The interplay of stiffness and force anisotropies drives embryo elongation
The morphogenesis of tissues, like the deformation of an object, results from the interplay between their material properties and the mechanical forces exerted on them. The importance of mechanical forces in influencing cell behaviour is widely recognized, whereas the importance of tissue material p...
Main Authors: | , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2017-02-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/23866 |
_version_ | 1811200672448643072 |
---|---|
author | Thanh Thi Kim Vuong-Brender Martine Ben Amar Julien Pontabry Michel Labouesse |
author_facet | Thanh Thi Kim Vuong-Brender Martine Ben Amar Julien Pontabry Michel Labouesse |
author_sort | Thanh Thi Kim Vuong-Brender |
collection | DOAJ |
description | The morphogenesis of tissues, like the deformation of an object, results from the interplay between their material properties and the mechanical forces exerted on them. The importance of mechanical forces in influencing cell behaviour is widely recognized, whereas the importance of tissue material properties, in particular stiffness, has received much less attention. Using Caenorhabditis elegans as a model, we examine how both aspects contribute to embryonic elongation. Measuring the opening shape of the epidermal actin cortex after laser nano-ablation, we assess the spatiotemporal changes of actomyosin-dependent force and stiffness along the antero-posterior and dorso-ventral axis. Experimental data and analytical modelling show that myosin-II-dependent force anisotropy within the lateral epidermis, and stiffness anisotropy within the fiber-reinforced dorso-ventral epidermis are critical in driving embryonic elongation. Together, our results establish a quantitative link between cortical tension, material properties and morphogenesis of an entire embryo. |
first_indexed | 2024-04-12T02:07:34Z |
format | Article |
id | doaj.art-26a747d900454cbca8cf9f024943b274 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T02:07:34Z |
publishDate | 2017-02-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
spelling | doaj.art-26a747d900454cbca8cf9f024943b2742022-12-22T03:52:29ZengeLife Sciences Publications LtdeLife2050-084X2017-02-01610.7554/eLife.23866The interplay of stiffness and force anisotropies drives embryo elongationThanh Thi Kim Vuong-Brender0https://orcid.org/0000-0001-6594-2881Martine Ben Amar1https://orcid.org/0000-0001-9132-2053Julien Pontabry2https://orcid.org/0000-0001-7412-4645Michel Labouesse3https://orcid.org/0000-0001-7995-5843Laboratoire de Biologie du Développement - Institut de Biologie Paris Seine (LBD - IBPS), Sorbonne Universités, UPMC Univ Paris 06, CNRS, Paris, France; Development and Stem Cells Program, IGBMC, CNRS (UMR7104), INSERM (U964), Université de Strasbourg, Illkirch, FranceLaboratoire de Physique Statistique, Ecole Normale Supérieure, UPMC Université Pierre et Marie Curie, Université Paris Diderot, CNRS, Paris, France; Institut Universitaire de Cancérologie, Faculté de Médecine, Université Pierre et Marie Curie-Paris, Paris, FranceDevelopment and Stem Cells Program, IGBMC, CNRS (UMR7104), INSERM (U964), Université de Strasbourg, Illkirch, FranceLaboratoire de Biologie du Développement - Institut de Biologie Paris Seine (LBD - IBPS), Sorbonne Universités, UPMC Univ Paris 06, CNRS, Paris, France; Development and Stem Cells Program, IGBMC, CNRS (UMR7104), INSERM (U964), Université de Strasbourg, Illkirch, FranceThe morphogenesis of tissues, like the deformation of an object, results from the interplay between their material properties and the mechanical forces exerted on them. The importance of mechanical forces in influencing cell behaviour is widely recognized, whereas the importance of tissue material properties, in particular stiffness, has received much less attention. Using Caenorhabditis elegans as a model, we examine how both aspects contribute to embryonic elongation. Measuring the opening shape of the epidermal actin cortex after laser nano-ablation, we assess the spatiotemporal changes of actomyosin-dependent force and stiffness along the antero-posterior and dorso-ventral axis. Experimental data and analytical modelling show that myosin-II-dependent force anisotropy within the lateral epidermis, and stiffness anisotropy within the fiber-reinforced dorso-ventral epidermis are critical in driving embryonic elongation. Together, our results establish a quantitative link between cortical tension, material properties and morphogenesis of an entire embryo.https://elifesciences.org/articles/23866embryonic elongationforce anisotropystiffness anisotropyactomyosinlaser nano-ablationfiber-reinforced material |
spellingShingle | Thanh Thi Kim Vuong-Brender Martine Ben Amar Julien Pontabry Michel Labouesse The interplay of stiffness and force anisotropies drives embryo elongation eLife embryonic elongation force anisotropy stiffness anisotropy actomyosin laser nano-ablation fiber-reinforced material |
title | The interplay of stiffness and force anisotropies drives embryo elongation |
title_full | The interplay of stiffness and force anisotropies drives embryo elongation |
title_fullStr | The interplay of stiffness and force anisotropies drives embryo elongation |
title_full_unstemmed | The interplay of stiffness and force anisotropies drives embryo elongation |
title_short | The interplay of stiffness and force anisotropies drives embryo elongation |
title_sort | interplay of stiffness and force anisotropies drives embryo elongation |
topic | embryonic elongation force anisotropy stiffness anisotropy actomyosin laser nano-ablation fiber-reinforced material |
url | https://elifesciences.org/articles/23866 |
work_keys_str_mv | AT thanhthikimvuongbrender theinterplayofstiffnessandforceanisotropiesdrivesembryoelongation AT martinebenamar theinterplayofstiffnessandforceanisotropiesdrivesembryoelongation AT julienpontabry theinterplayofstiffnessandforceanisotropiesdrivesembryoelongation AT michellabouesse theinterplayofstiffnessandforceanisotropiesdrivesembryoelongation AT thanhthikimvuongbrender interplayofstiffnessandforceanisotropiesdrivesembryoelongation AT martinebenamar interplayofstiffnessandforceanisotropiesdrivesembryoelongation AT julienpontabry interplayofstiffnessandforceanisotropiesdrivesembryoelongation AT michellabouesse interplayofstiffnessandforceanisotropiesdrivesembryoelongation |