Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
- University of Massachusetts, United States
- Worcester Polytechnic Institute, United States
Abstract
A monolayer of highly motile cells can establish long-range orientational order, which can be explained by hydrodynamic theory of active gels and fluids. However, it is less clear how cell shape changes and rearrangement are governed when the monolayer is in mechanical equilibrium states when cell motility diminishes. In this work, we report that rat embryonic fibroblasts (REF), when confined in circular mesoscale patterns on rigid substrates, can transition from the spindle shapes to more compact morphologies. Cells align radially only at the pattern boundary when they are in the mechanical equilibrium. This radial alignment disappears when cell contractility or cell-cell adhesion is reduced. Unlike monolayers of spindle-like cells such as NIH-3T3 fibroblasts with minimal intercellular interactions or epithelial cells like Madin-Darby canine kidney (MDCK) with strong cortical actin network, confined REF monolayers present an actin gradient with isotropic meshwork, suggesting the existence of a stiffness gradient. In addition, the REF cells tend to condense on soft substrates, a collective cell behavior we refer to as the 'condensation tendency'. This condensation tendency, together with geometrical confinement, induces tensile prestretch (i.e., an isotropic stretch that causes tissue to contract when released) to the confined monolayer. By developing a Voronoi-cell model, we demonstrate that the combined global tissue prestretch and cell stiffness differential between the inner and boundary cells can sufficiently define the cell radial alignment at the pattern boundary.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. All sequencing data were uploaded to the GEO public repository (https://www.ncbi.nlm.nih.gov/geo/) and were assigned series GSE148155.
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CELL CONTRACTILITY AND AN ACTIN GRADIENT DRIVE POLAR ALIGNMENT OF FIBROBLASTS IN CONSTRAINED GEOMETRIESNCBI Gene Expression Omnibus, GSE148155.
Article and author information
Author details
Funding
National Science Foundation (CMMI 1662835)
- Yubing Sun
National Science Foundation (CMMI 1846866)
- Yubing Sun
National Science Foundation (DMS 2012330)
- Min Wu
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Aleksandra M Walczak, École Normale Supérieure, France
Version history
- Preprint posted: June 24, 2020 (view preprint)
- Received: June 24, 2020
- Accepted: September 9, 2021
- Accepted Manuscript published: September 20, 2021 (version 1)
- Version of Record published: September 28, 2021 (version 2)
Copyright
© 2021, Xie et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
eLife 10:e60381.
https://doi.org/10.7554/eLife.60381
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