ALFY-Controlled DVL3 Autophagy Regulates Wnt Signaling, Determining Human Brain Size
Identifieur interne : 001486 ( Main/Exploration ); précédent : 001485; suivant : 001487ALFY-Controlled DVL3 Autophagy Regulates Wnt Signaling, Determining Human Brain Size
Auteurs : Rotem Kadir [Israël] ; Tamar Harel [Israël] ; Barak Markus [Israël] ; Yonatan Perez [Israël] ; Anna Bakhrat [Israël] ; Idan Cohen [Israël] ; Michael Volodarsky [Israël] ; Miora Feintsein-Linial [Israël] ; Elana Chervinski [Israël] ; Joel Zlotogora [Israël] ; Sara Sivan [Israël] ; Ramon Y. Birnbaum [Israël] ; Uri Abdu [Israël] ; Stavit Shalev [Israël] ; Ohad S. Birk [Israël]Source :
- PLoS Genetics [ 1553-7390 ] ; 2016.
Abstract
Primary microcephaly is a congenital neurodevelopmental disorder of reduced head circumference and brain volume, with fewer neurons in the cortex of the developing brain due to premature transition between symmetrical and asymmetrical cellular division of the neuronal stem cell layer during neurogenesis. We now show through linkage analysis and whole exome sequencing, that a dominant mutation in ALFY, encoding an autophagy scaffold protein, causes human primary microcephaly. We demonstrate the dominant effect of the mutation in drosophila: transgenic flies harboring the human mutant allele display small brain volume, recapitulating the disease phenotype. Moreover, eye-specific expression of human mutant ALFY causes rough eye phenotype. In molecular terms, we demonstrate that normally ALFY attenuates the canonical Wnt signaling pathway via autophagy-dependent removal specifically of aggregates of DVL3 and not of Dvl1 or Dvl2. Thus, autophagic attenuation of Wnt signaling through removal of Dvl3 aggregates by ALFY acts in determining human brain size.
Url:
DOI: 10.1371/journal.pgen.1005919
PubMed: 27008544
PubMed Central: 4805177
Affiliations:
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sort="Harel, Tamar" uniqKey="Harel T" first="Tamar" last="Harel">Tamar Harel</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Markus, Barak" sort="Markus, Barak" uniqKey="Markus B" first="Barak" last="Markus">Barak Markus</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Perez, Yonatan" sort="Perez, Yonatan" uniqKey="Perez Y" first="Yonatan" last="Perez">Yonatan Perez</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Bakhrat, Anna" sort="Bakhrat, Anna" uniqKey="Bakhrat A" first="Anna" last="Bakhrat">Anna Bakhrat</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Life Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Department of Life Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Cohen, Idan" sort="Cohen, Idan" uniqKey="Cohen I" first="Idan" last="Cohen">Idan Cohen</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Volodarsky, Michael" sort="Volodarsky, Michael" uniqKey="Volodarsky M" first="Michael" last="Volodarsky">Michael Volodarsky</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Feintsein Linial, Miora" sort="Feintsein Linial, Miora" uniqKey="Feintsein Linial M" first="Miora" last="Feintsein-Linial">Miora Feintsein-Linial</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Chervinski, Elana" sort="Chervinski, Elana" uniqKey="Chervinski E" first="Elana" last="Chervinski">Elana Chervinski</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Genetics Institute, HaEmek Medical Center, Afula, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Genetics Institute, HaEmek Medical Center, Afula</wicri:regionArea><wicri:noRegion>Afula</wicri:noRegion></affiliation></author><author><name sortKey="Zlotogora, Joel" sort="Zlotogora, Joel" uniqKey="Zlotogora J" first="Joel" last="Zlotogora">Joel Zlotogora</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Community Genetics, Public Health Services, Ministry of Health, Jerusalem, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Department of Community Genetics, Public Health Services, Ministry of Health, Jerusalem</wicri:regionArea><wicri:noRegion>Jerusalem</wicri:noRegion></affiliation></author><author><name sortKey="Sivan, Sara" sort="Sivan, Sara" uniqKey="Sivan S" first="Sara" last="Sivan">Sara Sivan</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Birnbaum, Ramon Y" sort="Birnbaum, Ramon Y" uniqKey="Birnbaum R" first="Ramon Y." last="Birnbaum">Ramon Y. Birnbaum</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Life Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Department of Life Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Abdu, Uri" sort="Abdu, Uri" uniqKey="Abdu U" first="Uri" last="Abdu">Uri Abdu</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Life Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Department of Life Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author><author><name sortKey="Shalev, Stavit" sort="Shalev, Stavit" uniqKey="Shalev S" first="Stavit" last="Shalev">Stavit Shalev</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Genetics Institute, HaEmek Medical Center, Afula, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Genetics Institute, HaEmek Medical Center, Afula</wicri:regionArea><wicri:noRegion>Afula</wicri:noRegion></affiliation></author><author><name sortKey="Birk, Ohad S" sort="Birk, Ohad S" uniqKey="Birk O" first="Ohad S." last="Birk">Ohad S. Birk</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>The Morris Kahn Laboratory of Human Genetics, National Institute for Biotechnology in the Negev and Faculty of Health Sciences, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Genetics Institute, Soroka University Medical Center, Ben Gurion University, Beer Sheva, Israel</addr-line></nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Genetics Institute, Soroka University Medical Center, Ben Gurion University, Beer Sheva</wicri:regionArea><wicri:noRegion>Beer Sheva</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS Genetics</title><idno type="ISSN">1553-7390</idno><idno type="eISSN">1553-7404</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Primary microcephaly is a congenital neurodevelopmental disorder of reduced head circumference and brain volume, with fewer neurons in the cortex of the developing brain due to premature transition between symmetrical and asymmetrical cellular division of the neuronal stem cell layer during neurogenesis. We now show through linkage analysis and whole exome sequencing, that a dominant mutation in ALFY, encoding an autophagy scaffold protein, causes human primary microcephaly. We demonstrate the dominant effect of the mutation in drosophila: transgenic flies harboring the human mutant allele display small brain volume, recapitulating the disease phenotype. Moreover, eye-specific expression of human mutant ALFY causes rough eye phenotype. In molecular terms, we demonstrate that normally ALFY attenuates the canonical Wnt signaling pathway via autophagy-dependent removal specifically of aggregates of DVL3 and not of Dvl1 or Dvl2. Thus, autophagic attenuation of Wnt signaling through removal of Dvl3 aggregates by ALFY acts in determining human brain size.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Mahmood, S" uniqKey="Mahmood S">S Mahmood</name></author><author><name sortKey="Ahmad, W" uniqKey="Ahmad W">W Ahmad</name></author><author><name sortKey="Hassan, Mj" uniqKey="Hassan M">MJ Hassan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gilmore, Ec" uniqKey="Gilmore E">EC Gilmore</name></author><author><name sortKey="Walsh, Ca" uniqKey="Walsh C">CA Walsh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fish, Jl" uniqKey="Fish J">JL Fish</name></author><author><name sortKey="Dehay, C" uniqKey="Dehay C">C Dehay</name></author><author><name sortKey="Kennedy, H" uniqKey="Kennedy H">H Kennedy</name></author><author><name sortKey="Huttner, Wb" uniqKey="Huttner W">WB 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Flusser</name></author><author><name sortKey="Ofir, R" uniqKey="Ofir R">R Ofir</name></author><author><name sortKey="Shelef, I" uniqKey="Shelef I">I Shelef</name></author><author><name sortKey="Narkis, G" uniqKey="Narkis G">G Narkis</name></author><author><name sortKey="Vardi, G" uniqKey="Vardi G">G Vardi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Perez, Y" uniqKey="Perez Y">Y Perez</name></author><author><name sortKey="Gradstein, L" uniqKey="Gradstein L">L Gradstein</name></author><author><name sortKey="Flusser, H" uniqKey="Flusser H">H Flusser</name></author><author><name sortKey="Markus, B" uniqKey="Markus B">B Markus</name></author><author><name sortKey="Cohen, I" uniqKey="Cohen I">I Cohen</name></author><author><name sortKey="Langer, Y" uniqKey="Langer Y">Y Langer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pfeiffer, Bd" uniqKey="Pfeiffer B">BD Pfeiffer</name></author><author><name sortKey="Ngo, Tt" uniqKey="Ngo T">TT Ngo</name></author><author><name sortKey="Hibbard, Kl" uniqKey="Hibbard K">KL Hibbard</name></author><author><name sortKey="Murphy, C" uniqKey="Murphy C">C Murphy</name></author><author><name sortKey="Jenett, A" uniqKey="Jenett A">A Jenett</name></author><author><name sortKey="Truman, Jw" uniqKey="Truman J">JW Truman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brand, Ah" uniqKey="Brand A">AH Brand</name></author><author><name sortKey="Perrimon, N" uniqKey="Perrimon N">N Perrimon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jenett, A" uniqKey="Jenett A">A Jenett</name></author><author><name sortKey="Rubin, Gm" uniqKey="Rubin G">GM Rubin</name></author><author><name sortKey="Ngo, Tt" uniqKey="Ngo T">TT Ngo</name></author><author><name sortKey="Shepherd, D" uniqKey="Shepherd D">D Shepherd</name></author><author><name sortKey="Murphy, C" uniqKey="Murphy C">C Murphy</name></author><author><name sortKey="Dionne, H" uniqKey="Dionne H">H Dionne</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Chaumont, F" uniqKey="De Chaumont F">F de Chaumont</name></author><author><name sortKey="Dallongeville, S" uniqKey="Dallongeville S">S Dallongeville</name></author><author><name sortKey="Chenouard, N" uniqKey="Chenouard N">N Chenouard</name></author><author><name sortKey="Herve, N" uniqKey="Herve N">N Herve</name></author><author><name sortKey="Pop, S" uniqKey="Pop S">S Pop</name></author><author><name sortKey="Provoost, T" uniqKey="Provoost T">T Provoost</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Israël</li></country></list><tree><country name="Israël"><noRegion><name sortKey="Kadir, Rotem" sort="Kadir, Rotem" uniqKey="Kadir R" first="Rotem" last="Kadir">Rotem Kadir</name></noRegion><name sortKey="Abdu, Uri" sort="Abdu, Uri" uniqKey="Abdu U" first="Uri" last="Abdu">Uri Abdu</name><name sortKey="Bakhrat, Anna" sort="Bakhrat, Anna" uniqKey="Bakhrat A" first="Anna" last="Bakhrat">Anna Bakhrat</name><name sortKey="Birk, Ohad S" sort="Birk, Ohad S" uniqKey="Birk O" first="Ohad S." last="Birk">Ohad S. Birk</name><name sortKey="Birk, Ohad S" sort="Birk, Ohad S" uniqKey="Birk O" first="Ohad S." last="Birk">Ohad S. Birk</name><name sortKey="Birnbaum, Ramon Y" sort="Birnbaum, Ramon Y" uniqKey="Birnbaum R" first="Ramon Y." last="Birnbaum">Ramon Y. Birnbaum</name><name sortKey="Chervinski, Elana" sort="Chervinski, Elana" uniqKey="Chervinski E" first="Elana" last="Chervinski">Elana Chervinski</name><name sortKey="Cohen, Idan" sort="Cohen, Idan" uniqKey="Cohen I" first="Idan" last="Cohen">Idan Cohen</name><name sortKey="Feintsein Linial, Miora" sort="Feintsein Linial, Miora" uniqKey="Feintsein Linial M" first="Miora" last="Feintsein-Linial">Miora Feintsein-Linial</name><name sortKey="Harel, Tamar" sort="Harel, Tamar" uniqKey="Harel T" first="Tamar" last="Harel">Tamar Harel</name><name sortKey="Markus, Barak" sort="Markus, Barak" uniqKey="Markus B" first="Barak" last="Markus">Barak Markus</name><name sortKey="Perez, Yonatan" sort="Perez, Yonatan" uniqKey="Perez Y" first="Yonatan" last="Perez">Yonatan Perez</name><name sortKey="Shalev, Stavit" sort="Shalev, Stavit" uniqKey="Shalev S" first="Stavit" last="Shalev">Stavit Shalev</name><name sortKey="Sivan, Sara" sort="Sivan, Sara" uniqKey="Sivan S" first="Sara" last="Sivan">Sara Sivan</name><name sortKey="Volodarsky, Michael" sort="Volodarsky, Michael" uniqKey="Volodarsky M" first="Michael" last="Volodarsky">Michael Volodarsky</name><name sortKey="Zlotogora, Joel" sort="Zlotogora, Joel" uniqKey="Zlotogora J" first="Joel" last="Zlotogora">Joel Zlotogora</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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