Morphogenetic oscillations during symmetry breaking of regeneratingHydra vulgariscells

Abstract

During the process of regeneration, the fresh-water polyp Hydra vulgaris first builds a hollow sphere consisting of a cell bilayer. This cell ball undergoes subsequent shape transformations, at a later stage it creates tentacles and a foot to form an animal. We describe and analyze the transformation of the hollow sphere to the first non-spherical shape by means of contour analysis. We observe that the cell ball shows characteristic oscillations in size and shape which accompany symmetry breaking. Quantitative analysis of these oscillations provides information on the cell bilayer mechanics and hydrodynamic flows involved. In order to explain the origin of the observed oscillations, we propose three different physical scenarios of oscillation generation.

Hydra Molecular Network Reaches Criticality at the Symmetry-Breaking Axis-Defining Moment

“…We suggest that it is a Wnt expressing organizer, consisting of only 5-10 cells, which causes the localized weakening of the cell bilayer and the release of osmotic pressure during phase II. This agrees with the expected size of the pressure-releasing hole, of the order of cell size [15]. Following this idea, the weakening of the cell bilayer can be understood as early mouth formation, a topological change providing a certain parallel to gastrulation.…”

“…2(a). We have described these oscillations as pressure buildup in the hydra ball due to osmotic swelling [15,16] until a sudden pressure release occurs. The cycles change abruptly after about 20 hours from high amplitude, low frequency oscillations (phase I) to low amplitude, high frequency oscillations (phase II) [ Fig.…”

“…During phase II, a weak spot in the hydra cell bilayer causes the sphere to release pressure at a decreased threshold, thus reducing the amplitude of the inflation-contraction cycles. At the transition between both phases, the elastic properties of the cell sphere become anisotropic in the direction of the developmental axis [15,17].…”

Critical Behavior and Axis Defining Symmetry Breaking inHydraEmbryonic Development

“…The entire animal can even reform from a cell aggregate as small as 10 4 cells, made from dissociated and randomly condensed Hydra cells [3,4]. The reformation starts with the cells forming an inflating, hollow, spherical cell bilayer [5,6]. The cells then define a new foot-head axis, and further development takes place according to its direction.…”

A Physical Model of Cellular Symmetry Breaking

“…This sphere inflates by uptake of fluid and builds up pressure because of stretching of the cells, analogous to the accumulation of stress in the actin gel growing around a bead. It has been proposed that this stress is released by rupture of the cell layer, followed by rapid shrinkage of the cell wall and reswelling, thus generating an oscillation mechanism (Fütterer et al 2003). Interestingly, it has been suggested in a recent paper (Soriano et al 2009) that Hydra symmetry breaking is a combination of a mechanical and a biochemical (Turing) instability: Mechanical stresses in the cell aggregate affect the diffusion rates of proteins and thereby provide the biochemical conditions necessary for a Turing instability.…”