RuvbL1 and RuvbL2 enhance aggresome formation and disaggregate amyloid fibrils
Identifieur interne : 000041 ( Pmc/Curation ); précédent : 000040; suivant : 000042RuvbL1 and RuvbL2 enhance aggresome formation and disaggregate amyloid fibrils
Auteurs : Nava Zaarur [États-Unis] ; Xiaobin Xu [États-Unis] ; Patrick Lestienne [France] ; Anatoli B. Meriin [États-Unis] ; Mark Mccomb [États-Unis] ; Catherine E. Costello [États-Unis] ; Gary P. Newnam [États-Unis] ; Rakhee Ganti [États-Unis] ; Nina V. Romanova [Russie] ; Maruda Shanmugasundaram [États-Unis] ; Sara Tn Silva [Portugal] ; Tiago M. Bandeiras [Portugal] ; Pedro M. Matias [Portugal] ; Kirill S. Lobachev [États-Unis] ; Igor K. Lednev [États-Unis] ; Yury O. Chernoff [États-Unis, Russie] ; Michael Y. Sherman [États-Unis]Source :
- The EMBO Journal [ 0261-4189 ] ; 2015.
Abstract
The aggresome is an organelle that recruits aggregated proteins for storage and degradation. We performed an siRNA screen for proteins involved in aggresome formation and identified novel mammalian AAA+ protein disaggregases RuvbL1 and RuvbL2. Depletion of RuvbL1 or RuvbL2 suppressed aggresome formation and caused buildup of multiple cytoplasmic aggregates. Similarly, downregulation of RuvbL orthologs in yeast suppressed the formation of an aggresome-like body and enhanced the aggregate toxicity. In contrast, their overproduction enhanced the resistance to proteotoxic stress independently of chaperone Hsp104. Mammalian RuvbL associated with the aggresome, and the aggresome substrate synphilin-1 interacted directly with the RuvbL1 barrel-like structure near the opening of the central channel. Importantly, polypeptides with unfolded structures and amyloid fibrils stimulated the ATPase activity of RuvbL. Finally, disassembly of protein aggregates was promoted by RuvbL. These data indicate that RuvbL complexes serve as chaperones in protein disaggregation.
Url:
DOI: 10.15252/embj.201591245
PubMed: 26303906
PubMed Central: 4570522
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<front><div type="abstract" xml:lang="en"><p>The aggresome is an organelle that recruits aggregated proteins for storage and degradation. We performed an siRNA screen for proteins involved in aggresome formation and identified novel mammalian AAA+ protein disaggregases RuvbL1 and RuvbL2. Depletion of RuvbL1 or RuvbL2 suppressed aggresome formation and caused buildup of multiple cytoplasmic aggregates. Similarly, downregulation of RuvbL orthologs in yeast suppressed the formation of an aggresome-like body and enhanced the aggregate toxicity. In contrast, their overproduction enhanced the resistance to proteotoxic stress independently of chaperone Hsp104. Mammalian RuvbL associated with the aggresome, and the aggresome substrate synphilin-1 interacted directly with the RuvbL1 barrel-like structure near the opening of the central channel. Importantly, polypeptides with unfolded structures and amyloid fibrils stimulated the ATPase activity of RuvbL. Finally, disassembly of protein aggregates was promoted by RuvbL. These data indicate that RuvbL complexes serve as chaperones in protein disaggregation.</p>
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<article-meta><article-id pub-id-type="pmid">26303906</article-id>
<article-id pub-id-type="pmc">4570522</article-id>
<article-id pub-id-type="doi">10.15252/embj.201591245</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>RuvbL1 and RuvbL2 enhance aggresome formation and disaggregate amyloid fibrils</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zaarur</surname>
<given-names>Nava</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xu</surname>
<given-names>Xiaobin</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lestienne</surname>
<given-names>Patrick</given-names>
</name>
<xref ref-type="aff" rid="au3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meriin</surname>
<given-names>Anatoli B</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McComb</surname>
<given-names>Mark</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Costello</surname>
<given-names>Catherine E</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Newnam</surname>
<given-names>Gary P</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ganti</surname>
<given-names>Rakhee</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Romanova</surname>
<given-names>Nina V</given-names>
</name>
<xref ref-type="aff" rid="au5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shanmugasundaram</surname>
<given-names>Maruda</given-names>
</name>
<xref ref-type="aff" rid="au6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Silva</surname>
<given-names>Sara TN</given-names>
</name>
<xref ref-type="aff" rid="au7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bandeiras</surname>
<given-names>Tiago M</given-names>
</name>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Matias</surname>
<given-names>Pedro M</given-names>
</name>
<xref ref-type="aff" rid="au7">7</xref>
<xref ref-type="aff" rid="au8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lobachev</surname>
<given-names>Kirill S</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lednev</surname>
<given-names>Igor K</given-names>
</name>
<xref ref-type="aff" rid="au6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chernoff</surname>
<given-names>Yury O</given-names>
</name>
<xref ref-type="aff" rid="au4">4</xref>
<xref ref-type="aff" rid="au5">5</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sherman</surname>
<given-names>Michael Y</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
<xref ref-type="corresp" rid="cor2">**</xref>
</contrib>
<aff id="au1"><label>1</label>
<institution>Department of Biochemistry, Boston University School of Medicine</institution>
<addr-line>Boston, MA, USA</addr-line>
</aff>
<aff id="au2"><label>2</label>
<institution>Center for Biomedical Mass Spectrometry, Boston University School of Medicine</institution>
<addr-line>Boston, MA, USA</addr-line>
</aff>
<aff id="au3"><label>3</label>
<institution>INSERM U 1053, University of Bordeaux Segalen</institution>
<addr-line>Bordeaux, France</addr-line>
</aff>
<aff id="au4"><label>4</label>
<institution>School of Biology, Georgia Institute of Technology</institution>
<addr-line>Atlanta, GA, USA</addr-line>
</aff>
<aff id="au5"><label>5</label>
<institution>Laboratory of Amyloid Biology and Institute of Translational Biomedicine, St. Petersburg State University</institution>
<addr-line>St. Petersburg, Russia</addr-line>
</aff>
<aff id="au6"><label>6</label>
<institution>Department of Chemistry, University at Albany, State University of New York</institution>
<addr-line>Albany, NY, USA</addr-line>
</aff>
<aff id="au7"><label>7</label>
<institution>Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa</institution>
<addr-line>Oeiras, Portugal</addr-line>
</aff>
<aff id="au8"><label>8</label>
<institution>Instituto de Biologia Experimental e Tecnológica</institution>
<addr-line>Oeiras, Portugal</addr-line>
</aff>
</contrib-group>
<author-notes><corresp id="cor1">*Corresponding author. Tel: +1 404 894 1157; E-mail: <email>yury.chernoff@biology.gatech.edu</email>
</corresp>
<corresp id="cor2">**Corresponding author. Tel: +1 617 638 5971; E-mail: <email>sherma1@bu.edu</email>
</corresp>
<fn><p><bold>Subject Categories</bold>
Protein Biosynthesis & Quality Control</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>14</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>24</day>
<month>8</month>
<year>2015</year>
</pub-date>
<volume>34</volume>
<issue>18</issue>
<fpage>2363</fpage>
<lpage>2382</lpage>
<history><date date-type="received"><day>10</day>
<month>2</month>
<year>2015</year>
</date>
<date date-type="rev-recd"><day>09</day>
<month>7</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>13</day>
<month>7</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>© 2015 The Authors</copyright-statement>
<copyright-year>2015</copyright-year>
</permissions>
<abstract><p>The aggresome is an organelle that recruits aggregated proteins for storage and degradation. We performed an siRNA screen for proteins involved in aggresome formation and identified novel mammalian AAA+ protein disaggregases RuvbL1 and RuvbL2. Depletion of RuvbL1 or RuvbL2 suppressed aggresome formation and caused buildup of multiple cytoplasmic aggregates. Similarly, downregulation of RuvbL orthologs in yeast suppressed the formation of an aggresome-like body and enhanced the aggregate toxicity. In contrast, their overproduction enhanced the resistance to proteotoxic stress independently of chaperone Hsp104. Mammalian RuvbL associated with the aggresome, and the aggresome substrate synphilin-1 interacted directly with the RuvbL1 barrel-like structure near the opening of the central channel. Importantly, polypeptides with unfolded structures and amyloid fibrils stimulated the ATPase activity of RuvbL. Finally, disassembly of protein aggregates was promoted by RuvbL. These data indicate that RuvbL complexes serve as chaperones in protein disaggregation.</p>
</abstract>
<kwd-group><kwd>aggresome</kwd>
<kwd>amyloid</kwd>
<kwd>disaggregation</kwd>
<kwd>RuvbL</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>
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