The chicken embryo as an efficient model to test the function of muscle fusion genes in amniotes
Identifieur interne : 000051 ( Pmc/Checkpoint ); précédent : 000050; suivant : 000052The chicken embryo as an efficient model to test the function of muscle fusion genes in amniotes
Auteurs : Daniel Sieiro [Australie, France] ; Nadège Véron [Australie] ; Christophe Marcelle [Australie, France]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
The fusion of myoblasts into multinucleated myotubes is a crucial step of muscle growth during development and of muscle repair in the adult. While multiple genes were shown to play a role in this process, a vertebrate model where novel candidates can be tested and analyzed at high throughput and relative ease has been lacking. Here, we show that the early chicken embryo is a fast and robust model in which functional testing of muscle fusion candidate genes can be performed. We have used known modulators of muscle fusion, Rac1 and Cdc42, along with the
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DOI: 10.1371/journal.pone.0177681
PubMed: 28520772
PubMed Central: 5433753
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last="Marcelle">Christophe Marcelle</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon</wicri:regionArea><placeName><region type="region">Auvergne-Rhône-Alpes</region><region type="old region">Rhône-Alpes</region><settlement type="city">Lyon</settlement><settlement type="city">Lyon</settlement></placeName><orgName type="university">Université Claude Bernard Lyon 1</orgName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28520772</idno><idno type="pmc">5433753</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433753</idno><idno type="RBID">PMC:5433753</idno><idno type="doi">10.1371/journal.pone.0177681</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">002979</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002979</idno><idno type="wicri:Area/Pmc/Curation">002829</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002829</idno><idno type="wicri:Area/Pmc/Checkpoint">000051</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000051</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The chicken embryo as an efficient model to test the function of muscle fusion genes in amniotes</title><author><name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon</wicri:regionArea><placeName><region type="region">Auvergne-Rhône-Alpes</region><region type="old region">Rhône-Alpes</region><settlement type="city">Lyon</settlement><settlement type="city">Lyon</settlement></placeName><orgName type="university">Université Claude Bernard Lyon 1</orgName></affiliation></author><author><name sortKey="Veron, Nadege" sort="Veron, Nadege" uniqKey="Veron N" first="Nadège" last="Véron">Nadège Véron</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon</wicri:regionArea><placeName><region type="region">Auvergne-Rhône-Alpes</region><region type="old region">Rhône-Alpes</region><settlement type="city">Lyon</settlement><settlement type="city">Lyon</settlement></placeName><orgName type="university">Université Claude Bernard Lyon 1</orgName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The fusion of myoblasts into multinucleated myotubes is a crucial step of muscle growth during development and of muscle repair in the adult. While multiple genes were shown to play a role in this process, a vertebrate model where novel candidates can be tested and analyzed at high throughput and relative ease has been lacking. Here, we show that the early chicken embryo is a fast and robust model in which functional testing of muscle fusion candidate genes can be performed. We have used known modulators of muscle fusion, Rac1 and Cdc42, along with the <italic>in vivo</italic> electroporation of integrated, inducible vectors, to show that the chicken embryo is a suitable model in which their function can be tested and quantified. In addition to nuclei content, specific characteristics of the experimental model allow a fine characterization of additional morphological features that are nearly impossible to assess in other model organisms. This study should establish the chicken embryo as a cheap, reliable and powerful model in which novel vertebrate muscle fusion candidates can be evaluated.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Pavlath, Gk" uniqKey="Pavlath G">GK Pavlath</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Abmayr, S" uniqKey="Abmayr S">S Abmayr</name></author><author><name sortKey="Pavlath, G" uniqKey="Pavlath G">G Pavlath</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rochlin, K" uniqKey="Rochlin K">K Rochlin</name></author><author><name sortKey="Yu, S" uniqKey="Yu S">S Yu</name></author><author><name sortKey="Roy, S" uniqKey="Roy S">S Roy</name></author><author><name sortKey="Baylies, M" uniqKey="Baylies M">M Baylies</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kim, Jh" uniqKey="Kim J">JH Kim</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28520772</article-id><article-id pub-id-type="pmc">5433753</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0177681</article-id><article-id pub-id-type="publisher-id">PONE-D-17-02227</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cell Physiology</subject><subj-group><subject>Cell Fusion</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Developmental Biology</subject><subj-group><subject>Embryology</subject><subj-group><subject>Embryos</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Bioassays and Physiological Analysis</subject><subj-group><subject>Muscle Analysis</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Developmental Biology</subject><subj-group><subject>Organism Development</subject><subj-group><subject>Organogenesis</subject><subj-group><subject>Somites</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Muscle Physiology</subject><subj-group><subject>Muscle Functions</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Muscle Physiology</subject><subj-group><subject>Muscle Functions</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Types</subject><subj-group><subject>Animal Cells</subject><subj-group><subject>Muscle Fibers</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Musculoskeletal System</subject><subj-group><subject>Muscles</subject><subj-group><subject>Muscle Fibers</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Musculoskeletal System</subject><subj-group><subject>Muscles</subject><subj-group><subject>Muscle Fibers</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Specimen Preparation and Treatment</subject><subj-group><subject>Mechanical Treatment of Specimens</subject><subj-group><subject>Specimen Disruption</subject><subj-group><subject>Electroporation</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Structures and Organelles</subject><subj-group><subject>Cell Membranes</subject><subj-group><subject>Membrane Fusion</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>The chicken embryo as an efficient model to test the function of muscle fusion genes in amniotes</article-title><alt-title alt-title-type="running-head">Testing muscle fusion in chicken embryo</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Sieiro</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Véron</surname><given-names>Nadège</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9612-7609</contrib-id><name><surname>Marcelle</surname><given-names>Christophe</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, Victoria, Australia</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Institut NeuroMyoGène (INMG), Université Claude Bernard Lyon1, Faculty of Medicine Laënnec, Lyon, France</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Asakura</surname><given-names>Atsushi</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of Minnesota Medical Center, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> CM DS.</p></list-item><list-item><p><bold>Formal analysis:</bold> DS CM.</p></list-item><list-item><p><bold>Funding acquisition:</bold> CM.</p></list-item><list-item><p><bold>Investigation:</bold> NV DS.</p></list-item><list-item><p><bold>Methodology:</bold> CM DS NV.</p></list-item><list-item><p><bold>Project administration:</bold> CM.</p></list-item><list-item><p><bold>Resources:</bold> CM.</p></list-item><list-item><p><bold>Supervision:</bold> CM.</p></list-item><list-item><p><bold>Validation:</bold> CM NV DS.</p></list-item><list-item><p><bold>Visualization:</bold> DS.</p></list-item><list-item><p><bold>Writing – original draft:</bold> CM DS.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> CM DS.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>christophe.marcelle@monash.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>16</day><month>5</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>5</issue><elocation-id>e0177681</elocation-id><history><date date-type="received"><day>8</day><month>2</month><year>2017</year></date><date date-type="accepted"><day>30</day><month>4</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Sieiro et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Sieiro et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0177681.pdf"></self-uri><abstract><p>The fusion of myoblasts into multinucleated myotubes is a crucial step of muscle growth during development and of muscle repair in the adult. While multiple genes were shown to play a role in this process, a vertebrate model where novel candidates can be tested and analyzed at high throughput and relative ease has been lacking. Here, we show that the early chicken embryo is a fast and robust model in which functional testing of muscle fusion candidate genes can be performed. We have used known modulators of muscle fusion, Rac1 and Cdc42, along with the <italic>in vivo</italic> electroporation of integrated, inducible vectors, to show that the chicken embryo is a suitable model in which their function can be tested and quantified. In addition to nuclei content, specific characteristics of the experimental model allow a fine characterization of additional morphological features that are nearly impossible to assess in other model organisms. This study should establish the chicken embryo as a cheap, reliable and powerful model in which novel vertebrate muscle fusion candidates can be evaluated.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000925</institution-id><institution>National Health and Medical Research Council</institution></institution-wrap></funding-source><award-id>APP1087743</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9612-7609</contrib-id><name><surname>Marcelle</surname><given-names>Christophe</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution>Programme Avenir Lyon St Etienne</institution></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9612-7609</contrib-id><name><surname>Marcelle</surname><given-names>Christophe</given-names></name></principal-award-recipient></award-group><funding-statement>This work was supported by grants from the National Health and Medical Research Council (NHMRC, Australia) to C.M. and N.V. and by the Programme Avenir Lyon Saint-Etienne (PALSE) from the University of Lyon to C.M. and D.S. The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government. The NeuroMyoGene Institute is supported by grants from the Association Française contre les Myopathies (AFM).</funding-statement></funding-group><counts><fig-count count="4"></fig-count><table-count count="0"></table-count><page-count count="13"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc><affiliations><list><country><li>Australie</li><li>France</li></country><region><li>Auvergne-Rhône-Alpes</li><li>Rhône-Alpes</li></region><settlement><li>Lyon</li></settlement><orgName><li>Université Claude Bernard Lyon 1</li></orgName></list><tree><country name="Australie"><noRegion><name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name></noRegion><name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name><name sortKey="Veron, Nadege" sort="Veron, Nadege" uniqKey="Veron N" first="Nadège" last="Véron">Nadège Véron</name></country><country name="France"><region name="Auvergne-Rhône-Alpes"><name sortKey="Sieiro, Daniel" sort="Sieiro, Daniel" uniqKey="Sieiro D" first="Daniel" last="Sieiro">Daniel Sieiro</name></region><name sortKey="Marcelle, Christophe" sort="Marcelle, Christophe" uniqKey="Marcelle C" first="Christophe" last="Marcelle">Christophe Marcelle</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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