Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression

Long noncoding RNAs (lncRNAs) are vastly transcribed and extensively studied but lncRNAs overlapping with the sense orientation of mRNA have been poorly studied. We analyzed the lncRNA DAPALR overlapping with the 5' UTR of the Doublesex1 (Dsx1), the male determining gene in Daphnia magna. By af...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS genetics 2021-07, Vol.17 (7), p.e1009683-e1009683
Hauptverfasser: Perez, Christelle Alexa Garcia, Adachi, Shungo, Nong, Quang Dang, Adhitama, Nikko, Matsuura, Tomoaki, Natsume, Toru, Wada, Tadashi, Kato, Yasuhiko, Watanabe, Hajime
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e1009683
container_issue 7
container_start_page e1009683
container_title PLoS genetics
container_volume 17
creator Perez, Christelle Alexa Garcia
Adachi, Shungo
Nong, Quang Dang
Adhitama, Nikko
Matsuura, Tomoaki
Natsume, Toru
Wada, Tadashi
Kato, Yasuhiko
Watanabe, Hajime
description Long noncoding RNAs (lncRNAs) are vastly transcribed and extensively studied but lncRNAs overlapping with the sense orientation of mRNA have been poorly studied. We analyzed the lncRNA DAPALR overlapping with the 5' UTR of the Doublesex1 (Dsx1), the male determining gene in Daphnia magna. By affinity purification, we identified an RNA binding protein, Shep as a DAPALR binding protein. Shep also binds to Dsx1 5' UTR by recognizing the overlapping sequence and suppresses translation of the mRNA. In vitro and in vivo analyses indicated that DAPALR increased Dsx1 translation efficiency by sequestration of Shep. This regulation was impaired when the Shep binding site in DAPALR was deleted. These results suggest that Shep suppresses the unintentional translation of Dsx1 by setting a threshold; and when the sense lncRNA DAPALR is expressed, DAPALR cancels the suppression caused by Shep. This mechanism may be important to show dimorphic gene expressions such as sex determination and it may account for the binary expression in various developmental processes.
doi_str_mv 10.1371/journal.pgen.1009683
format Article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_2561940529</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A670982449</galeid><doaj_id>oai_doaj_org_article_ec4349c4d921424abb7251efb732e657</doaj_id><sourcerecordid>A670982449</sourcerecordid><originalsourceid>FETCH-LOGICAL-c769t-601739a08fefc1bb53ab7df0163d9e57996319453ec03db3631b85bb3a1a0d2e3</originalsourceid><addsrcrecordid>eNqVk99vFCEQxzdGY2v1PzBxExOjD3fCAsvyYnJp_HFJ0yat-kpYdvaOCwdb2G3a_162t5qu6YOGB2D4zHeGgcmy1xgtMeH4484PwSm77DbglhghUVbkSXaMGSMLThF9-mB9lL2IcYcQYZXgz7MjQgkWoiLHWXMFLsLC30CwquuM2-TW6cvzVa5irvIGtL_LfZv3QbloVW98ipkH6ALE6EPeBd-DcXmb1o3Z-9Btjc5TSpDD7T2UPF5mz1plI7ya5pPsx5fP30-_Lc4uvq5PV2cLzUvRL0qEOREKVS20Gtc1I6rmTYtwSRoBjAtRprQpI6ARaWqSdnXF6poorFBTADnJ3hx0O-ujnAoUZcHK5IZYIRKxPhCNVzvZBbNX4U56ZeS9wYeNVKE32oIETQkVmjaiwLSgqq55wTC0NScFlIwnrU9TtKHeQ6PBpSLZmej8xJmt3PgbWRGGBUFJ4P0kEPz1ALGXexM1WKsc-GHMm5Wk4gXCCX37F_r47SZqo9IFjGt9iqtHUbkqORJVQelILR-h0mhgb7R30Jpknzl8mDkkpofbfqOGGOX66vI_2PN_Zy9-ztl3D9gtKNtvo7fD-CHjHKQHUAcfY4D2z4NgJMfG-V05OTaOnBqH_AIM_AjZ</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2561940529</pqid></control><display><type>article</type><title>Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression</title><source>Public Library of Science (PLoS) Journals Open Access</source><source>Free E-Journal (出版社公開部分のみ)</source><source>PubMed Central</source><source>Directory of Open Access Journals</source><creator>Perez, Christelle Alexa Garcia ; Adachi, Shungo ; Nong, Quang Dang ; Adhitama, Nikko ; Matsuura, Tomoaki ; Natsume, Toru ; Wada, Tadashi ; Kato, Yasuhiko ; Watanabe, Hajime</creator><contributor>Delneri, Daniela</contributor><creatorcontrib>Perez, Christelle Alexa Garcia ; Adachi, Shungo ; Nong, Quang Dang ; Adhitama, Nikko ; Matsuura, Tomoaki ; Natsume, Toru ; Wada, Tadashi ; Kato, Yasuhiko ; Watanabe, Hajime ; Delneri, Daniela</creatorcontrib><description>Long noncoding RNAs (lncRNAs) are vastly transcribed and extensively studied but lncRNAs overlapping with the sense orientation of mRNA have been poorly studied. We analyzed the lncRNA DAPALR overlapping with the 5' UTR of the Doublesex1 (Dsx1), the male determining gene in Daphnia magna. By affinity purification, we identified an RNA binding protein, Shep as a DAPALR binding protein. Shep also binds to Dsx1 5' UTR by recognizing the overlapping sequence and suppresses translation of the mRNA. In vitro and in vivo analyses indicated that DAPALR increased Dsx1 translation efficiency by sequestration of Shep. This regulation was impaired when the Shep binding site in DAPALR was deleted. These results suggest that Shep suppresses the unintentional translation of Dsx1 by setting a threshold; and when the sense lncRNA DAPALR is expressed, DAPALR cancels the suppression caused by Shep. This mechanism may be important to show dimorphic gene expressions such as sex determination and it may account for the binary expression in various developmental processes.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009683</identifier><identifier>PMID: 34319983</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>5' Untranslated Regions ; Biology and life sciences ; Females ; Gene expression ; Genetic translation ; Genomes ; Males ; Physiological aspects ; Protein purification ; Proteins ; RNA ; RNA-binding protein ; Sex determination ; Translation</subject><ispartof>PLoS genetics, 2021-07, Vol.17 (7), p.e1009683-e1009683</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Perez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Perez et al 2021 Perez et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c769t-601739a08fefc1bb53ab7df0163d9e57996319453ec03db3631b85bb3a1a0d2e3</citedby><cites>FETCH-LOGICAL-c769t-601739a08fefc1bb53ab7df0163d9e57996319453ec03db3631b85bb3a1a0d2e3</cites><orcidid>0000-0001-5232-411X ; 0000-0001-7864-7654 ; 0000-0003-1015-6781 ; 0000-0002-4428-3669 ; 0000-0001-9657-6554 ; 0000-0002-1041-1044 ; 0000-0001-9414-1549</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/PMC8351930/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351930/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids></links><search><contributor>Delneri, Daniela</contributor><creatorcontrib>Perez, Christelle Alexa Garcia</creatorcontrib><creatorcontrib>Adachi, Shungo</creatorcontrib><creatorcontrib>Nong, Quang Dang</creatorcontrib><creatorcontrib>Adhitama, Nikko</creatorcontrib><creatorcontrib>Matsuura, Tomoaki</creatorcontrib><creatorcontrib>Natsume, Toru</creatorcontrib><creatorcontrib>Wada, Tadashi</creatorcontrib><creatorcontrib>Kato, Yasuhiko</creatorcontrib><creatorcontrib>Watanabe, Hajime</creatorcontrib><title>Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression</title><title>PLoS genetics</title><description>Long noncoding RNAs (lncRNAs) are vastly transcribed and extensively studied but lncRNAs overlapping with the sense orientation of mRNA have been poorly studied. We analyzed the lncRNA DAPALR overlapping with the 5' UTR of the Doublesex1 (Dsx1), the male determining gene in Daphnia magna. By affinity purification, we identified an RNA binding protein, Shep as a DAPALR binding protein. Shep also binds to Dsx1 5' UTR by recognizing the overlapping sequence and suppresses translation of the mRNA. In vitro and in vivo analyses indicated that DAPALR increased Dsx1 translation efficiency by sequestration of Shep. This regulation was impaired when the Shep binding site in DAPALR was deleted. These results suggest that Shep suppresses the unintentional translation of Dsx1 by setting a threshold; and when the sense lncRNA DAPALR is expressed, DAPALR cancels the suppression caused by Shep. This mechanism may be important to show dimorphic gene expressions such as sex determination and it may account for the binary expression in various developmental processes.</description><subject>5' Untranslated Regions</subject><subject>Biology and life sciences</subject><subject>Females</subject><subject>Gene expression</subject><subject>Genetic translation</subject><subject>Genomes</subject><subject>Males</subject><subject>Physiological aspects</subject><subject>Protein purification</subject><subject>Proteins</subject><subject>RNA</subject><subject>RNA-binding protein</subject><subject>Sex determination</subject><subject>Translation</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk99vFCEQxzdGY2v1PzBxExOjD3fCAsvyYnJp_HFJ0yat-kpYdvaOCwdb2G3a_162t5qu6YOGB2D4zHeGgcmy1xgtMeH4484PwSm77DbglhghUVbkSXaMGSMLThF9-mB9lL2IcYcQYZXgz7MjQgkWoiLHWXMFLsLC30CwquuM2-TW6cvzVa5irvIGtL_LfZv3QbloVW98ipkH6ALE6EPeBd-DcXmb1o3Z-9Btjc5TSpDD7T2UPF5mz1plI7ya5pPsx5fP30-_Lc4uvq5PV2cLzUvRL0qEOREKVS20Gtc1I6rmTYtwSRoBjAtRprQpI6ARaWqSdnXF6poorFBTADnJ3hx0O-ujnAoUZcHK5IZYIRKxPhCNVzvZBbNX4U56ZeS9wYeNVKE32oIETQkVmjaiwLSgqq55wTC0NScFlIwnrU9TtKHeQ6PBpSLZmej8xJmt3PgbWRGGBUFJ4P0kEPz1ALGXexM1WKsc-GHMm5Wk4gXCCX37F_r47SZqo9IFjGt9iqtHUbkqORJVQelILR-h0mhgb7R30Jpknzl8mDkkpofbfqOGGOX66vI_2PN_Zy9-ztl3D9gtKNtvo7fD-CHjHKQHUAcfY4D2z4NgJMfG-V05OTaOnBqH_AIM_AjZ</recordid><startdate>20210728</startdate><enddate>20210728</enddate><creator>Perez, Christelle Alexa Garcia</creator><creator>Adachi, Shungo</creator><creator>Nong, Quang Dang</creator><creator>Adhitama, Nikko</creator><creator>Matsuura, Tomoaki</creator><creator>Natsume, Toru</creator><creator>Wada, Tadashi</creator><creator>Kato, Yasuhiko</creator><creator>Watanabe, Hajime</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5232-411X</orcidid><orcidid>https://orcid.org/0000-0001-7864-7654</orcidid><orcidid>https://orcid.org/0000-0003-1015-6781</orcidid><orcidid>https://orcid.org/0000-0002-4428-3669</orcidid><orcidid>https://orcid.org/0000-0001-9657-6554</orcidid><orcidid>https://orcid.org/0000-0002-1041-1044</orcidid><orcidid>https://orcid.org/0000-0001-9414-1549</orcidid></search><sort><creationdate>20210728</creationdate><title>Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression</title><author>Perez, Christelle Alexa Garcia ; Adachi, Shungo ; Nong, Quang Dang ; Adhitama, Nikko ; Matsuura, Tomoaki ; Natsume, Toru ; Wada, Tadashi ; Kato, Yasuhiko ; Watanabe, Hajime</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c769t-601739a08fefc1bb53ab7df0163d9e57996319453ec03db3631b85bb3a1a0d2e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>5' Untranslated Regions</topic><topic>Biology and life sciences</topic><topic>Females</topic><topic>Gene expression</topic><topic>Genetic translation</topic><topic>Genomes</topic><topic>Males</topic><topic>Physiological aspects</topic><topic>Protein purification</topic><topic>Proteins</topic><topic>RNA</topic><topic>RNA-binding protein</topic><topic>Sex determination</topic><topic>Translation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Perez, Christelle Alexa Garcia</creatorcontrib><creatorcontrib>Adachi, Shungo</creatorcontrib><creatorcontrib>Nong, Quang Dang</creatorcontrib><creatorcontrib>Adhitama, Nikko</creatorcontrib><creatorcontrib>Matsuura, Tomoaki</creatorcontrib><creatorcontrib>Natsume, Toru</creatorcontrib><creatorcontrib>Wada, Tadashi</creatorcontrib><creatorcontrib>Kato, Yasuhiko</creatorcontrib><creatorcontrib>Watanabe, Hajime</creatorcontrib><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>ProQuest - Health &amp; Medical Complete保健、医学与药学数据库</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Perez, Christelle Alexa Garcia</au><au>Adachi, Shungo</au><au>Nong, Quang Dang</au><au>Adhitama, Nikko</au><au>Matsuura, Tomoaki</au><au>Natsume, Toru</au><au>Wada, Tadashi</au><au>Kato, Yasuhiko</au><au>Watanabe, Hajime</au><au>Delneri, Daniela</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression</atitle><jtitle>PLoS genetics</jtitle><date>2021-07-28</date><risdate>2021</risdate><volume>17</volume><issue>7</issue><spage>e1009683</spage><epage>e1009683</epage><pages>e1009683-e1009683</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Long noncoding RNAs (lncRNAs) are vastly transcribed and extensively studied but lncRNAs overlapping with the sense orientation of mRNA have been poorly studied. We analyzed the lncRNA DAPALR overlapping with the 5' UTR of the Doublesex1 (Dsx1), the male determining gene in Daphnia magna. By affinity purification, we identified an RNA binding protein, Shep as a DAPALR binding protein. Shep also binds to Dsx1 5' UTR by recognizing the overlapping sequence and suppresses translation of the mRNA. In vitro and in vivo analyses indicated that DAPALR increased Dsx1 translation efficiency by sequestration of Shep. This regulation was impaired when the Shep binding site in DAPALR was deleted. These results suggest that Shep suppresses the unintentional translation of Dsx1 by setting a threshold; and when the sense lncRNA DAPALR is expressed, DAPALR cancels the suppression caused by Shep. This mechanism may be important to show dimorphic gene expressions such as sex determination and it may account for the binary expression in various developmental processes.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>34319983</pmid><doi>10.1371/journal.pgen.1009683</doi><orcidid>https://orcid.org/0000-0001-5232-411X</orcidid><orcidid>https://orcid.org/0000-0001-7864-7654</orcidid><orcidid>https://orcid.org/0000-0003-1015-6781</orcidid><orcidid>https://orcid.org/0000-0002-4428-3669</orcidid><orcidid>https://orcid.org/0000-0001-9657-6554</orcidid><orcidid>https://orcid.org/0000-0002-1041-1044</orcidid><orcidid>https://orcid.org/0000-0001-9414-1549</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1553-7404
ispartof PLoS genetics, 2021-07, Vol.17 (7), p.e1009683-e1009683
issn 1553-7404
1553-7390
1553-7404
language eng
recordid cdi_plos_journals_2561940529
source Public Library of Science (PLoS) Journals Open Access; Free E-Journal (出版社公開部分のみ); PubMed Central; Directory of Open Access Journals
subjects 5' Untranslated Regions
Biology and life sciences
Females
Gene expression
Genetic translation
Genomes
Males
Physiological aspects
Protein purification
Proteins
RNA
RNA-binding protein
Sex determination
Translation
title Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T08%3A39%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Sense-overlapping%20lncRNA%20as%20a%20decoy%20of%20translational%20repressor%20protein%20for%20dimorphic%20gene%20expression&rft.jtitle=PLoS%20genetics&rft.au=Perez,%20Christelle%20Alexa%20Garcia&rft.date=2021-07-28&rft.volume=17&rft.issue=7&rft.spage=e1009683&rft.epage=e1009683&rft.pages=e1009683-e1009683&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1009683&rft_dat=%3Cgale_plos_%3EA670982449%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2561940529&rft_id=info:pmid/34319983&rft_galeid=A670982449&rft_doaj_id=oai_doaj_org_article_ec4349c4d921424abb7251efb732e657&rfr_iscdi=true