Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation

Abstract

Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.

Actin-based force generation and cell adhesion in tissue morphogenesis

“…In addition to force generation, supracellular cytoskeletal structures are also likely to affect the mechanical state of tissues in a developing embryo, such as whether it behaves like a solid or liquid. Indeed, recent evidence suggests that tissue fluidity can be modulated by multicellular actomyosin patterns and that this is important for gap closure in the context of wound healing and normal developmental processes 189,190 . Further studies linking supracellular actomyosin structures to the material properties of tissues in diverse systems will be necessary to unravel this connection.…”

Intertissue mechanical interactions shape the olfactory circuit in zebrafish

“…Laser ablations were initially used to sever subcellular structures that support force transmission to provoke a sudden mechanical imbalance: the initial recoil velocity of the ablated structure gives, under some assumptions, an estimation of the tension prior ablation [54][55][56] . Laser ablation can also be performed at tissue-scale to create a wound and estimate tissue stress [57][58][59][60][61] . To estimate mechanical stresses at the periphery of the ngn1:gfp + cell group within the OP, we performed linear supracellular laser cuts in anterior, lateral and posterior borders of the ngn1:gfp + cluster in control embryos and rx3 -/mutants, at 16s (as depicted in Figure 5A, Video 4).…”

Interactive design of GPU-accelerated Image Data Flow Graphs and cross-platform deployment using multi-lingual code generation

“…In order to study these layers in detail, spatial transformations can be applied to convert the cylindrical volume into image stacks ranging from the inside to the outside containing images which correspond to mucosa and muscularis externae layers respectively. Cartographic projections are the method of choice for visualising intensities along three-dimensional surfaces into two dimensions [29–31]. One simple form of such a projection is a maximum intensity projection along lines going from the center axis of a cylinder to its surface.…”