Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling

During epithelial contraction, cells generate forces to constrict their surface and, concurrently, fine-tune the length of their adherens junctions to ensure force transmission. While many studies have focused on understanding force generation, little is known on how junctional length is controlled....

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Authors: Sumi, Angughali Aheto, 1986-, Hayes, D. Peran, 1983-, D'Angelo, Arturo, Colombelli, Julien, Salbreux, Guillaume, Dierkes, Kai, Solon, Jérôme
Format: article
Status:Published version
Publication Date:2018
Country:España
Institution:Universitat Pompeu Fabra
Repository:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/42836
Online Access:http://hdl.handle.net/10230/42836
http://dx.doi.org/10.1016/j.devcel.2018.10.025
Access Level:Open access
Keyword:Drosophila dorsal closure
E-cadherin
Actomyosin cytoskeleton
Adherens junction
Biophysical modeling
Endocytosis
Epithelial contraction
Morphogenesis
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spelling Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recyclingSumi, Angughali Aheto, 1986-Hayes, D. Peran, 1983-D'Angelo, ArturoColombelli, JulienSalbreux, GuillaumeDierkes, KaiSolon, JérômeDrosophila dorsal closureE-cadherinActomyosin cytoskeletonAdherens junctionBiophysical modelingEndocytosisEpithelial contractionMorphogenesisDuring epithelial contraction, cells generate forces to constrict their surface and, concurrently, fine-tune the length of their adherens junctions to ensure force transmission. While many studies have focused on understanding force generation, little is known on how junctional length is controlled. Here, we show that, during amnioserosa contraction in Drosophila dorsal closure, adherens junctions reduce their length in coordination with the shrinkage of apical cell area, maintaining a nearly constant junctional straightness. We reveal that junctional straightness and integrity depend on the endocytic machinery and on the mechanosensitive activity of the actomyosin cytoskeleton. On one hand, upon junctional stretch and decrease in E-cadherin density, actomyosin relocalizes from the medial area to the junctions, thus maintaining junctional integrity. On the other hand, when junctions have excess material and ruffles, junction removal is enhanced, and high junctional straightness and tension are restored. These two mechanisms control junctional length and integrity during morphogenesis.The research leading to the results has received funding from the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership and Centro de Excelencia Severo Ochoa and to the Plan Nacional, BFU2010-16546 and BFU2015-68754.Elsevier201920192018info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/42836http://dx.doi.org/10.1016/j.devcel.2018.10.025reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésDevelopmental Cell. 2018;47(4):453-63info:eu-repo/grantAgreement/ES/3PN/BFU2010-16546info:eu-repo/grantAgreement/ES/1PE/BFU2015-68754© 2018 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/428362026-06-12T07:21:37Z
dc.title.none.fl_str_mv Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
title Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
spellingShingle Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
Sumi, Angughali Aheto, 1986-
Drosophila dorsal closure
E-cadherin
Actomyosin cytoskeleton
Adherens junction
Biophysical modeling
Endocytosis
Epithelial contraction
Morphogenesis
title_short Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
title_full Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
title_fullStr Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
title_full_unstemmed Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
title_sort Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling
dc.creator.none.fl_str_mv Sumi, Angughali Aheto, 1986-
Hayes, D. Peran, 1983-
D'Angelo, Arturo
Colombelli, Julien
Salbreux, Guillaume
Dierkes, Kai
Solon, Jérôme
author Sumi, Angughali Aheto, 1986-
author_facet Sumi, Angughali Aheto, 1986-
Hayes, D. Peran, 1983-
D'Angelo, Arturo
Colombelli, Julien
Salbreux, Guillaume
Dierkes, Kai
Solon, Jérôme
author_role author
author2 Hayes, D. Peran, 1983-
D'Angelo, Arturo
Colombelli, Julien
Salbreux, Guillaume
Dierkes, Kai
Solon, Jérôme
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Drosophila dorsal closure
E-cadherin
Actomyosin cytoskeleton
Adherens junction
Biophysical modeling
Endocytosis
Epithelial contraction
Morphogenesis
topic Drosophila dorsal closure
E-cadherin
Actomyosin cytoskeleton
Adherens junction
Biophysical modeling
Endocytosis
Epithelial contraction
Morphogenesis
description During epithelial contraction, cells generate forces to constrict their surface and, concurrently, fine-tune the length of their adherens junctions to ensure force transmission. While many studies have focused on understanding force generation, little is known on how junctional length is controlled. Here, we show that, during amnioserosa contraction in Drosophila dorsal closure, adherens junctions reduce their length in coordination with the shrinkage of apical cell area, maintaining a nearly constant junctional straightness. We reveal that junctional straightness and integrity depend on the endocytic machinery and on the mechanosensitive activity of the actomyosin cytoskeleton. On one hand, upon junctional stretch and decrease in E-cadherin density, actomyosin relocalizes from the medial area to the junctions, thus maintaining junctional integrity. On the other hand, when junctions have excess material and ruffles, junction removal is enhanced, and high junctional straightness and tension are restored. These two mechanisms control junctional length and integrity during morphogenesis.
publishDate 2018
dc.date.none.fl_str_mv 2018
2019
2019
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/42836
http://dx.doi.org/10.1016/j.devcel.2018.10.025
url http://hdl.handle.net/10230/42836
http://dx.doi.org/10.1016/j.devcel.2018.10.025
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Developmental Cell. 2018;47(4):453-63
info:eu-repo/grantAgreement/ES/3PN/BFU2010-16546
info:eu-repo/grantAgreement/ES/1PE/BFU2015-68754
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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