Probing embryonic tissue mechanics with laser hole-drilling

TL;DR

This study employs laser hole-drilling to measure and analyze the mechanical properties of embryonic epithelium during dorsal closure in fruit flies, revealing a transition from fluid-like to solid-like tissue behavior.

Contribution

It introduces a novel laser ablation method for in vivo, subcellular resolution mechanical assessment of embryonic tissues during development.

Findings

Tissue mechanics are intermediate between a continuous sheet and a cellular foam.

Tensile stress is distributed between cell interfaces and actin networks.

Tissue transitions to a more solid-like state during closure.

Abstract

We use laser hole-drilling to assess the mechanics of an embryonic epithelium during development - in vivo and with subcellular resolution. We ablate a subcellular cylindrical hole clean through the epithelium, and track the subsequent recoil of adjacent cells (on ms time scales). We investigate dorsal closure in the fruit fly with emphasis on apical constriction of amnioserosa cells. The mechanical behavior of this epithelium falls between that of a continuous sheet and a 2D cellular foam (a network of tensile interfaces). Tensile stress is carried both by cell-cell interfaces and by the cells' apical actin networks. Our results show that stress is slightly concentrated along interfaces (1.6-fold), but only in early closure. Furthermore, closure is marked by a decrease in the recoil power-law exponent - implying a transition to a more solid-like tissue. We use the site- and stage-dependence of the recoil kinetics to constrain how the cellular mechanics change during closure. We apply these results to test extant computational models.