Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination.

Bing He,Hanqing Guo,Michael Swan

doi:10.7554/elife.69082

Abstract

Apical constriction driven by actin and non-muscle myosin II (actomyosin) provides a well-conserved mechanism to mediate epithelial folding. It remains unclear how contractile forces near the apical surface of a cell sheet drive out-of-the-plane bending of the sheet and whether myosin contractility is required throughout folding. By optogenetic-mediated acute inhibition of actomyosin, we find that during Drosophila mesoderm invagination, actomyosin contractility is critical to prevent tissue relaxation during the early, 'priming' stage of folding but is dispensable for the actual folding step after the tissue passes through a stereotyped transitional configuration. This binary response suggests that Drosophila mesoderm is mechanically bistable during gastrulation. Computer modeling analysis demonstrates that the binary tissue response to actomyosin inhibition can be recapitulated in the simulated epithelium that undergoes buckling-like deformation jointly mediated by apical constriction in the mesoderm and in-plane compression generated by apicobasal shrinkage of the surrounding ectoderm. Interestingly, comparison between wild-type and snail mutants that fail to specify the mesoderm demonstrates that the lateral ectoderm undergoes apicobasal shrinkage during gastrulation independently of mesoderm invagination. We propose that Drosophila mesoderm invagination is achieved through an interplay between local apical constriction and mechanical bistability of the epithelium that facilitates epithelial buckling.

Highlights

Contractile forces generated by actin and myosin (“actomyosin”) networks are widely employed in embryogenesis to drive cell motility and cell shape change that pattern epithelial tissues (Martin and Goldstein, 2014; Munjal and Lecuit, 2014)
The 35 invagination of the presumptive mesoderm during Drosophila gastrulation is a well36 characterized epithelial folding process mediated by apical constriction
We investigate the mechanics of ventral furrow formation by asking whether 82 actomyosin contractility is required throughout the folding process

Summary

Introduction

Contractile forces generated by actin and myosin (“actomyosin”) networks are widely employed in embryogenesis to drive cell motility and cell shape change that pattern epithelial tissues (Martin and Goldstein, 2014; Munjal and Lecuit, 2014). It has been observed that the maximal rate of apical constriction (or cell lengthening) and the maximal rate of tissue invagination occur at distinct times (Polyakov et al, 2014; Rauzi et al, 2015), and timed injection of Rok inhibitor indicates that the late stage of ventral furrow invagination is less sensitive to myosin inactivation (Krajcovic and Minden, 2012). A similar disruption of ventral furrow formation can be achieved by increasing actomyosin contractility in the lateral ectoderm (Perez-Mockus et al, 2017) While these pioneer studies highlight the importance of cross-tissue coordination during mesoderm invagination, the actual mechanical mechanism that drives the folding of the mesodermal epithelium and the potential role of the surrounding ectodermal tissue remain to be elucidated. We further hypothesize that the mechanical bistability of the mesoderm is attributed to ectodermal compression and functions together with active cell shape change in the 97 mesoderm to facilitate mesoderm invagination

Results

Discussion

Materials and Methods

Figures and Figure Legends