Mechanical control of global cell behaviour during dorsal closure inDrosophila

Abstract

Halfway through embryonic development, the epidermis of Drosophila exhibits a gap at the dorsal side covered by an extraembryonic epithelium, the amnioserosa (AS). Dorsal closure (DC) is the process whereby interactions between the two epithelia establish epidermal continuity. Although genetic and biomechanical analysis have identified the AS as a force-generating tissue, we do not know how individual cell behaviours are transformed into tissue movements. To approach this question we have applied a novel image-analysis method to measure strain rates in local domains of cells and performed a kinematic analysis of DC. Our study reveals spatial and temporal differences in the rate of apical constriction of AS cells. We find a slow phase of DC, during which apical contraction of cells at the posterior end predominates, and a subsequent fast phase, during which all the cells engage in the contraction, which correlates with the zippering process. There is a radial gradient of AS apical contraction, with marginal cells contracting earlier than more centrally located cells. We have applied this analysis to the study of mutant situations and associated a particular genotype with quantitative and reproducible changes in the rate of cell contraction and hence in the overall rate of the process. Our mutant analysis reveals the contribution of mechanical elements to the rate and pattern of DC.

Drosophilamorphogenesis: Tissue force laws and the modeling of dorsal closure

“…2(A)]. We note that recent treatments of amnioserosal contractility in closure focus on investigating and modeling force contributions from individual cells in the amnioserosa (Gorfinkiel et al, 2009;Solon et al, 2009). The forces p = AS dx, p 0 = AS,0 dx, and a = a AS dx in Eq.…”

“…Other defects caused by mutations in integrin subunits or interacting proteins included delayed formation of the canthi and slowed closure, defects in adhesion between the amnioserosa and the yolk cell, defects in adhesion between the peripheral amnioserosa cells and the leading edge cells, aberrant actin rich purse strings, and alterations in the pattern of contraction of amnioserosa cells (Stark et al, 1997;Kadrmas et al, 2004;Narasimha and Brown, 2004;Reed et al, 2004;Wada et al, 2007;Gorfinkiel et al, 2009). Here, we simulated the closure behavior of the myospheroid embryo simply by constraining the movement of the canthi, i.e., the positions of the canthi (x ant and x post ) were fixed.…”

“…The purse strings shorten, largely through contractions near the canthi [see below ], and cells of the lateral epidermis elongate toward the dorsal midline. At the same time, cells of the amnioserosa actively change shape anisotropically as their apical surfaces contract to help draw the lateral epidermal sheets together (Kiehart et al, 2000;Jacinto et al, 2002;Gorfinkiel et al, 2009;Solon et al, 2009). Recent experiments demonstrate that cell shape changes in the amnioserosa are contributed by forces produced near cell junctions and distributed over the apical cytoskeleton (Ma et al, 2009).…”

“…In addition, our experimental observations indicate that the predominant cellular movement in this stage of dorsal closure occurs normal to the dorsal midline, so we also implement this observation as an assumption of the model (unpublished observations). When brought into close proximity, presumably by forces from the supracellular purse string and the amnioserosa, the two flanks of the lateral epidermis are "zipped" together at the canthi as filopodia and lamellipodia from opposing leading edges interdigitate, and a seam is formed (Jacinto et al, 2000;Bloor and Kiehart, 2002;Gorfinkiel et al, 2009). Ultimately, the dorsal surface is covered by a continuous epithelium that appears seamless.…”

Cadherin-based intercellular adhesions organize epithelial cell–matrix traction forces

“…This work defines the importance of cadherin-based cell-cell adhesions in coordinating mechanical activity of epithelial cells and has implications for the mechanical regulation of epithelial tissues during development, homeostasis, and disease. mechanotransduction | traction force microscopy M echanical interactions of individual cells have a crucial role in the spatial organization of tissues (1,2) and in embryonic development (3)(4)(5). The mechanical cooperation of cells is evident in dynamic processes such as flow-induced alignment of vascular endothelial cells (6) and muscle contraction (7).…”