Cell signaling stabilizes morphogenesis against noise

Embryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, adhesion, etc.) and mechanical interactions. How should these be coordinated to lead to complex and robust morphologies? To explore this question, we randomly wired genes and cell behaviors into a h...

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Detalles Bibliográficos
Autores: Hagolani, Pascal F., Zimm, Roland, Marin-Riera, Miquel, Salazar-Ciudad, Isaac
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/44191
Acceso en línea:http://hdl.handle.net/10230/44191
http://dx.doi.org/10.1242/dev.179309
Access Level:acceso abierto
Palabra clave:Complexity
Development
Evolution
Gene networks
Morphogenesis
Robustness
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spelling Cell signaling stabilizes morphogenesis against noiseHagolani, Pascal F.Zimm, RolandMarin-Riera, MiquelSalazar-Ciudad, IsaacComplexityDevelopmentEvolutionGene networksMorphogenesisRobustnessEmbryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, adhesion, etc.) and mechanical interactions. How should these be coordinated to lead to complex and robust morphologies? To explore this question, we randomly wired genes and cell behaviors into a huge number of networks in EmbryoMaker. EmbryoMaker is a computational model of animal development that simulates how the 3D positions of cells, i.e. morphology, change over time due to such networks. We found that any gene network can lead to complex morphologies if this activates cell behaviors over large regions of the embryo. Importantly, however, for such complex morphologies to be robust to noise, gene networks should include cell signaling that compartmentalizes the embryo into small regions where cell behaviors are regulated differently. If, instead, cell behaviors are equally regulated over large regions, complex but non-robust morphologies arise. We explain how compartmentalization enhances robustness and why it is a general feature of animal development. Our results are consistent with theories proposing that robustness evolved by the co-option of gene networks and extracellular cell signaling in early animal evolution.Company of Biologists20202019info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/44191http://dx.doi.org/10.1242/dev.179309reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésDevelopment. 2019; 146(20). pii: dev179309© Company of Biologists http://dx.doi.org/10.1242/dev.179309info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/441912026-06-12T07:21:37Z
dc.title.none.fl_str_mv Cell signaling stabilizes morphogenesis against noise
title Cell signaling stabilizes morphogenesis against noise
spellingShingle Cell signaling stabilizes morphogenesis against noise
Hagolani, Pascal F.
Complexity
Development
Evolution
Gene networks
Morphogenesis
Robustness
title_short Cell signaling stabilizes morphogenesis against noise
title_full Cell signaling stabilizes morphogenesis against noise
title_fullStr Cell signaling stabilizes morphogenesis against noise
title_full_unstemmed Cell signaling stabilizes morphogenesis against noise
title_sort Cell signaling stabilizes morphogenesis against noise
dc.creator.none.fl_str_mv Hagolani, Pascal F.
Zimm, Roland
Marin-Riera, Miquel
Salazar-Ciudad, Isaac
author Hagolani, Pascal F.
author_facet Hagolani, Pascal F.
Zimm, Roland
Marin-Riera, Miquel
Salazar-Ciudad, Isaac
author_role author
author2 Zimm, Roland
Marin-Riera, Miquel
Salazar-Ciudad, Isaac
author2_role author
author
author
dc.subject.none.fl_str_mv Complexity
Development
Evolution
Gene networks
Morphogenesis
Robustness
topic Complexity
Development
Evolution
Gene networks
Morphogenesis
Robustness
description Embryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, adhesion, etc.) and mechanical interactions. How should these be coordinated to lead to complex and robust morphologies? To explore this question, we randomly wired genes and cell behaviors into a huge number of networks in EmbryoMaker. EmbryoMaker is a computational model of animal development that simulates how the 3D positions of cells, i.e. morphology, change over time due to such networks. We found that any gene network can lead to complex morphologies if this activates cell behaviors over large regions of the embryo. Importantly, however, for such complex morphologies to be robust to noise, gene networks should include cell signaling that compartmentalizes the embryo into small regions where cell behaviors are regulated differently. If, instead, cell behaviors are equally regulated over large regions, complex but non-robust morphologies arise. We explain how compartmentalization enhances robustness and why it is a general feature of animal development. Our results are consistent with theories proposing that robustness evolved by the co-option of gene networks and extracellular cell signaling in early animal evolution.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
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/10230/44191
http://dx.doi.org/10.1242/dev.179309
url http://hdl.handle.net/10230/44191
http://dx.doi.org/10.1242/dev.179309
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Development. 2019; 146(20). pii: dev179309
dc.rights.none.fl_str_mv © Company of Biologists http://dx.doi.org/10.1242/dev.179309
info:eu-repo/semantics/openAccess
rights_invalid_str_mv © Company of Biologists http://dx.doi.org/10.1242/dev.179309
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Company of Biologists
publisher.none.fl_str_mv Company of Biologists
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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score 15.812429

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