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...
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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 |
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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 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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. 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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 |
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