Contractile and mechanical properties of epithelia with perturbed actomyosin dynamics

PLoS One. 2014 Apr 23;9(4):e95695. doi: 10.1371/journal.pone.0095695. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Animals
  • Drosophila
  • Drosophila Proteins / metabolism*
  • Epithelial Cells / metabolism*
  • Linear Models
  • Myosins / metabolism*
  • Phosphorylation

Substances

  • Drosophila Proteins
  • Myosins

Grant support

Ministerio de Ciencia e Innovación (grant BFU-2011-25828), Marie Curie Career Integration Grant (PCIG09-GA-2011-293479), Biotechnology and Biological Sciences Research Council (grant BB/J010278/1), Physics of Medicine Initiative. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.