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piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm

Identifieur interne : 000000 ( Pmc/Checkpoint ); suivant : 000001

piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm

Auteurs : Jérémy Dufourt [France] ; Gwénaëlle Bontonou [France] ; Aymeric Chartier [France] ; Camille Jahan [France] ; Anne-Cécile Meunier [France] ; Stéphanie Pierson [France] ; Paul F. Harrison ; Catherine Papin [France] ; Traude H. Beilharz ; Martine Simonelig [France]

Source :

RBID : PMC:5670238

Abstract

Piwi-interacting RNAs (piRNAs) and PIWI proteins play a crucial role in germ cells by repressing transposable elements and regulating gene expression. In Drosophila, maternal piRNAs are loaded into the embryo mostly bound to the PIWI protein Aubergine (Aub). Aub targets maternal mRNAs through incomplete base-pairing with piRNAs and can induce their destabilization in the somatic part of the embryo. Paradoxically, these Aub-dependent unstable mRNAs encode germ cell determinants that are selectively stabilized in the germ plasm. Here we show that piRNAs and Aub actively protect germ cell mRNAs in the germ plasm. Aub directly interacts with the germline-specific poly(A) polymerase Wispy, thus leading to mRNA polyadenylation and stabilization in the germ plasm. These results reveal a role for piRNAs in mRNA stabilization and identify Aub as an interactor of Wispy for mRNA polyadenylation. They further highlight the role of Aub and piRNAs in embryonic patterning through two opposite functions.


Url:
DOI: 10.1038/s41467-017-01431-5
PubMed: 29101389
PubMed Central: 5670238


Affiliations:


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PMC:5670238

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<front>
<div type="abstract" xml:lang="en">
<p id="Par1">Piwi-interacting RNAs (piRNAs) and PIWI proteins play a crucial role in germ cells by repressing transposable elements and regulating gene expression. In
<italic>Drosophila</italic>
, maternal piRNAs are loaded into the embryo mostly bound to the PIWI protein Aubergine (Aub). Aub targets maternal mRNAs through incomplete base-pairing with piRNAs and can induce their destabilization in the somatic part of the embryo. Paradoxically, these Aub-dependent unstable mRNAs encode germ cell determinants that are selectively stabilized in the germ plasm. Here we show that piRNAs and Aub actively protect germ cell mRNAs in the germ plasm. Aub directly interacts with the germline-specific poly(A) polymerase Wispy, thus leading to mRNA polyadenylation and stabilization in the germ plasm. These results reveal a role for piRNAs in mRNA stabilization and identify Aub as an interactor of Wispy for mRNA polyadenylation. They further highlight the role of Aub and piRNAs in embryonic patterning through two opposite functions.</p>
</div>
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</div1>
</back>
</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Nat Commun</journal-id>
<journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id>
<journal-title-group>
<journal-title>Nature Communications</journal-title>
</journal-title-group>
<issn pub-type="epub">2041-1723</issn>
<publisher>
<publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">29101389</article-id>
<article-id pub-id-type="pmc">5670238</article-id>
<article-id pub-id-type="publisher-id">1431</article-id>
<article-id pub-id-type="doi">10.1038/s41467-017-01431-5</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Dufourt</surname>
<given-names>Jérémy</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bontonou</surname>
<given-names>Gwénaëlle</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chartier</surname>
<given-names>Aymeric</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jahan</surname>
<given-names>Camille</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Meunier</surname>
<given-names>Anne-Cécile</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pierson</surname>
<given-names>Stéphanie</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-3980-268X</contrib-id>
<name>
<surname>Harrison</surname>
<given-names>Paul F.</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author" deceased="yes">
<name>
<surname>Papin</surname>
<given-names>Catherine</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Beilharz</surname>
<given-names>Traude H.</given-names>
</name>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-3731-6979</contrib-id>
<name>
<surname>Simonelig</surname>
<given-names>Martine</given-names>
</name>
<address>
<phone>+33 4 34 35 99 59</phone>
<email>Martine.Simonelig@igh.cnrs.fr</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<aff id="Aff1">
<label>1</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0000 9886 5504</institution-id>
<institution-id institution-id-type="GRID">grid.462268.c</institution-id>
<institution>mRNA Regulation and Development,</institution>
<institution>Institute of Human Genetics, UMR9002 CNRS-University of Montpellier,</institution>
</institution-wrap>
141 rue de la Cardonille, 34396 Montpellier Cedex 5, France</aff>
<aff id="Aff2">
<label>2</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 7857</institution-id>
<institution-id institution-id-type="GRID">grid.1002.3</institution-id>
<institution>Monash Bioinformatics Platform,</institution>
<institution>Monash University,</institution>
</institution-wrap>
Melbourne, VIC 3800 Australia</aff>
<aff id="Aff3">
<label>3</label>
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 1936 7857</institution-id>
<institution-id institution-id-type="GRID">grid.1002.3</institution-id>
<institution>Development and Stem Cells Program,</institution>
<institution>Monash Biomedicine Discovery Institute, Monash University,</institution>
</institution-wrap>
Melbourne, VIC 3800 Australia</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>3</day>
<month>11</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>3</day>
<month>11</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<year>2017</year>
</pub-date>
<volume>8</volume>
<elocation-id>1305</elocation-id>
<history>
<date date-type="received">
<day>10</day>
<month>1</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>18</day>
<month>9</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>© The Author(s) 2017</copyright-statement>
<license license-type="OpenAccess">
<license-p>
<bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<p id="Par1">Piwi-interacting RNAs (piRNAs) and PIWI proteins play a crucial role in germ cells by repressing transposable elements and regulating gene expression. In
<italic>Drosophila</italic>
, maternal piRNAs are loaded into the embryo mostly bound to the PIWI protein Aubergine (Aub). Aub targets maternal mRNAs through incomplete base-pairing with piRNAs and can induce their destabilization in the somatic part of the embryo. Paradoxically, these Aub-dependent unstable mRNAs encode germ cell determinants that are selectively stabilized in the germ plasm. Here we show that piRNAs and Aub actively protect germ cell mRNAs in the germ plasm. Aub directly interacts with the germline-specific poly(A) polymerase Wispy, thus leading to mRNA polyadenylation and stabilization in the germ plasm. These results reveal a role for piRNAs in mRNA stabilization and identify Aub as an interactor of Wispy for mRNA polyadenylation. They further highlight the role of Aub and piRNAs in embryonic patterning through two opposite functions.</p>
</abstract>
<abstract id="Abs2" abstract-type="web-summary">
<p id="Par2">In
<italic>Drosophila</italic>
embryos, Piwi-interacting RNAs (piRNAs) loaded into the PIWI protein Aubergine target and destabilize maternal mRNAs. Here, the authors provide evidence that piRNAs and Aubergine cooperate with the Wispy poly(A) polymerase to stabilize these mRNAs in the germ plasm.</p>
</abstract>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2017</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>France</li>
</country>
<region>
<li>Languedoc-Roussillon</li>
<li>Occitanie (région administrative)</li>
</region>
<settlement>
<li>Montpellier</li>
</settlement>
</list>
<tree>
<noCountry>
<name sortKey="Beilharz, Traude H" sort="Beilharz, Traude H" uniqKey="Beilharz T" first="Traude H." last="Beilharz">Traude H. Beilharz</name>
<name sortKey="Harrison, Paul F" sort="Harrison, Paul F" uniqKey="Harrison P" first="Paul F." last="Harrison">Paul F. Harrison</name>
</noCountry>
<country name="France">
<region name="Occitanie (région administrative)">
<name sortKey="Dufourt, Jeremy" sort="Dufourt, Jeremy" uniqKey="Dufourt J" first="Jérémy" last="Dufourt">Jérémy Dufourt</name>
</region>
<name sortKey="Bontonou, Gwenaelle" sort="Bontonou, Gwenaelle" uniqKey="Bontonou G" first="Gwénaëlle" last="Bontonou">Gwénaëlle Bontonou</name>
<name sortKey="Chartier, Aymeric" sort="Chartier, Aymeric" uniqKey="Chartier A" first="Aymeric" last="Chartier">Aymeric Chartier</name>
<name sortKey="Jahan, Camille" sort="Jahan, Camille" uniqKey="Jahan C" first="Camille" last="Jahan">Camille Jahan</name>
<name sortKey="Meunier, Anne Cecile" sort="Meunier, Anne Cecile" uniqKey="Meunier A" first="Anne-Cécile" last="Meunier">Anne-Cécile Meunier</name>
<name sortKey="Papin, Catherine" sort="Papin, Catherine" uniqKey="Papin C" first="Catherine" last="Papin">Catherine Papin</name>
<name sortKey="Pierson, Stephanie" sort="Pierson, Stephanie" uniqKey="Pierson S" first="Stéphanie" last="Pierson">Stéphanie Pierson</name>
<name sortKey="Simonelig, Martine" sort="Simonelig, Martine" uniqKey="Simonelig M" first="Martine" last="Simonelig">Martine Simonelig</name>
</country>
</tree>
</affiliations>
</record>

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