Actomyosin-based tissue folding requires a multicellular myosin gradient

Abstract

Tissue folding promotes three-dimensional (3D) form during development. In many cases, folding is associated with myosin accumulation at the apical surface of epithelial cells, as seen in the vertebrate neural tube and the Drosophila ventral furrow. This type of folding is characterized by constriction of apical cell surfaces, and the resulting cell shape change is thought to cause tissue folding. Here, we use quantitative microscopy to measure the pattern of transcription, signaling, myosin activation and cell shape in the Drosophila mesoderm. We found that cells within the ventral domain accumulate different amounts of active apical non-muscle myosin 2 depending on the distance from the ventral midline. This gradient in active myosin depends on a newly quantified gradient in upstream signaling proteins. A 3D continuum model of the embryo with induced contractility demonstrates that contractility gradients, but not contractility per se, promote changes to surface curvature and folding. As predicted by the model, experimental broadening of the myosin domain in vivo disrupts tissue curvature where myosin is uniform. Our data argue that apical contractility gradients are important for tissue folding.

Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction

“…A requirement for cell ratcheting to maintain uniform furrow behaviors Previous work has demonstrated that a gradient of forces is present across the incipient furrow during mesoderm invagination in Drosophila (Heer et al, 2017). As cells will experience different pulling forces across this gradient, we questioned whether a requirement for cell ratcheting would be equally present in apically constricting cells.…”

Gait-optimized locomotion of wave-driven soft sheets

“…30 Equations of motion are obtained variationally from energy functionals based on the standard Koiter shell model. [31][32][33] Elastic dynamics are overdamped, consistent with growth processes in both living and engineered systems. 28 As a consequence, it is assumed at any time t that the system is in its minimal energy configuration.…”

“…28 As a consequence, it is assumed at any time t that the system is in its minimal energy configuration. For our system, these energy functionals are given in terms of the difference between the instantaneous metric a and curvature b tensors of the surface, and prescribed reference tensors % a and % b which define the local equilibrium behavior: 32,34…”

“…Such an approximation is suitable for cases in which mechanical equilibration occurs must faster than growth processes, and is a common assumption in morphoelastic processes. 32 Because elasticity dominates over damping, we assume that at each instant, the system is in its reference configuration and is quasi-statically evolving from one moment to the next. Although friction accounts for the net motion of the body, elasticity is so dominant that it can be assumed that friction affects the center-of-mass position only and not the shape.…”

Development and maintenance of functional actomyosin networks

“…Contraction of the actomyosin cytoskeleton drives cell and tissue movements during morphogenesis (Siedlik and Nelson, 2015;Heer et al, 2017) and wound closure (Russo et al, 2005), and allows cells to perceive and respond to mechanical stress (Clark et al, 2007). In non-muscle cells, cell contraction is driven by the interaction of the motor protein, non-muscle myosin II (NMII), with filamentous actin.…”