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Epithelial cells sacrifice excess area to preserve fluidity in response to external mechanical stress.

ABSTRACT: Viscoelastic properties of epithelial cells subject to shape changes were monitored by indentation-retraction/relaxation experiments. MDCK II cells cultured on extensible polydimethylsiloxane substrates were laterally stretched and, in response, displayed increased cortex contractility and loss of excess surface area. Thereby, the cells preserve their fluidity but inevitably become stiffer. We found similar behavior in demixed cell monolayers of ZO-1/2 double knock down (dKD) cells, cells exposed to different temperatures and after removal of cholesterol from the plasma membrane. Conversely, the mechanical response of single cells adhered onto differently sized patches displays no visible rheological change. Sacrificing excess surface area allows the cells to respond to mechanical challenges without losing their ability to flow. They gain a new degree of freedom that permits resolving the interdependence of fluidity β on stiffness [Formula: see text]. We also propose a model that permits to tell apart contributions from excess membrane area and excess cell surface area.

SUBMITTER: Bodenschatz JFE

PROVIDER: S-EPMC9395404 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Epithelial cells sacrifice excess area to preserve fluidity in response to external mechanical stress.

Bodenschatz Jonathan F E JFE Ajmail Karim K Skamrahl Mark M Vache Marian M Gottwald Jannis J Nehls Stefan S Janshoff Andreas A

Communications biology 20220822 1

Viscoelastic properties of epithelial cells subject to shape changes were monitored by indentation-retraction/relaxation experiments. MDCK II cells cultured on extensible polydimethylsiloxane substrates were laterally stretched and, in response, displayed increased cortex contractility and loss of excess surface area. Thereby, the cells preserve their fluidity but inevitably become stiffer. We found similar behavior in demixed cell monolayers of ZO-1/2 double knock down (dKD) cells, cells expose ...[more]

PMID: 35995827

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Project description:Morphogenesis in early development involves complex and extreme deformations in response to intra- and intercellular forces. Zebrafish epiboly, the spreading of the blastoderm to cover and engulf the large yolk cell, is a key early event that sets the stage for gastrulation, but is poorly understood. The enveloping layer (EVL), the thin squamous outer epithelium of the blastoderm, bound at its edges to the yolk cell by tight junctions, plays a central role. The marginal EVL cells receive through their tight junctions, forces generated in the yolk cell, and propagate those forces through the rest of the EVL; and the resulting EVL expansion is required for epiboly of the deep cells within the blastoderm. However, we don't know how these exogenous forces are generated and regulated; several alternative force generation mechanisms have been proposed. In order to model their relative contributions, we need a mechanical model of the EVL capable of responding to such forces and undergoing the drastic deformation of epiboly. The expanding EVL more than doubles its surface area and experiences significant shear as it deforms from a thin cap at the pole to become a complete sphere, necessarily requiring extensive internal rearrangement. We constructed an agent-based model of the EVL and its response to exogenous forces using the center-based simulation framework, Tissue Forge. Our model captures the large viscoelastic deformation of the EVL by cell rearrangement, and incorporates algorithmic strategies to accommodate these dynamic changes while maintaining tissue cohesion. Features observed in living embryos, such as the straightening of the initially ragged leading edge, also emerge in the model. We identified two key components required for realistic epiboly in the model: first, a mechanism to enable tissue remodeling by cell rearrangement without tearing the tissue, and second, a regulatory negative feedback on the forces driving EVL expansion, to synchronize the advancement of the EVL margin. We discuss the implications of these findings for the behavior of living EVL and the mechanisms that drive epiboly.

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Epithelial cells sacrifice excess area to preserve fluidity in response to external mechanical stress.

Publications

Epithelial cells sacrifice excess area to preserve fluidity in response to external mechanical stress.

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