>27</Day></PubDate></JournalIssue><Title>Genome biology and evolution</Title><ISOAbbreviation>Genome Biol Evol</ISOAbbreviation></Journal><ArticleTitle>Methylated Cytosines Mutate to Transcription Factor Binding Sites that Drive Tetrapod Evolution.</ArticleTitle><Pagination><MedlinePgn>3155-69</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/gbe/evv205</ELocationID><Abstract><AbstractText>In mammals, the cytosine in CG dinucleotides is typically methylated producing 5-methylcytosine (5mC), a chemically less stable form of cytosine that can spontaneously deaminate to thymidine resulting in a T•G mismatched base pair. Unlike other eukaryotes that efficiently repair this mismatched base pair back to C•G, in mammals, 5mCG deamination is mutagenic, sometimes producing TG dinucleotides, explaining the depletion of CG dinucleotides in mammalian genomes. It was suggested that new TG dinucleotides generate genetic diversity that may be critical for evolutionary change. We tested this conjecture by examining the DNA sequence properties of regulatory sequences identified by DNase I hypersensitive sites (DHSs) in human and mouse genomes. We hypothesized that the new TG dinucleotides generate transcription factor binding sites (TFBS) that become tissue-specific DHSs (TS-DHSs). We find that 8-mers containing the CG dinucleotide are enriched in DHSs in both species. However, 8-mers containing a TG and no CG dinucleotide are preferentially enriched in TS-DHSs when compared with 8-mers with neither a TG nor a CG dinucleotide. The most enriched 8-mer with a TG and no CG dinucleotide in tissue-specific regulatory regions in both genomes is the AP-1 motif ( TG: A(C)/GT CA: N), and we find evidence that TG dinucleotides in the AP-1 motif arose from CG dinucleotides. Additional TS-DHS-enriched TFBS containing the TG/CA dinucleotide are the E-Box motif (G CA: GC TG: C), the NF-1 motif (GG CATG: CC), and the GR (glucocorticoid receptor) motif (G-A CATG: T-C). Our results support the suggestion that cytosine methylation is mutagenic in tetrapods producing TG dinucleotides that create TFBS that drive evolution. </AbstractText><CopyrightInformation>Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution 2015. This work is written by US Government employees and is in the public domain in the US.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>He</LastName><ForeName>Ximiao</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tillo</LastName><ForeName>Desiree</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vierstra</LastName><ForeName>Jeff</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Genome Sciences, University of Washington.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Syed</LastName><ForeName>Khund-Sayeed</ForeName><Initials>KS</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Deng</LastName><ForeName>Callie</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ray</LastName><ForeName>G Jordan</ForeName><Initials>GJ</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Stamatoyannopoulos</LastName><ForeName>John</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Genome Sciences, University of Washington.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>FitzGerald</LastName><ForeName>Peter C</ForeName><Initials>PC</Initials><AffiliationInfo><Affiliation>Genome Analysis Unit, Genetics Branch, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vinson</LastName><ForeName>Charles</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratory of Metabolism, National Cancer Institute, National Institutes of Health, Bethesda, Maryland vinsonc@mail.nih.gov.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Agency>Intramural NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052060">Research Support, N.I.H., Intramural</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>10</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Genome Biol Evol</MedlineTA><NlmUniqueID>101509707</NlmUniqueID><ISSNLinking>1759-6653</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D015226">Dinucleoside Phosphates</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>2382-65-2</RegistryNumber><NameOfSubstance UI="C015772">cytidylyl-3'-5'-guanosine</NameOfSubstance></Chemical><Chemical><RegistryNumber>6R795CQT4H</RegistryNumber><NameOfSubstance UI="D044503">5-Methylcytosine</NameOfSubstance></Chemical><Chemical><RegistryNumber>8J337D1HZY</RegistryNumber><NameOfSubstance UI="D003596">Cytosine</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D044503" MajorTopicYN="N">5-Methylcytosine</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001665" MajorTopicYN="N">Binding Sites</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005075" MajorTopicYN="Y">Biological Evolution</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D003596" MajorTopicYN="N">Cytosine</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019175" MajorTopicYN="Y">DNA Methylation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015226" MajorTopicYN="N">Dinucleoside Phosphates</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020411" MajorTopicYN="N">Oligonucleotide Array Sequence Analysis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">AP-1</Keyword><Keyword MajorTopicYN="N">CG methylation</Keyword><Keyword MajorTopicYN="N">TFBS</Keyword><Keyword MajorTopicYN="N">TG dinucleotide</Keyword><Keyword 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