Nonlinear sequence similarity between the Xist and Rsx long noncoding RNAs suggests shared functions of tandem repeat domains.
Identifieur interne : 002220 ( Ncbi/Merge ); précédent : 002219; suivant : 002221Nonlinear sequence similarity between the Xist and Rsx long noncoding RNAs suggests shared functions of tandem repeat domains.
Auteurs : Daniel Sprague [États-Unis] ; Shafagh A. Waters [Australie] ; Jessime M. Kirk [États-Unis] ; Jeremy R. Wang [États-Unis] ; Paul B. Samollow [États-Unis] ; Paul D. Waters [Australie] ; J Mauro Calabrese [États-Unis]Source :
- RNA (New York, N.Y.) [ 1469-9001 ] ; 2019.
Descripteurs français
- KwdFr :
- ARN long non codant (), ARN long non codant (génétique), Analyse de regroupements, Animaux, Domaines protéiques, Humains, Inactivation du chromosome X, Marsupialia (génétique), Marsupialia (métabolisme), Protéines du groupe Polycomb (métabolisme), Similitude de séquences d'acides nucléiques, Séquences répétées en tandem.
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : RNA, Long Noncoding.
- chemical , genetics : RNA, Long Noncoding.
- chemical , metabolism : Polycomb-Group Proteins.
- genetics : Marsupialia.
- metabolism : Marsupialia.
- Animals, Cluster Analysis, Humans, Protein Domains, Sequence Homology, Nucleic Acid, Tandem Repeat Sequences, X Chromosome Inactivation.
Abstract
The marsupial inactive X chromosome expresses a long noncoding RNA (lncRNA) called Rsx that has been proposed to be the functional analog of eutherian Xist Despite the possibility that Xist and Rsx encode related functions, the two lncRNAs harbor no linear sequence similarity. However, both lncRNAs harbor domains of tandemly repeated sequence. In Xist, these repeat domains are known to be critical for function. Using k-mer based comparison, we show that the repeat domains of Xist and Rsx unexpectedly partition into two major clusters that each harbor substantial levels of nonlinear sequence similarity. Xist Repeats B, C, and D were most similar to each other and to Rsx Repeat 1, whereas Xist Repeats A and E were most similar to each other and to Rsx Repeats 2, 3, and 4. Similarities at the level of k-mers corresponded to domain-specific enrichment of protein-binding motifs. Within individual domains, protein-binding motifs were often enriched to extreme levels. Our data support the hypothesis that Xist and Rsx encode similar functions through different spatial arrangements of functionally analogous protein-binding domains. We propose that the two clusters of repeat domains in Xist and Rsx function in part to cooperatively recruit PRC1 and PRC2 to chromatin. The physical manner in which these domains engage with protein cofactors may be just as critical to the function of the domains as the protein cofactors themselves. The general approaches we outline in this report should prove useful in the study of any set of RNAs.
DOI: 10.1261/rna.069815.118
PubMed: 31097619
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Waters</name><affiliation wicri:level="1"><nlm:affiliation>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, New South Wales 2052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, New South Wales 2052</wicri:regionArea><wicri:noRegion>New South Wales 2052</wicri:noRegion></affiliation></author><author><name sortKey="Calabrese, J Mauro" sort="Calabrese, J Mauro" uniqKey="Calabrese J" first="J Mauro" last="Calabrese">J Mauro Calabrese</name><affiliation wicri:level="4"><nlm:affiliation>Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599</wicri:regionArea><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName><placeName><settlement type="city">Chapel Hill (Caroline du Nord)</settlement><region type="state">Caroline du Nord</region></placeName></affiliation></author></analytic><series><title level="j">RNA (New York, N.Y.)</title><idno type="eISSN">1469-9001</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Cluster Analysis</term><term>Humans</term><term>Marsupialia (genetics)</term><term>Marsupialia (metabolism)</term><term>Polycomb-Group Proteins (metabolism)</term><term>Protein Domains</term><term>RNA, Long Noncoding (chemistry)</term><term>RNA, Long Noncoding (genetics)</term><term>Sequence Homology, Nucleic Acid</term><term>Tandem Repeat Sequences</term><term>X Chromosome Inactivation</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>ARN long non codant ()</term><term>ARN long non codant (génétique)</term><term>Analyse de regroupements</term><term>Animaux</term><term>Domaines protéiques</term><term>Humains</term><term>Inactivation du chromosome X</term><term>Marsupialia (génétique)</term><term>Marsupialia (métabolisme)</term><term>Protéines du groupe Polycomb (métabolisme)</term><term>Similitude de séquences d'acides nucléiques</term><term>Séquences répétées en tandem</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>RNA, Long Noncoding</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>RNA, Long Noncoding</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Polycomb-Group Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Marsupialia</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>ARN long non codant</term><term>Marsupialia</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Marsupialia</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Marsupialia</term><term>Protéines du groupe Polycomb</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cluster Analysis</term><term>Humans</term><term>Protein Domains</term><term>Sequence Homology, Nucleic Acid</term><term>Tandem Repeat Sequences</term><term>X Chromosome Inactivation</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>ARN long non codant</term><term>Analyse de regroupements</term><term>Animaux</term><term>Domaines protéiques</term><term>Humains</term><term>Inactivation du chromosome X</term><term>Similitude de séquences d'acides nucléiques</term><term>Séquences répétées en tandem</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The marsupial inactive X chromosome expresses a long noncoding RNA (lncRNA) called <i>Rsx</i> that has been proposed to be the functional analog of eutherian <i>Xist</i> Despite the possibility that <i>Xist</i> and <i>Rsx</i> encode related functions, the two lncRNAs harbor no linear sequence similarity. However, both lncRNAs harbor domains of tandemly repeated sequence. In <i>Xist</i>, these repeat domains are known to be critical for function. Using <i>k</i>-mer based comparison, we show that the repeat domains of <i>Xist</i> and <i>Rsx</i> unexpectedly partition into two major clusters that each harbor substantial levels of nonlinear sequence similarity. <i>Xist</i> Repeats B, C, and D were most similar to each other and to <i>Rsx</i> Repeat 1, whereas <i>Xist</i> Repeats A and E were most similar to each other and to <i>Rsx</i> Repeats 2, 3, and 4. Similarities at the level of <i>k</i>-mers corresponded to domain-specific enrichment of protein-binding motifs. Within individual domains, protein-binding motifs were often enriched to extreme levels. Our data support the hypothesis that <i>Xist</i> and <i>Rsx</i> encode similar functions through different spatial arrangements of functionally analogous protein-binding domains. We propose that the two clusters of repeat domains in <i>Xist</i> and <i>Rsx</i> function in part to cooperatively recruit PRC1 and PRC2 to chromatin. The physical manner in which these domains engage with protein cofactors may be just as critical to the function of the domains as the protein cofactors themselves. The general approaches we outline in this report should prove useful in the study of any set of RNAs.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31097619</PMID><DateCompleted><Year>2019</Year><Month>11</Month><Day>04</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-9001</ISSN><JournalIssue CitedMedium="Internet"><Volume>25</Volume><Issue>8</Issue><PubDate><Year>2019</Year><Month>08</Month></PubDate></JournalIssue><Title>RNA (New York, N.Y.)</Title><ISOAbbreviation>RNA</ISOAbbreviation></Journal><ArticleTitle>Nonlinear sequence similarity between the <i>Xist</i> and <i>Rsx</i> long noncoding RNAs suggests shared functions of tandem repeat domains.</ArticleTitle><Pagination><MedlinePgn>1004-1019</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1261/rna.069815.118</ELocationID><Abstract><AbstractText>The marsupial inactive X chromosome expresses a long noncoding RNA (lncRNA) called <i>Rsx</i> that has been proposed to be the functional analog of eutherian <i>Xist</i> Despite the possibility that <i>Xist</i> and <i>Rsx</i> encode related functions, the two lncRNAs harbor no linear sequence similarity. However, both lncRNAs harbor domains of tandemly repeated sequence. In <i>Xist</i>, these repeat domains are known to be critical for function. Using <i>k</i>-mer based comparison, we show that the repeat domains of <i>Xist</i> and <i>Rsx</i> unexpectedly partition into two major clusters that each harbor substantial levels of nonlinear sequence similarity. <i>Xist</i> Repeats B, C, and D were most similar to each other and to <i>Rsx</i> Repeat 1, whereas <i>Xist</i> Repeats A and E were most similar to each other and to <i>Rsx</i> Repeats 2, 3, and 4. Similarities at the level of <i>k</i>-mers corresponded to domain-specific enrichment of protein-binding motifs. Within individual domains, protein-binding motifs were often enriched to extreme levels. Our data support the hypothesis that <i>Xist</i> and <i>Rsx</i> encode similar functions through different spatial arrangements of functionally analogous protein-binding domains. We propose that the two clusters of repeat domains in <i>Xist</i> and <i>Rsx</i> function in part to cooperatively recruit PRC1 and PRC2 to chromatin. The physical manner in which these domains engage with protein cofactors may be just as critical to the function of the domains as the protein cofactors themselves. The general approaches we outline in this report should prove useful in the study of any set of RNAs.</AbstractText><CopyrightInformation>© 2019 Sprague et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Sprague</LastName><ForeName>Daniel</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Curriculum in Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Waters</LastName><ForeName>Shafagh A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, New South Wales 2052, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Women's and Children's Health, Faculty of Medicine, University of New South Wales, Sydney, New South Wales 2052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kirk</LastName><ForeName>Jessime M</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jeremy R</ForeName><Initials>JR</Initials><AffiliationInfo><Affiliation>Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Samollow</LastName><ForeName>Paul B</ForeName><Initials>PB</Initials><AffiliationInfo><Affiliation>Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas 77843, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Waters</LastName><ForeName>Paul D</ForeName><Initials>PD</Initials><AffiliationInfo><Affiliation>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, New South Wales 2052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Calabrese</LastName><ForeName>J Mauro</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 GM121806</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D003160">Comparative Study</PublicationType><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>05</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>RNA</MedlineTA><NlmUniqueID>9509184</NlmUniqueID><ISSNLinking>1355-8382</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D063146">Polycomb-Group Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D062085">RNA, Long Noncoding</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016000" MajorTopicYN="N">Cluster Analysis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008394" MajorTopicYN="N">Marsupialia</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D063146" MajorTopicYN="N">Polycomb-Group Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D062085" MajorTopicYN="N">RNA, Long Noncoding</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012689" MajorTopicYN="N">Sequence Homology, Nucleic Acid</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020080" MajorTopicYN="N">Tandem Repeat 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