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Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos

In the two-cell stage embryos of Caenorhabditis elegans, the contact surface of the two blastomeres forms a curve that bulges from the AB blastomere to the P(1) blastomere. This curve is a consequence of the high intracellular hydrostatic pressure of AB compared with that of P(1). However, the highe...

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Autores principales: Fujita, Masashi, Onami, Shuichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3254656/
https://www.ncbi.nlm.nih.gov/pubmed/22253922
http://dx.doi.org/10.1371/journal.pone.0030224
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author Fujita, Masashi
Onami, Shuichi
author_facet Fujita, Masashi
Onami, Shuichi
author_sort Fujita, Masashi
collection PubMed
description In the two-cell stage embryos of Caenorhabditis elegans, the contact surface of the two blastomeres forms a curve that bulges from the AB blastomere to the P(1) blastomere. This curve is a consequence of the high intracellular hydrostatic pressure of AB compared with that of P(1). However, the higher pressure in AB is intriguing because AB has a larger volume than P(1). In soap bubbles, which are a widely used model of cell shape, a larger bubble has lower pressure than a smaller bubble. Here, we reveal that the higher pressure in AB is mediated by its higher cortical tension. The cell fusion experiments confirmed that the curvature of the contact surface is related to the pressure difference between the cells. Chemical and genetic interferences showed that the pressure difference is mediated by actomyosin. Fluorescence imaging indicated that non-muscle myosin is enriched in the AB cortex. The cell killing experiments provided evidence that AB but not P(1) is responsible for the pressure difference. Computer simulation clarified that the cell-to-cell heterogeneity of cortical tensions is indispensable for explaining the pressure difference. This study demonstrates that heterogeneity in surface tension results in significant deviations of cell behavior compared to simple soap bubble models, and thus must be taken into consideration in understanding cell shape within embryos.
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spelling pubmed-32546562012-01-17 Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos Fujita, Masashi Onami, Shuichi PLoS One Research Article In the two-cell stage embryos of Caenorhabditis elegans, the contact surface of the two blastomeres forms a curve that bulges from the AB blastomere to the P(1) blastomere. This curve is a consequence of the high intracellular hydrostatic pressure of AB compared with that of P(1). However, the higher pressure in AB is intriguing because AB has a larger volume than P(1). In soap bubbles, which are a widely used model of cell shape, a larger bubble has lower pressure than a smaller bubble. Here, we reveal that the higher pressure in AB is mediated by its higher cortical tension. The cell fusion experiments confirmed that the curvature of the contact surface is related to the pressure difference between the cells. Chemical and genetic interferences showed that the pressure difference is mediated by actomyosin. Fluorescence imaging indicated that non-muscle myosin is enriched in the AB cortex. The cell killing experiments provided evidence that AB but not P(1) is responsible for the pressure difference. Computer simulation clarified that the cell-to-cell heterogeneity of cortical tensions is indispensable for explaining the pressure difference. This study demonstrates that heterogeneity in surface tension results in significant deviations of cell behavior compared to simple soap bubble models, and thus must be taken into consideration in understanding cell shape within embryos. Public Library of Science 2012-01-10 /pmc/articles/PMC3254656/ /pubmed/22253922 http://dx.doi.org/10.1371/journal.pone.0030224 Text en Fujita, Onami. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Fujita, Masashi
Onami, Shuichi
Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title_full Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title_fullStr Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title_full_unstemmed Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title_short Cell-to-Cell Heterogeneity in Cortical Tension Specifies Curvature of Contact Surfaces in Caenorhabditis elegans Embryos
title_sort cell-to-cell heterogeneity in cortical tension specifies curvature of contact surfaces in caenorhabditis elegans embryos
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3254656/
https://www.ncbi.nlm.nih.gov/pubmed/22253922
http://dx.doi.org/10.1371/journal.pone.0030224
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