Emergent material properties of developing epithelial tissues

[Background] Force generation and the material properties of cells and tissues are central to morphogenesis but remain difficult to measure in vivo. Insight is often limited to the ratios of mechanical properties obtained through disruptive manipulation, and the appropriate models relating stress an...

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Autores: Machado, Pedro F., Duque, Julia, Étienne, Jocelyn, Martinez-Arias, Alfonso, Blanchard, Guy B., Gorfinkiel, Nicole
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2015
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/125809
Acceso en línea:http://hdl.handle.net/10261/125809
Access Level:acceso abierto
Palabra clave:Viscoelastic fluid
Mechanical properties
Apical contraction
Actomyosin
Oscillations
Hysteresis
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Emergent material properties of developing epithelial tissues
title Emergent material properties of developing epithelial tissues
spellingShingle Emergent material properties of developing epithelial tissues
Machado, Pedro F.
Viscoelastic fluid
Mechanical properties
Apical contraction
Actomyosin
Oscillations
Hysteresis
title_short Emergent material properties of developing epithelial tissues
title_full Emergent material properties of developing epithelial tissues
title_fullStr Emergent material properties of developing epithelial tissues
title_full_unstemmed Emergent material properties of developing epithelial tissues
title_sort Emergent material properties of developing epithelial tissues
dc.creator.none.fl_str_mv Machado, Pedro F.
Duque, Julia
Étienne, Jocelyn
Martinez-Arias, Alfonso
Blanchard, Guy B.
Gorfinkiel, Nicole
author Machado, Pedro F.
author_facet Machado, Pedro F.
Duque, Julia
Étienne, Jocelyn
Martinez-Arias, Alfonso
Blanchard, Guy B.
Gorfinkiel, Nicole
author_role author
author2 Duque, Julia
Étienne, Jocelyn
Martinez-Arias, Alfonso
Blanchard, Guy B.
Gorfinkiel, Nicole
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv University of Cambridge
Ministerio de Ciencia e Innovación (España)
European Commission
Biotechnology and Biological Sciences Research Council (UK)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Viscoelastic fluid
Mechanical properties
Apical contraction
Actomyosin
Oscillations
Hysteresis
topic Viscoelastic fluid
Mechanical properties
Apical contraction
Actomyosin
Oscillations
Hysteresis
description [Background] Force generation and the material properties of cells and tissues are central to morphogenesis but remain difficult to measure in vivo. Insight is often limited to the ratios of mechanical properties obtained through disruptive manipulation, and the appropriate models relating stress and strain are unknown. The Drosophila amnioserosa epithelium progressively contracts over 3 hours of dorsal closure, during which cell apices exhibit area fluctuations driven by medial myosin pulses with periods of 1.5–6 min. Linking these two timescales and understanding how pulsatile contractions drive morphogenetic movements is an urgent challenge.
publishDate 2015
dc.date.none.fl_str_mv 2015
2015
2015
2015
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/125809
url http://hdl.handle.net/10261/125809
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/FP7/293479
http://dx.doi.org/10.1186/s12915-015-0200-y
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Emergent material properties of developing epithelial tissuesMachado, Pedro F.Duque, JuliaÉtienne, JocelynMartinez-Arias, AlfonsoBlanchard, Guy B.Gorfinkiel, NicoleViscoelastic fluidMechanical propertiesApical contractionActomyosinOscillationsHysteresis[Background] Force generation and the material properties of cells and tissues are central to morphogenesis but remain difficult to measure in vivo. Insight is often limited to the ratios of mechanical properties obtained through disruptive manipulation, and the appropriate models relating stress and strain are unknown. The Drosophila amnioserosa epithelium progressively contracts over 3 hours of dorsal closure, during which cell apices exhibit area fluctuations driven by medial myosin pulses with periods of 1.5–6 min. Linking these two timescales and understanding how pulsatile contractions drive morphogenetic movements is an urgent challenge.[Results] We present a novel framework to measure in a continuous manner the mechanical properties of epithelial cells in the natural context of a tissue undergoing morphogenesis. We show that the relationship between apicomedial myosin fluorescence intensity and strain during fluctuations is consistent with a linear behaviour, although with a lag. We thus used myosin fluorescence intensity as a proxy for active force generation and treated cells as natural experiments of mechanical response under cyclic loading, revealing unambiguous mechanical properties from the hysteresis loop relating stress to strain. Amnioserosa cells can be described as a contractile viscoelastic fluid. We show that their emergent mechanical behaviour can be described by a linear viscoelastic rheology at timescales relevant for tissue morphogenesis. For the first time, we establish relative changes in separate effective mechanical properties in vivo. Over the course of dorsal closure, the tissue solidifies and effective stiffness doubles as net contraction of the tissue commences. Combining our findings with those from previous laser ablation experiments, we show that both apicomedial and junctional stress also increase over time, with the relative increase in apicomedial stress approximately twice that of other obtained measures.[Conclusions] Our results show that in an epithelial tissue undergoing net contraction, stiffness and stress are coupled. Dorsal closure cell apical contraction is driven by the medial region where the relative increase in stress is greater than that of stiffness. At junctions, by contrast, the relative increase in the mechanical properties is the same, so the junctional contribution to tissue deformation is constant over time. An increase in myosin activity is likely to underlie, at least in part, the change in medioapical properties and we suggest that its greater effect on stress relative to stiffness is fundamental to actomyosin systems and confers on tissues the ability to regulate contraction rates in response to changes in external mechanics.We thank the following funding bodies for their support: Herchel Smith Fund (PFM), Ministerio de Ciencia e Innovación (NG and JD, BFU2011-25828 and Ramón y Cajal fellowship award), Marie Curie Career Integration Grant (NG, PCIG09-GA-2011-293479), Biotechnology and Biological Sciences Research Council (GBB, grant BB/J010278/1) and Rhône-Alpes Complex System Institute (JE).Peer reviewedBioMed CentralUniversity of CambridgeMinisterio de Ciencia e Innovación (España)European CommissionBiotechnology and Biological Sciences Research Council (UK)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2015201520152015info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/125809reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/FP7/293479http://dx.doi.org/10.1186/s12915-015-0200-ySíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1258092026-05-22T06:33:51Z
score 15,811543

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