Quantifying dorsal closure in three dimensions

Abstract

The three-dimensional surface of dorsal-closure-staged Drosophila embryos is indented by two purse strings that surround an eye-shaped amnioserosa tissue. The amnioserosa forms a remarkably smooth, asymmetric dome that bulges outward due to the embryo’s internal pressure. Quantitative analysis with Laplace’s formula indicates that the elastic properties of the amnioserosa are isotropic and uniform.

Cell Sheet Morphogenesis: Dorsal Closure inDrosophila melanogasteras a Model System

“…In addition, the amnioserosa bulges into the perivitelline space as a smooth, asymmetric dome, and the purse strings can indent the embryo surface. These observations suggest a pressure internal to the embryo (Lu et al 2016). Moreover, loss of amnioserosa cell volume may be essential for force production in the amnioserosa (Saias et al 2015).…”

“…Ultimately, Integrin/ECM interactions drive the close apposition of the amnioserosa with the surface of the yolk with its Actomyosin-rich cortex (Figure 2; see Supplemental Video 2, reproduced with permission from Reed et al 2004), which is likely to provide structural stability to the otherwise thin and flexible amnioserosa cell sheet. The amnioserosa and the yolk to which it is tightly adhered bulge outward in a remarkably smooth, asymmetric dome: Quantitative analysis indicates that the amnioserosa has uniform and isotropic surface tension (Lu et al 2016).…”

“…These models are nicely summarized in a recent review (Hayes & Solon 2017). Several other biophysical models that account for the balance of these forces that drive the completion of closure have also been proposed and are discussed elsewhere (Solon et al 2009, Wang et al 2012, Jayasinghe et al 2013, Dierkes et al 2014, Lu et al 2015, Machado et al 2015, Gorfinkiel 2016, Hara et al 2016, Lu et al 2016, Hayes & Solon 2017, Yu & Fernandez-Gonzalez 2017). A future review will compare models for molecular-, cellular- and tissue-level forces (A. Aristotelous, J.M.…”

Mathematical models of dorsal closure

“…One example is the three-dimensional, molecular and cellular model for zipping, which models the asymmetry in zipping at the anterior and posterior canthi as due to the molecular dynamics of interface remodeling in combination with differences in the tissue forces produced by the amnioserosa at each canthus (Lu et al, 2015). A second example is the three dimensional, time-dependent geometry of the dorsal opening, where analysis of the doming of the amnioserosa quantified its isotropic elasticity (Lu et al, 2016). A third example is the observation that the volume of an amnioserosa cell is not constant during dorsal closure, questioning the assumption that these cells would be isovolumetric and providing an extra force that may contribute to closure (Saias et al, 2015).…”

“…It is natural to assume a two-dimensional geometry, 2D, as a framework for constructing a mathematical model of dorsal closure. Nevertheless, especially at the beginning of closure, the amniosersa and the dorsal side of the embryo have real 3D character (Chen et al, 2014; Lu et al, 2016) and new models should take this three dimensionality into account. The majority of existing models indeed treat the amnioserosa as a 2D planar ellipsoidal or eye-shaped region (Hutson et al, 2003; Layton et al, 2009; Almeida et al, 2011; Solon et al, 2009; Wang et al, 2012; Dureau et al, 2016; Dierkes et al, 2014).…”