Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders
Identifieur interne : 000058 ( Pmc/Curation ); précédent : 000057; suivant : 000059Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders
Auteurs : Sandra Blanco [Royaume-Uni] ; Sabine Dietmann [Royaume-Uni] ; Joana V. Flores [Royaume-Uni] ; Shobbir Hussain [Royaume-Uni] ; Claudia Kutter [Royaume-Uni] ; Peter Humphreys [Royaume-Uni] ; Margus Lukk [Royaume-Uni] ; Patrick Lombard [Royaume-Uni] ; Lucas Treps [France] ; Martyna Popis [Royaume-Uni] ; Stefanie Kellner [Allemagne] ; Sabine M. Hölter [Allemagne] ; Lillian Garrett [Allemagne] ; Wolfgang Wurst [Allemagne] ; Lore Becker [Allemagne] ; Thomas Klopstock [Allemagne] ; Helmut Fuchs [Allemagne] ; Valerie Gailus-Durner [Allemagne] ; Martin Hrab De Angelis [Allemagne] ; Ragnhildur T. Kárad Ttir [Royaume-Uni] ; Mark Helm [Allemagne] ; Jernej Ule [Royaume-Uni] ; Joseph G. Gleeson [États-Unis] ; Duncan T. Odom [Royaume-Uni] ; Michaela Frye [Royaume-Uni]Source :
- The EMBO Journal [ 0261-4189 ] ; 2014.
Abstract
Mutations in the cytosine-5 RNA methyltransferase NSun2 cause microcephaly and other neurological abnormalities in mice and human. How post-transcriptional methylation contributes to the human disease is currently unknown. By comparing gene expression data with global cytosine-5 RNA methylomes in patient fibroblasts and NSun2-deficient mice, we find that loss of cytosine-5 RNA methylation increases the angiogenin-mediated endonucleolytic cleavage of transfer RNAs (tRNA) leading to an accumulation of 5′ tRNA-derived small RNA fragments. Accumulation of 5′ tRNA fragments in the absence of NSun2 reduces protein translation rates and activates stress pathways leading to reduced cell size and increased apoptosis of cortical, hippocampal and striatal neurons. Mechanistically, we demonstrate that angiogenin binds with higher affinity to tRNAs lacking site-specific NSun2-mediated methylation and that the presence of 5′ tRNA fragments is sufficient and required to trigger cellular stress responses. Furthermore, the enhanced sensitivity of NSun2-deficient brains to oxidative stress can be rescued through inhibition of angiogenin during embryogenesis. In conclusion, failure in NSun2-mediated tRNA methylation contributes to human diseases via stress-induced RNA cleavage.
Url:
DOI: 10.15252/embj.201489282
PubMed: 25063673
PubMed Central: 4195770
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</nlm:aff>
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</nlm:aff>
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</nlm:aff>
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<affiliation wicri:level="1"><nlm:aff id="au6"><institution>Institute of Developmental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Garrett, Lillian" sort="Garrett, Lillian" uniqKey="Garrett L" first="Lillian" last="Garrett">Lillian Garrett</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au6"><institution>Institute of Developmental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wurst, Wolfgang" sort="Wurst, Wolfgang" uniqKey="Wurst W" first="Wolfgang" last="Wurst">Wolfgang Wurst</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au6"><institution>Institute of Developmental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au7"><institution>German Center for Vertigo and Balance Disorders</institution>
<addr-line>Munich, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Munich</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Becker, Lore" sort="Becker, Lore" uniqKey="Becker L" first="Lore" last="Becker">Lore Becker</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au8"><institution>Institute for Experimental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
</author>
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<affiliation wicri:level="1"><nlm:aff id="au7"><institution>German Center for Vertigo and Balance Disorders</institution>
<addr-line>Munich, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Munich</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au9"><institution>Department of Neurology, Friedrich-Baur-Institute, Ludwig-Maximilians-University</institution>
<addr-line>Munich, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Munich</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Fuchs, Helmut" sort="Fuchs, Helmut" uniqKey="Fuchs H" first="Helmut" last="Fuchs">Helmut Fuchs</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au8"><institution>Institute for Experimental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
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</author>
<author><name sortKey="Gailus Durner, Valerie" sort="Gailus Durner, Valerie" uniqKey="Gailus Durner V" first="Valerie" last="Gailus-Durner">Valerie Gailus-Durner</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au8"><institution>Institute for Experimental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hrab De Angelis, Martin" sort="Hrab De Angelis, Martin" uniqKey="Hrab De Angelis M" first="Martin" last="Hrab De Angelis">Martin Hrab De Angelis</name>
<affiliation wicri:level="1"><nlm:aff id="au5"><institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="au8"><institution>Institute for Experimental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Neuherberg</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="au1"><institution>Wellcome Trust – Medical Research Council Cambridge Stem Cell Institute, University of Cambridge</institution>
<addr-line>Cambridge, UK</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Cambridge</wicri:regionArea>
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<author><name sortKey="Helm, Mark" sort="Helm, Mark" uniqKey="Helm M" first="Mark" last="Helm">Mark Helm</name>
<affiliation wicri:level="1"><nlm:aff id="au4"><institution>Johannes Gutenberg University Mainz, Institute for Pharmacy and Biochemistry</institution>
<addr-line>Mainz, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Mainz</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="au10"><institution>Department of Molecular Neuroscience, UCL Institute of Neurology</institution>
<addr-line>London, UK</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>London</wicri:regionArea>
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<author><name sortKey="Gleeson, Joseph G" sort="Gleeson, Joseph G" uniqKey="Gleeson J" first="Joseph G" last="Gleeson">Joseph G. Gleeson</name>
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<addr-line>New York, NY, USA</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>New York, NY</wicri:regionArea>
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<author><name sortKey="Odom, Duncan T" sort="Odom, Duncan T" uniqKey="Odom D" first="Duncan T" last="Odom">Duncan T. Odom</name>
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<addr-line>Cambridge, UK</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Cambridge</wicri:regionArea>
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<author><name sortKey="Frye, Michaela" sort="Frye, Michaela" uniqKey="Frye M" first="Michaela" last="Frye">Michaela Frye</name>
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<addr-line>Cambridge, UK</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Cambridge</wicri:regionArea>
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</analytic>
<series><title level="j">The EMBO Journal</title>
<idno type="ISSN">0261-4189</idno>
<idno type="eISSN">1460-2075</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
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<front><div type="abstract" xml:lang="en"><p>Mutations in the cytosine-5 RNA methyltransferase NSun2 cause microcephaly and other neurological abnormalities in mice and human. How post-transcriptional methylation contributes to the human disease is currently unknown. By comparing gene expression data with global cytosine-5 RNA methylomes in patient fibroblasts and NSun2-deficient mice, we find that loss of cytosine-5 RNA methylation increases the angiogenin-mediated endonucleolytic cleavage of transfer RNAs (tRNA) leading to an accumulation of 5′ tRNA-derived small RNA fragments. Accumulation of 5′ tRNA fragments in the absence of NSun2 reduces protein translation rates and activates stress pathways leading to reduced cell size and increased apoptosis of cortical, hippocampal and striatal neurons. Mechanistically, we demonstrate that angiogenin binds with higher affinity to tRNAs lacking site-specific NSun2-mediated methylation and that the presence of 5′ tRNA fragments is sufficient and required to trigger cellular stress responses. Furthermore, the enhanced sensitivity of NSun2-deficient brains to oxidative stress can be rescued through inhibition of angiogenin during embryogenesis. In conclusion, failure in NSun2-mediated tRNA methylation contributes to human diseases via stress-induced RNA cleavage.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">EMBO J</journal-id>
<journal-id journal-id-type="iso-abbrev">EMBO J</journal-id>
<journal-id journal-id-type="publisher-id">embj</journal-id>
<journal-title-group><journal-title>The EMBO Journal</journal-title>
</journal-title-group>
<issn pub-type="ppub">0261-4189</issn>
<issn pub-type="epub">1460-2075</issn>
<publisher><publisher-name>BlackWell Publishing Ltd</publisher-name>
<publisher-loc>Oxford, UK</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25063673</article-id>
<article-id pub-id-type="pmc">4195770</article-id>
<article-id pub-id-type="doi">10.15252/embj.201489282</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Blanco</surname>
<given-names>Sandra</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dietmann</surname>
<given-names>Sabine</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Flores</surname>
<given-names>Joana V</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hussain</surname>
<given-names>Shobbir</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kutter</surname>
<given-names>Claudia</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Humphreys</surname>
<given-names>Peter</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lukk</surname>
<given-names>Margus</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lombard</surname>
<given-names>Patrick</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Treps</surname>
<given-names>Lucas</given-names>
</name>
<xref ref-type="aff" rid="au3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Popis</surname>
<given-names>Martyna</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kellner</surname>
<given-names>Stefanie</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hölter</surname>
<given-names>Sabine M</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Garrett</surname>
<given-names>Lillian</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wurst</surname>
<given-names>Wolfgang</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au6">6</xref>
<xref ref-type="aff" rid="au7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Becker</surname>
<given-names>Lore</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Klopstock</surname>
<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="au7">7</xref>
<xref ref-type="aff" rid="au9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fuchs</surname>
<given-names>Helmut</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gailus-Durner</surname>
<given-names>Valerie</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hrabĕ de Angelis</surname>
<given-names>Martin</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Káradóttir</surname>
<given-names>Ragnhildur T</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Helm</surname>
<given-names>Mark</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ule</surname>
<given-names>Jernej</given-names>
</name>
<xref ref-type="aff" rid="au10">10</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gleeson</surname>
<given-names>Joseph G</given-names>
</name>
<xref ref-type="aff" rid="au11">11</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Odom</surname>
<given-names>Duncan T</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Frye</surname>
<given-names>Michaela</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<aff id="au1"><label>1</label>
<institution>Wellcome Trust – Medical Research Council Cambridge Stem Cell Institute, University of Cambridge</institution>
<addr-line>Cambridge, UK</addr-line>
</aff>
<aff id="au2"><label>2</label>
<institution>Li Ka Shing Centre, CR-UK Cambridge Institute, University of Cambridge</institution>
<addr-line>Cambridge, UK</addr-line>
</aff>
<aff id="au3"><label>3</label>
<institution>CNRS, UMR8104</institution>
<addr-line>Paris, France</addr-line>
</aff>
<aff id="au4"><label>4</label>
<institution>Johannes Gutenberg University Mainz, Institute for Pharmacy and Biochemistry</institution>
<addr-line>Mainz, Germany</addr-line>
</aff>
<aff id="au5"><label>5</label>
<institution>German Mouse Clinic, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</aff>
<aff id="au6"><label>6</label>
<institution>Institute of Developmental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</aff>
<aff id="au7"><label>7</label>
<institution>German Center for Vertigo and Balance Disorders</institution>
<addr-line>Munich, Germany</addr-line>
</aff>
<aff id="au8"><label>8</label>
<institution>Institute for Experimental Genetics, Helmholtz Zentrum München</institution>
<addr-line>Neuherberg, Germany</addr-line>
</aff>
<aff id="au9"><label>9</label>
<institution>Department of Neurology, Friedrich-Baur-Institute, Ludwig-Maximilians-University</institution>
<addr-line>Munich, Germany</addr-line>
</aff>
<aff id="au10"><label>10</label>
<institution>Department of Molecular Neuroscience, UCL Institute of Neurology</institution>
<addr-line>London, UK</addr-line>
</aff>
<aff id="au11"><label>11</label>
<institution>Laboratory of Pediatric Brain Diseases, Howard Hughes Medical Institute, The Rockefeller University</institution>
<addr-line>New York, NY, USA</addr-line>
</aff>
</contrib-group>
<author-notes><corresp id="cor1">*Corresponding author. Tel: +44 1223 760230; Fax: +44 1223 760241; E-mails: <email>Michaela.Frye@cancer.org.uk</email>
; <email>mf364@cam.ac.uk</email>
</corresp>
<fn><p><bold>Subject Categories</bold>
Molecular Biology of Disease; Neuroscience; RNA Biology</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>17</day>
<month>9</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>25</day>
<month>7</month>
<year>2014</year>
</pub-date>
<volume>33</volume>
<issue>18</issue>
<fpage>2020</fpage>
<lpage>2039</lpage>
<history><date date-type="received"><day>16</day>
<month>6</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>23</day>
<month>6</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© 2014 The Authors. Published under the terms of the CC BY 4.0 license</copyright-statement>
<copyright-year>2014</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<related-article related-article-type="companion" id="d35e386" vol="33" page="1981" xlink:href="25216676" ext-link-type="pubmed"></related-article>
<abstract><p>Mutations in the cytosine-5 RNA methyltransferase NSun2 cause microcephaly and other neurological abnormalities in mice and human. How post-transcriptional methylation contributes to the human disease is currently unknown. By comparing gene expression data with global cytosine-5 RNA methylomes in patient fibroblasts and NSun2-deficient mice, we find that loss of cytosine-5 RNA methylation increases the angiogenin-mediated endonucleolytic cleavage of transfer RNAs (tRNA) leading to an accumulation of 5′ tRNA-derived small RNA fragments. Accumulation of 5′ tRNA fragments in the absence of NSun2 reduces protein translation rates and activates stress pathways leading to reduced cell size and increased apoptosis of cortical, hippocampal and striatal neurons. Mechanistically, we demonstrate that angiogenin binds with higher affinity to tRNAs lacking site-specific NSun2-mediated methylation and that the presence of 5′ tRNA fragments is sufficient and required to trigger cellular stress responses. Furthermore, the enhanced sensitivity of NSun2-deficient brains to oxidative stress can be rescued through inhibition of angiogenin during embryogenesis. In conclusion, failure in NSun2-mediated tRNA methylation contributes to human diseases via stress-induced RNA cleavage.</p>
</abstract>
<kwd-group><kwd>5-methylcytidine</kwd>
<kwd>Misu</kwd>
<kwd>NSun2</kwd>
<kwd>RNA modification</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>
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