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Cytoplasmic NOTCH and membrane-derived β-catenin link cell fate choice to epithelial-mesenchymal transition during myogenesis

Identifieur interne : 003591 ( Ncbi/Merge ); précédent : 003590; suivant : 003592

Cytoplasmic NOTCH and membrane-derived β-catenin link cell fate choice to epithelial-mesenchymal transition during myogenesis

Auteurs : Daniel Sieiro [Australie, France] ; Anne C. Rios [Australie] ; Claire E. Hirst [Australie] ; Christophe Marcelle [Australie, France]

Source :

RBID : PMC:4917337

Abstract

How cells in the embryo coordinate epithelial plasticity with cell fate decision in a fast changing cellular environment is largely unknown. In chick embryos, skeletal muscle formation is initiated by migrating Delta1-expressing neural crest cells that trigger NOTCH signaling and myogenesis in selected epithelial somite progenitor cells, which rapidly translocate into the nascent muscle to differentiate. Here, we uncovered at the heart of this response a signaling module encompassing NOTCH, GSK-3β, SNAI1 and β-catenin. Independent of its transcriptional function, NOTCH profoundly inhibits GSK-3β activity. As a result SNAI1 is stabilized, triggering an epithelial to mesenchymal transition. This allows the recruitment of β-catenin from the membrane, which acts as a transcriptional co-factor to activate myogenesis, independently of WNT ligand. Our results intimately associate the initiation of myogenesis to a change in cell adhesion and may reveal a general principle for coupling cell fate changes to EMT in many developmental and pathological processes.

DOI:http://dx.doi.org/10.7554/eLife.14847.001


Url:
DOI: 10.7554/eLife.14847
PubMed: 27218451
PubMed Central: 4917337

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PMC:4917337

Le document en format XML

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<institution content-type="dept">Australian Regenerative Medicine Institute</institution>
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<addr-line>Clayton</addr-line>
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<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name>
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<institution content-type="dept">Australian Regenerative Medicine Institute</institution>
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<institution>Monash University</institution>
,
<addr-line>Clayton</addr-line>
,
<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<affiliation wicri:level="1">
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<institution content-type="dept">Institut NeuroMyoGene</institution>
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<institution>University Lyon 1, CNRS UMR 5310, INSERM U 1217</institution>
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<addr-line>Villeurbanne</addr-line>
,
<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author>
<name sortKey="Rios, Anne C" sort="Rios, Anne C" uniqKey="Rios A" first="Anne C" last="Rios">Anne C. Rios</name>
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<institution content-type="dept">Australian Regenerative Medicine Institute</institution>
,
<institution>Monash University</institution>
,
<addr-line>Clayton</addr-line>
,
<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<name sortKey="Hirst, Claire E" sort="Hirst, Claire E" uniqKey="Hirst C" first="Claire E" last="Hirst">Claire E. Hirst</name>
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<institution content-type="dept">Australian Regenerative Medicine Institute</institution>
,
<institution>Monash University</institution>
,
<addr-line>Clayton</addr-line>
,
<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author>
<name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name>
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<nlm:aff id="aff1">
<institution content-type="dept">Australian Regenerative Medicine Institute</institution>
,
<institution>Monash University</institution>
,
<addr-line>Clayton</addr-line>
,
<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="aff2">
<institution content-type="dept">Institut NeuroMyoGene</institution>
,
<institution>University Lyon 1, CNRS UMR 5310, INSERM U 1217</institution>
,
<addr-line>Villeurbanne</addr-line>
,
<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<series>
<title level="j">eLife</title>
<idno type="eISSN">2050-084X</idno>
<imprint>
<date when="????">????</date>
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<div type="abstract" xml:lang="en">
<p>How cells in the embryo coordinate epithelial plasticity with cell fate decision in a fast changing cellular environment is largely unknown. In chick embryos, skeletal muscle formation is initiated by migrating Delta1-expressing neural crest cells that trigger NOTCH signaling and myogenesis in selected epithelial somite progenitor cells, which rapidly translocate into the nascent muscle to differentiate. Here, we uncovered at the heart of this response a signaling module encompassing NOTCH, GSK-3β, SNAI1 and β-catenin. Independent of its transcriptional function, NOTCH profoundly inhibits GSK-3β activity. As a result SNAI1 is stabilized, triggering an epithelial to mesenchymal transition. This allows the recruitment of β-catenin from the membrane, which acts as a transcriptional co-factor to activate myogenesis, independently of WNT ligand. Our results intimately associate the initiation of myogenesis to a change in cell adhesion and may reveal a general principle for coupling cell fate changes to EMT in many developmental and pathological processes.</p>
<p>
<bold>DOI:</bold>
<ext-link ext-link-type="doi" xlink:href="10.7554/eLife.14847.001">http://dx.doi.org/10.7554/eLife.14847.001</ext-link>
</p>
</div>
</front>
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<name sortKey="Xia, W" uniqKey="Xia W">W Xia</name>
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<name sortKey="Xu, J" uniqKey="Xu J">J Xu</name>
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<name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name>
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<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
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<author>
<name sortKey="Rios, Anne C" sort="Rios, Anne C" uniqKey="Rios A" first="Anne C" last="Rios">Anne C. Rios</name>
<affiliation wicri:level="1">
<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
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<author>
<name sortKey="Hirst, Claire E" sort="Hirst, Claire E" uniqKey="Hirst C" first="Claire E" last="Hirst">Claire E. Hirst</name>
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<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
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</author>
<author>
<name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name>
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<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
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<date when="2016">2016</date>
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<idno type="pmid">27218451</idno>
<idno type="doi">10.7554/eLife.14847</idno>
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<title xml:lang="en">Cytoplasmic NOTCH and membrane-derived β-catenin link cell fate choice to epithelial-mesenchymal transition during myogenesis.</title>
<author>
<name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name>
<affiliation wicri:level="1">
<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Rios, Anne C" sort="Rios, Anne C" uniqKey="Rios A" first="Anne C" last="Rios">Anne C. Rios</name>
<affiliation wicri:level="1">
<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Hirst, Claire E" sort="Hirst, Claire E" uniqKey="Hirst C" first="Claire E" last="Hirst">Claire E. Hirst</name>
<affiliation wicri:level="1">
<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name>
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<nlm:affiliation>Australian Regenerative Medicine Institute, Monash University, Clayton, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton</wicri:regionArea>
<wicri:noRegion>Clayton</wicri:noRegion>
</affiliation>
</author>
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<series>
<title level="j">eLife</title>
<idno type="eISSN">2050-084X</idno>
<imprint>
<date when="2016" type="published">2016</date>
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<front>
<div type="abstract" xml:lang="en">How cells in the embryo coordinate epithelial plasticity with cell fate decision in a fast changing cellular environment is largely unknown. In chick embryos, skeletal muscle formation is initiated by migrating Delta1-expressing neural crest cells that trigger NOTCH signaling and myogenesis in selected epithelial somite progenitor cells, which rapidly translocate into the nascent muscle to differentiate. Here, we uncovered at the heart of this response a signaling module encompassing NOTCH, GSK-3β, SNAI1 and β-catenin. Independent of its transcriptional function, NOTCH profoundly inhibits GSK-3β activity. As a result SNAI1 is stabilized, triggering an epithelial to mesenchymal transition. This allows the recruitment of β-catenin from the membrane, which acts as a transcriptional co-factor to activate myogenesis, independently of WNT ligand. Our results intimately associate the initiation of myogenesis to a change in cell adhesion and may reveal a general principle for coupling cell fate changes to EMT in many developmental and pathological processes.</div>
</front>
</TEI>
</pubmed>
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