Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes
Poly(UG) or 'pUG' dinucleotide repeats are highly abundant sequences in eukaryotic RNAs. In Caenorhabditis elegans, pUGs are added to RNA 3' ends to direct gene silencing within Mutator foci, a germ granule condensate. Here, we show that pUG RNAs efficiently self-assemble into gel con...
Gespeichert in:
| Veröffentlicht in: | Nucleic acids research 2024-11, Vol.52 (20), p.12582-12591 |
|---|---|
| Hauptverfasser: | , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 12591 |
|---|---|
| container_issue | 20 |
| container_start_page | 12582 |
| container_title | Nucleic acids research |
| container_volume | 52 |
| creator | Roschdi, Saeed Montemayor, Eric J Vivek, Rahul Bingman, Craig A Butcher, Samuel E |
| description | Poly(UG) or 'pUG' dinucleotide repeats are highly abundant sequences in eukaryotic RNAs. In Caenorhabditis elegans, pUGs are added to RNA 3' ends to direct gene silencing within Mutator foci, a germ granule condensate. Here, we show that pUG RNAs efficiently self-assemble into gel condensates through quadruplex (G4) interactions. Short pUG sequences form right-handed intermolecular G4s (pUG G4s), while longer pUGs form left-handed intramolecular G4s (pUG folds). We determined a 1.05 Å crystal structure of an intermolecular pUG G4, which reveals an eight stranded G4 dimer involving 48 nucleotides, 7 different G and U quartet conformations, 7 coordinated potassium ions, 8 sodium ions and a buried water molecule. A comparison of the intermolecular pUG G4 and intramolecular pUG fold structures provides insights into the molecular basis for G4 handedness and illustrates how a simple dinucleotide repeat sequence can form complex structures with diverse topologies. |
| doi_str_mv | 10.1093/nar/gkae870 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11551768</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3113752639</sourcerecordid><originalsourceid>FETCH-LOGICAL-c270t-14913286acf6cc340ecf544865d9602bfc9acaf1a1e990b4d2bc57cbae92d9a03</originalsourceid><addsrcrecordid>eNpVkE1LAzEQQIMoWqsn77JHRVaTTfYjJynFT4qC2nOYzc7qajZpk12x_95Ka9HTHObxZniEHDF6zqjkFxb8xesHYJHTLTJgPEtiIbNkmwwop2nMqCj2yH4I75QywVKxS_a45DkXuRiQ-2c0dQwhYFuaRQS2irSzFdoAXeNs5OqosR361hnUvQEfzZxZnExvTqOnh1E076Hy_czgF4YDslODCXi4nkMyvb56Gd_Gk8ebu_FoEuskp13MhGQ8KTLQdaY1FxR1nQpRZGklM5qUtZagoWbAUEpaiiopdZrrElAmlQTKh-Ry5Z31ZYuVRtt5MGrmmxb8Qjlo1P-Nbd7Uq_tUjKUpy7NiaThZG7yb9xg61TZBozFg0fVBccZ4nibZMtOQnK1Q7V0IHuvNHUbVT361zK_W-Zf08d_XNuxvb_4NVfGDwA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3113752639</pqid></control><display><type>article</type><title>Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Oxford Journals Open Access Collection</source><source>PubMed Central</source><source>Free Full-Text Journals in Chemistry</source><creator>Roschdi, Saeed ; Montemayor, Eric J ; Vivek, Rahul ; Bingman, Craig A ; Butcher, Samuel E</creator><creatorcontrib>Roschdi, Saeed ; Montemayor, Eric J ; Vivek, Rahul ; Bingman, Craig A ; Butcher, Samuel E</creatorcontrib><description>Poly(UG) or 'pUG' dinucleotide repeats are highly abundant sequences in eukaryotic RNAs. In Caenorhabditis elegans, pUGs are added to RNA 3' ends to direct gene silencing within Mutator foci, a germ granule condensate. Here, we show that pUG RNAs efficiently self-assemble into gel condensates through quadruplex (G4) interactions. Short pUG sequences form right-handed intermolecular G4s (pUG G4s), while longer pUGs form left-handed intramolecular G4s (pUG folds). We determined a 1.05 Å crystal structure of an intermolecular pUG G4, which reveals an eight stranded G4 dimer involving 48 nucleotides, 7 different G and U quartet conformations, 7 coordinated potassium ions, 8 sodium ions and a buried water molecule. A comparison of the intermolecular pUG G4 and intramolecular pUG fold structures provides insights into the molecular basis for G4 handedness and illustrates how a simple dinucleotide repeat sequence can form complex structures with diverse topologies.</description><identifier>ISSN: 0305-1048</identifier><identifier>ISSN: 1362-4962</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkae870</identifier><identifier>PMID: 39373474</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Animals ; Caenorhabditis elegans - genetics ; Crystallography, X-Ray ; G-Quadruplexes ; Models, Molecular ; Molecular and Structural Biology ; Nucleic Acid Conformation ; Poly U - chemistry ; Poly U - genetics ; RNA - chemistry ; RNA - genetics</subject><ispartof>Nucleic acids research, 2024-11, Vol.52 (20), p.12582-12591</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of Nucleic Acids Research. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c270t-14913286acf6cc340ecf544865d9602bfc9acaf1a1e990b4d2bc57cbae92d9a03</cites><orcidid>0000-0001-6343-6643</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/PMC11551768/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11551768/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39373474$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Roschdi, Saeed</creatorcontrib><creatorcontrib>Montemayor, Eric J</creatorcontrib><creatorcontrib>Vivek, Rahul</creatorcontrib><creatorcontrib>Bingman, Craig A</creatorcontrib><creatorcontrib>Butcher, Samuel E</creatorcontrib><title>Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Poly(UG) or 'pUG' dinucleotide repeats are highly abundant sequences in eukaryotic RNAs. In Caenorhabditis elegans, pUGs are added to RNA 3' ends to direct gene silencing within Mutator foci, a germ granule condensate. Here, we show that pUG RNAs efficiently self-assemble into gel condensates through quadruplex (G4) interactions. Short pUG sequences form right-handed intermolecular G4s (pUG G4s), while longer pUGs form left-handed intramolecular G4s (pUG folds). We determined a 1.05 Å crystal structure of an intermolecular pUG G4, which reveals an eight stranded G4 dimer involving 48 nucleotides, 7 different G and U quartet conformations, 7 coordinated potassium ions, 8 sodium ions and a buried water molecule. A comparison of the intermolecular pUG G4 and intramolecular pUG fold structures provides insights into the molecular basis for G4 handedness and illustrates how a simple dinucleotide repeat sequence can form complex structures with diverse topologies.</description><subject>Animals</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Crystallography, X-Ray</subject><subject>G-Quadruplexes</subject><subject>Models, Molecular</subject><subject>Molecular and Structural Biology</subject><subject>Nucleic Acid Conformation</subject><subject>Poly U - chemistry</subject><subject>Poly U - genetics</subject><subject>RNA - chemistry</subject><subject>RNA - genetics</subject><issn>0305-1048</issn><issn>1362-4962</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkE1LAzEQQIMoWqsn77JHRVaTTfYjJynFT4qC2nOYzc7qajZpk12x_95Ka9HTHObxZniEHDF6zqjkFxb8xesHYJHTLTJgPEtiIbNkmwwop2nMqCj2yH4I75QywVKxS_a45DkXuRiQ-2c0dQwhYFuaRQS2irSzFdoAXeNs5OqosR361hnUvQEfzZxZnExvTqOnh1E076Hy_czgF4YDslODCXi4nkMyvb56Gd_Gk8ebu_FoEuskp13MhGQ8KTLQdaY1FxR1nQpRZGklM5qUtZagoWbAUEpaiiopdZrrElAmlQTKh-Ry5Z31ZYuVRtt5MGrmmxb8Qjlo1P-Nbd7Uq_tUjKUpy7NiaThZG7yb9xg61TZBozFg0fVBccZ4nibZMtOQnK1Q7V0IHuvNHUbVT361zK_W-Zf08d_XNuxvb_4NVfGDwA</recordid><startdate>20241111</startdate><enddate>20241111</enddate><creator>Roschdi, Saeed</creator><creator>Montemayor, Eric J</creator><creator>Vivek, Rahul</creator><creator>Bingman, Craig A</creator><creator>Butcher, Samuel E</creator><general>Oxford University Press</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6343-6643</orcidid></search><sort><creationdate>20241111</creationdate><title>Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes</title><author>Roschdi, Saeed ; Montemayor, Eric J ; Vivek, Rahul ; Bingman, Craig A ; Butcher, Samuel E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c270t-14913286acf6cc340ecf544865d9602bfc9acaf1a1e990b4d2bc57cbae92d9a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Crystallography, X-Ray</topic><topic>G-Quadruplexes</topic><topic>Models, Molecular</topic><topic>Molecular and Structural Biology</topic><topic>Nucleic Acid Conformation</topic><topic>Poly U - chemistry</topic><topic>Poly U - genetics</topic><topic>RNA - chemistry</topic><topic>RNA - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Roschdi, Saeed</creatorcontrib><creatorcontrib>Montemayor, Eric J</creatorcontrib><creatorcontrib>Vivek, Rahul</creatorcontrib><creatorcontrib>Bingman, Craig A</creatorcontrib><creatorcontrib>Butcher, Samuel E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Roschdi, Saeed</au><au>Montemayor, Eric J</au><au>Vivek, Rahul</au><au>Bingman, Craig A</au><au>Butcher, Samuel E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2024-11-11</date><risdate>2024</risdate><volume>52</volume><issue>20</issue><spage>12582</spage><epage>12591</epage><pages>12582-12591</pages><issn>0305-1048</issn><issn>1362-4962</issn><eissn>1362-4962</eissn><abstract>Poly(UG) or 'pUG' dinucleotide repeats are highly abundant sequences in eukaryotic RNAs. In Caenorhabditis elegans, pUGs are added to RNA 3' ends to direct gene silencing within Mutator foci, a germ granule condensate. Here, we show that pUG RNAs efficiently self-assemble into gel condensates through quadruplex (G4) interactions. Short pUG sequences form right-handed intermolecular G4s (pUG G4s), while longer pUGs form left-handed intramolecular G4s (pUG folds). We determined a 1.05 Å crystal structure of an intermolecular pUG G4, which reveals an eight stranded G4 dimer involving 48 nucleotides, 7 different G and U quartet conformations, 7 coordinated potassium ions, 8 sodium ions and a buried water molecule. A comparison of the intermolecular pUG G4 and intramolecular pUG fold structures provides insights into the molecular basis for G4 handedness and illustrates how a simple dinucleotide repeat sequence can form complex structures with diverse topologies.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>39373474</pmid><doi>10.1093/nar/gkae870</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-6343-6643</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0305-1048 |
| ispartof | Nucleic acids research, 2024-11, Vol.52 (20), p.12582-12591 |
| issn | 0305-1048 1362-4962 1362-4962 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11551768 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Oxford Journals Open Access Collection; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animals Caenorhabditis elegans - genetics Crystallography, X-Ray G-Quadruplexes Models, Molecular Molecular and Structural Biology Nucleic Acid Conformation Poly U - chemistry Poly U - genetics RNA - chemistry RNA - genetics |
| title | Self-assembly and condensation of intermolecular poly(UG) RNA quadruplexes |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-20T09%3A57%3A16IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Self-assembly%20and%20condensation%20of%20intermolecular%20poly(UG)%20RNA%20quadruplexes&rft.jtitle=Nucleic%20acids%20research&rft.au=Roschdi,%20Saeed&rft.date=2024-11-11&rft.volume=52&rft.issue=20&rft.spage=12582&rft.epage=12591&rft.pages=12582-12591&rft.issn=0305-1048&rft.eissn=1362-4962&rft_id=info:doi/10.1093/nar/gkae870&rft_dat=%3Cproquest_pubme%3E3113752639%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3113752639&rft_id=info:pmid/39373474&rfr_iscdi=true |