Abstract

Mechanics has an important role during morphogenesis, both in the generation of forces driving cell shape changes and in determining the effective material properties of cells and tissues. Drosophila dorsal closure has emerged as a reference model system for investigating the interplay between tissue mechanics and cellular activity. During dorsal closure, the amnioserosa generates one of the major forces that drive closure through the apical contraction of its constituent cells. We combined quantitation of live data, genetic and mechanical perturbation and cell biology, to investigate how mechanical properties and contraction rate emerge from cytoskeletal activity. We found that a decrease in Myosin phosphorylation induces a fluidization of amnioserosa cells which become more compliant. Conversely, an increase in Myosin phosphorylation and an increase in actin linear polymerization induce a solidification of cells. Contrary to expectation, these two perturbations have an opposite effect on the strain rate of cells during DC. While an increase in actin polymerization increases the contraction rate of amnioserosa cells, an increase in Myosin phosphorylation gives rise to cells that contract very slowly. The quantification of how the perturbation induced by laser ablation decays throughout the tissue revealed that the tissue in these two mutant backgrounds reacts very differently. We suggest that the differences in the strain rate of cells in situations where Myosin activity or actin polymerization is increased arise from changes in how the contractile forces are transmitted and coordinated across the tissue through ECadherin-mediated adhesion. Altogether, our results show that there is an optimal level of Myosin activity to generate efficient contraction and suggest that the architecture of the actin cytoskeleton and the dynamics of adhesion complexes are important parameters for the emergence of coordinated activity throughout the tissue.

Highlights

  • Mechanical input is increasingly seen as an important regulator of development in both normal conditions and disease

  • Perturbing actin and myosin dynamics alters the strain rate of AS cells During dorsal closure (DC), AS cells progressively contract their apical surface area giving rise to one of the major forces driving the closure of the dorsal epidermis

  • We have previously measured the strain rate of AS cells over the course of DC and shown that it increases over time, the dynamics of which can be separated into two main phases, the slow and the fast phase, according to the pace at which the strain rate increases

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Summary

Introduction

Mechanical input is increasingly seen as an important regulator of development in both normal conditions and disease. Mechanical forces appear to regulate a variety of basic cellular processes such as cell adhesion, cell signalling, proliferation and differentiation (reviewed in [1,2]). Mechanics has a role both in the generation of forces important for cell shape changes and cellular rearrangements and in determining the effective mechanical properties of cells and tissues. Cell mechanical properties such as stiffness and viscosity are key cellular parameters that will influence how cells respond to forces and how they will transmit these forces across the tissue. Changes in mechanical properties in embryonic tissues can produce variation at the whole organismal level and contribute to the generation of variability in natural populations

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