Cargando…

Active cell divisions generate fourfold orientationally ordered phase in living tissue

Morphogenesis, the process through which genes generate form, establishes tissue-scale order as a template for constructing the complex shapes of the body plan. The extensive growth required to build these ordered substrates is fuelled by cell proliferation, which, naively, should destroy order. Und...

Descripción completa

Detalles Bibliográficos
Autores principales: Cislo, Dillon J., Yang, Fengshuo, Qin, Haodong, Pavlopoulos, Anastasios, Bowick, Mark J., Streichan, Sebastian J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545346/
https://www.ncbi.nlm.nih.gov/pubmed/37786880
http://dx.doi.org/10.1038/s41567-023-02025-3
_version_ 1785114652218228736
author Cislo, Dillon J.
Yang, Fengshuo
Qin, Haodong
Pavlopoulos, Anastasios
Bowick, Mark J.
Streichan, Sebastian J.
author_facet Cislo, Dillon J.
Yang, Fengshuo
Qin, Haodong
Pavlopoulos, Anastasios
Bowick, Mark J.
Streichan, Sebastian J.
author_sort Cislo, Dillon J.
collection PubMed
description Morphogenesis, the process through which genes generate form, establishes tissue-scale order as a template for constructing the complex shapes of the body plan. The extensive growth required to build these ordered substrates is fuelled by cell proliferation, which, naively, should destroy order. Understanding how active morphogenetic mechanisms couple cellular and mechanical processes to generate order–rather than annihilate it–remains an outstanding question in animal development. We show that cell divisions are the primary drivers of tissue flow, leading to a fourfold orientationally ordered phase. Waves of anisotropic cell proliferation propagate across the embryo with precise patterning. Defects introduced into the nascent lattice by cell divisions are moved out of the tissue bulk towards the boundary by subsequent divisions. Specific cell proliferation rates and orientations enable cell divisions to organize rather than fluidize the tissue. We observe this using live imaging and tissue cartography to analyse the dynamics of fourfold tissue ordering in the trunk segmental ectoderm of the crustacean Parhyale hawaiensis beginning 72 h after egg lay. The result is a robust, active mechanism for generating global orientational order in a non-equilibrium system that sets the stage for the subsequent development of shape and form.
format Online
Article
Text
id pubmed-10545346
institution National Center for Biotechnology Information
language English
publishDate 2023
record_format MEDLINE/PubMed
spelling pubmed-105453462023-10-02 Active cell divisions generate fourfold orientationally ordered phase in living tissue Cislo, Dillon J. Yang, Fengshuo Qin, Haodong Pavlopoulos, Anastasios Bowick, Mark J. Streichan, Sebastian J. Nat Phys Article Morphogenesis, the process through which genes generate form, establishes tissue-scale order as a template for constructing the complex shapes of the body plan. The extensive growth required to build these ordered substrates is fuelled by cell proliferation, which, naively, should destroy order. Understanding how active morphogenetic mechanisms couple cellular and mechanical processes to generate order–rather than annihilate it–remains an outstanding question in animal development. We show that cell divisions are the primary drivers of tissue flow, leading to a fourfold orientationally ordered phase. Waves of anisotropic cell proliferation propagate across the embryo with precise patterning. Defects introduced into the nascent lattice by cell divisions are moved out of the tissue bulk towards the boundary by subsequent divisions. Specific cell proliferation rates and orientations enable cell divisions to organize rather than fluidize the tissue. We observe this using live imaging and tissue cartography to analyse the dynamics of fourfold tissue ordering in the trunk segmental ectoderm of the crustacean Parhyale hawaiensis beginning 72 h after egg lay. The result is a robust, active mechanism for generating global orientational order in a non-equilibrium system that sets the stage for the subsequent development of shape and form. 2023-08 2023-05-01 /pmc/articles/PMC10545346/ /pubmed/37786880 http://dx.doi.org/10.1038/s41567-023-02025-3 Text en https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . Reprints and permissions information is available at www.nature.com/reprints (http://www.nature.com/reprints) .
spellingShingle Article
Cislo, Dillon J.
Yang, Fengshuo
Qin, Haodong
Pavlopoulos, Anastasios
Bowick, Mark J.
Streichan, Sebastian J.
Active cell divisions generate fourfold orientationally ordered phase in living tissue
title Active cell divisions generate fourfold orientationally ordered phase in living tissue
title_full Active cell divisions generate fourfold orientationally ordered phase in living tissue
title_fullStr Active cell divisions generate fourfold orientationally ordered phase in living tissue
title_full_unstemmed Active cell divisions generate fourfold orientationally ordered phase in living tissue
title_short Active cell divisions generate fourfold orientationally ordered phase in living tissue
title_sort active cell divisions generate fourfold orientationally ordered phase in living tissue
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545346/
https://www.ncbi.nlm.nih.gov/pubmed/37786880
http://dx.doi.org/10.1038/s41567-023-02025-3
work_keys_str_mv AT cislodillonj activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue
AT yangfengshuo activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue
AT qinhaodong activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue
AT pavlopoulosanastasios activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue
AT bowickmarkj activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue
AT streichansebastianj activecelldivisionsgeneratefourfoldorientationallyorderedphaseinlivingtissue