Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures
Identifieur interne : 001946 ( Pmc/Checkpoint ); précédent : 001945; suivant : 001947Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures
Auteurs : Benedetta Cerruti ; Alberto Puliafito ; Annette M. Shewan ; Wei Yu ; Alexander N. Combes ; Melissa H. Little ; Federica Chianale ; Luca Primo ; Guido Serini ; Keith E. Mostov ; Antonio Celani ; Andrea GambaSource :
- The Journal of Cell Biology [ 0021-9525 ] ; 2013.
Abstract
Mathematical modeling and analysis of 3D epithelial structures indicate that epithelial growth can take place far from mechanical equilibrium, depending on cell–cell and cell–ECM contact, cell division, cortical contractility, and cell motility.
Url:
DOI: 10.1083/jcb.201305044
PubMed: 24145168
PubMed Central: 3812962
Affiliations:
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Shewan</name><affiliation><nlm:aff wicri:cut=" and" id="aff2"><institution>School of Chemistry and Molecular Biosciences</institution></nlm:aff></affiliation></author><author><name sortKey="Yu, Wei" sort="Yu, Wei" uniqKey="Yu W" first="Wei" last="Yu">Wei Yu</name><affiliation><nlm:aff id="aff3"><institution>Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143</institution></nlm:aff></affiliation></author><author><name sortKey="Combes, Alexander N" sort="Combes, Alexander N" uniqKey="Combes A" first="Alexander N." last="Combes">Alexander N. Combes</name><affiliation><nlm:aff id="aff2"><institution>Institute for Molecular Bioscience, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia</institution></nlm:aff></affiliation></author><author><name sortKey="Little, Melissa H" sort="Little, Melissa H" uniqKey="Little M" first="Melissa H." last="Little">Melissa H. Little</name><affiliation><nlm:aff id="aff2"><institution>Institute for Molecular Bioscience, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia</institution></nlm:aff></affiliation></author><author><name sortKey="Chianale, Federica" sort="Chianale, Federica" uniqKey="Chianale F" first="Federica" last="Chianale">Federica Chianale</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Primo, Luca" sort="Primo, Luca" uniqKey="Primo L" first="Luca" last="Primo">Luca Primo</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>University of Torino, Torino 10124, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Serini, Guido" sort="Serini, Guido" uniqKey="Serini G" first="Guido" last="Serini">Guido Serini</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>University of Torino, Torino 10124, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Mostov, Keith E" sort="Mostov, Keith E" uniqKey="Mostov K" first="Keith E." last="Mostov">Keith E. 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Shewan</name><affiliation><nlm:aff wicri:cut=" and" id="aff2"><institution>School of Chemistry and Molecular Biosciences</institution></nlm:aff></affiliation></author><author><name sortKey="Yu, Wei" sort="Yu, Wei" uniqKey="Yu W" first="Wei" last="Yu">Wei Yu</name><affiliation><nlm:aff id="aff3"><institution>Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143</institution></nlm:aff></affiliation></author><author><name sortKey="Combes, Alexander N" sort="Combes, Alexander N" uniqKey="Combes A" first="Alexander N." last="Combes">Alexander N. Combes</name><affiliation><nlm:aff id="aff2"><institution>Institute for Molecular Bioscience, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia</institution></nlm:aff></affiliation></author><author><name sortKey="Little, Melissa H" sort="Little, Melissa H" uniqKey="Little M" first="Melissa H." last="Little">Melissa H. Little</name><affiliation><nlm:aff id="aff2"><institution>Institute for Molecular Bioscience, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia</institution></nlm:aff></affiliation></author><author><name sortKey="Chianale, Federica" sort="Chianale, Federica" uniqKey="Chianale F" first="Federica" last="Chianale">Federica Chianale</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Primo, Luca" sort="Primo, Luca" uniqKey="Primo L" first="Luca" last="Primo">Luca Primo</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>University of Torino, Torino 10124, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Serini, Guido" sort="Serini, Guido" uniqKey="Serini G" first="Guido" last="Serini">Guido Serini</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>University of Torino, Torino 10124, Italy</institution></nlm:aff></affiliation></author><author><name sortKey="Mostov, Keith E" sort="Mostov, Keith E" uniqKey="Mostov K" first="Keith E." last="Mostov">Keith E. Mostov</name><affiliation><nlm:aff id="aff3"><institution>Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143</institution></nlm:aff></affiliation></author><author><name sortKey="Celani, Antonio" sort="Celani, Antonio" uniqKey="Celani A" first="Antonio" last="Celani">Antonio Celani</name><affiliation><nlm:aff id="aff5"><institution>Unit “Physics of Biological Systems,” Institut Pasteur, Centre National de la Recherche Scientifique URA 2171, Paris F-75015, France</institution></nlm:aff></affiliation></author><author><name sortKey="Gamba, Andrea" sort="Gamba, Andrea" uniqKey="Gamba A" first="Andrea" last="Gamba">Andrea Gamba</name><affiliation><nlm:aff id="aff1"><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff7"><institution>Department of Applied Science and Technology, Politecnico di Torino, Torino 10129, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff8"><institution>Istituto Nazionale di Fisica Nucleare (INFN), Torino 10125, Italy</institution></nlm:aff></affiliation><affiliation><nlm:aff id="aff9"><institution>Human Genetics Foundation, Torino 10126, Italy</institution></nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Cell Biology</title><idno type="ISSN">0021-9525</idno><idno type="eISSN">1540-8140</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Mathematical modeling and analysis of 3D epithelial structures indicate that epithelial growth can take place far from mechanical equilibrium, depending on cell–cell and cell–ECM contact, cell division, cortical contractility, and cell motility.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Amonlirdviman, K" uniqKey="Amonlirdviman K">K. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Cell Biol</journal-id><journal-id journal-id-type="iso-abbrev">J. Cell Biol</journal-id><journal-id journal-id-type="hwp">jcb</journal-id><journal-title-group><journal-title>The Journal of Cell Biology</journal-title></journal-title-group><issn pub-type="ppub">0021-9525</issn><issn pub-type="epub">1540-8140</issn><publisher><publisher-name>The Rockefeller University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24145168</article-id><article-id pub-id-type="pmc">3812962</article-id><article-id pub-id-type="publisher-id">201305044</article-id><article-id pub-id-type="doi">10.1083/jcb.201305044</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Articles</subject><subj-group><subject>Article</subject></subj-group></subj-group></article-categories><title-group><article-title>Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures</article-title><alt-title alt-title-type="short">Out-of-equilibrium epithelial growth</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Cerruti</surname><given-names>Benedetta</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff6">7</xref></contrib><contrib contrib-type="author"><name><surname>Puliafito</surname><given-names>Alberto</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Shewan</surname><given-names>Annette M.</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Yu</surname><given-names>Wei</given-names></name><xref ref-type="aff" rid="aff3">4</xref></contrib><contrib contrib-type="author"><name><surname>Combes</surname><given-names>Alexander N.</given-names></name><xref ref-type="aff" rid="aff2">3</xref></contrib><contrib contrib-type="author"><name><surname>Little</surname><given-names>Melissa H.</given-names></name><xref ref-type="aff" rid="aff2">3</xref></contrib><contrib contrib-type="author"><name><surname>Chianale</surname><given-names>Federica</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Primo</surname><given-names>Luca</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">5</xref></contrib><contrib contrib-type="author"><name><surname>Serini</surname><given-names>Guido</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">5</xref></contrib><contrib contrib-type="author"><name><surname>Mostov</surname><given-names>Keith E.</given-names></name><xref ref-type="aff" rid="aff3">4</xref></contrib><contrib contrib-type="author"><name><surname>Celani</surname><given-names>Antonio</given-names></name><xref ref-type="aff" rid="aff5">6</xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Gamba</surname><given-names>Andrea</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff7">8</xref><xref ref-type="aff" rid="aff8">9</xref><xref ref-type="aff" rid="aff9">10</xref></contrib></contrib-group><aff id="aff1"><label>1</label><institution>Institute for Cancer Research and Treatment (IRCC), Candiolo 10060, Italy</institution></aff><aff id="aff2"><label>2</label><institution>School of Chemistry and Molecular Biosciences</institution> and<label>3</label><institution>Institute for Molecular Bioscience, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia</institution></aff><aff id="aff3"><label>4</label><institution>Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143</institution></aff><aff id="aff4"><label>5</label><institution>University of Torino, Torino 10124, Italy</institution></aff><aff id="aff5"><label>6</label><institution>Unit “Physics of Biological Systems,” Institut Pasteur, Centre National de la Recherche Scientifique URA 2171, Paris F-75015, France</institution></aff><aff id="aff6"><label>7</label><institution>Dipartimento di Fisica, Università di Roma “La Sapienza,” Rome 00185, Italy</institution></aff><aff id="aff7"><label>8</label><institution>Department of Applied Science and Technology, Politecnico di Torino, Torino 10129, Italy</institution></aff><aff id="aff8"><label>9</label><institution>Istituto Nazionale di Fisica Nucleare (INFN), Torino 10125, Italy</institution></aff><aff id="aff9"><label>10</label><institution>Human Genetics Foundation, Torino 10126, Italy</institution></aff><author-notes><corresp>Correspondence to Andrea Gamba: <email>andrea.gamba@ircc.it</email></corresp><fn><p>Benedetta Cerruti and Alberto Puliafito contributed equally to this paper.</p></fn><fn><p>Keith E. Mostov, Antonio Celani, and Andrea Gamba contributed equally to this paper.</p></fn></author-notes><pub-date pub-type="ppub"><day>28</day><month>10</month><year>2013</year></pub-date><volume>203</volume><issue>2</issue><fpage>359</fpage><lpage>372</lpage><history><date date-type="received"><day>9</day><month>5</month><year>2013</year></date><date date-type="accepted"><day>22</day><month>9</month><year>2013</year></date></history><permissions><copyright-statement>© 2013 Cerruti et al.</copyright-statement><copyright-year>2013</copyright-year><license license-type="openaccess"><license-p>This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see <ext-link ext-link-type="uri" xlink:href="http://www.rupress.org/terms">http://www.rupress.org/terms</ext-link>). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>).</license-p></license></permissions><self-uri xlink:role="icon" xlink:type="simple" xlink:href="JCB_201305044_thumb.gif"></self-uri><abstract abstract-type="precis"><p>Mathematical modeling and analysis of 3D epithelial structures indicate that epithelial growth can take place far from mechanical equilibrium, depending on cell–cell and cell–ECM contact, cell division, cortical contractility, and cell motility.</p></abstract><abstract><p>The growth of a well-formed epithelial structure is governed by mechanical constraints, cellular apico-basal polarity, and spatially controlled cell division. Here we compared the predictions of a mathematical model of epithelial growth with the morphological analysis of 3D epithelial structures. In both in vitro cyst models and in developing epithelial structures in vivo, epithelial growth could take place close to or far from mechanical equilibrium, and was determined by the hierarchy of time-scales of cell division, cell–cell rearrangements, and lumen dynamics. Equilibrium properties could be inferred by the analysis of cell–cell contact topologies, and the nonequilibrium phenotype was altered by inhibiting ROCK activity. The occurrence of an aberrant multilumen phenotype was linked to fast nonequilibrium growth, even when geometric control of cell division was correctly enforced. We predicted and verified experimentally that slowing down cell division partially rescued a multilumen phenotype induced by altered polarity. These results improve our understanding of the development of epithelial organs and, ultimately, of carcinogenesis.</p></abstract></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Celani, Antonio" sort="Celani, Antonio" uniqKey="Celani A" first="Antonio" last="Celani">Antonio Celani</name><name sortKey="Cerruti, Benedetta" sort="Cerruti, Benedetta" uniqKey="Cerruti B" first="Benedetta" last="Cerruti">Benedetta Cerruti</name><name sortKey="Chianale, Federica" sort="Chianale, Federica" uniqKey="Chianale F" first="Federica" last="Chianale">Federica Chianale</name><name sortKey="Combes, Alexander N" sort="Combes, Alexander N" uniqKey="Combes A" first="Alexander N." last="Combes">Alexander N. Combes</name><name sortKey="Gamba, Andrea" sort="Gamba, Andrea" uniqKey="Gamba A" first="Andrea" last="Gamba">Andrea Gamba</name><name sortKey="Little, Melissa H" sort="Little, Melissa H" uniqKey="Little M" first="Melissa H." last="Little">Melissa H. Little</name><name sortKey="Mostov, Keith E" sort="Mostov, Keith E" uniqKey="Mostov K" first="Keith E." last="Mostov">Keith E. Mostov</name><name sortKey="Primo, Luca" sort="Primo, Luca" uniqKey="Primo L" first="Luca" last="Primo">Luca Primo</name><name sortKey="Puliafito, Alberto" sort="Puliafito, Alberto" uniqKey="Puliafito A" first="Alberto" last="Puliafito">Alberto Puliafito</name><name sortKey="Serini, Guido" sort="Serini, Guido" uniqKey="Serini G" first="Guido" last="Serini">Guido Serini</name><name sortKey="Shewan, Annette M" sort="Shewan, Annette M" uniqKey="Shewan A" first="Annette M." last="Shewan">Annette M. Shewan</name><name sortKey="Yu, Wei" sort="Yu, Wei" uniqKey="Yu W" first="Wei" last="Yu">Wei Yu</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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