Cytoplasmic flows in starfish oocytes are fully determined by cortical contractions

Abstract

Cytoplasmic flows are an ubiquitous feature of biological systems, in particular in large cells, such as oocytes and eggs in early animal development. Here we show that cytoplasmic flows in starfish oocytes, which can be imaged well with transmission light microscopy, are fully determined by the cortical dynamics during surface contraction waves. We first show that the dynamics of the oocyte surface is highly symmetric around the animal-vegetal axis. We then mathematically solve the Stokes equation for flows inside a deforming sphere using the measured surface displacements as boundary conditions. Our theoretical predictions agree very well with the intracellular flows quantified by particle image velocimetry, proving that during this stage the starfish cytoplasm behaves as a simple Newtonian fluid on the micrometer scale. We calculate the pressure field inside the oocyte and find that its gradient is too small as to explain polar body extrusion, in contrast to earlier suggestions. Myosin II inhibition by blebbistatin confirms this conclusion, because it diminishes cell shape changes and hydrodynamic flow, but does not abolish polar body formation.

Computational modeling of active deformable membranes embedded in three-dimensional flows

“…Heer et al [47] determined the equilibrium shape of an elastic tissue layer folded into a deformable ellipsoidal shell, where myosin activity is incorporated as a preferred curvature of the shell. Klughammer et al [48] analytically calculated the flow inside a sphere that slightly deforms due to a traveling band of surface tension, which mimics cortical active tension, under the assumption of rotational symmetry. In all of these works the full dynamics of the external fluid was neglected and nearly all of them restricted themselves to deformations from simple rest shapes in the steady state.…”

Protein-free division of giant unilamellar vesicles controlled by enzymatic activity

“…Figure 2a indicates the relevant geometrical properties of the GUV, which can be extracted from confocal images. While living cells normally undergo symmetric division, where both daughter compartments are of similar size, some processes like oocyte maturation rely on assymmetric division [37]. In our model system, A lo = A ld leads to symmetric division as already demonstrated experimentally, whereas asymmetric division should be achieved otherwise.…”

Flow Induced Symmetry Breaking in a Conceptual Polarity Model

“…A different route of generalization is to consider advective flows that depend on the protein concentrations. In cells, such coupling arises, for instance, from myosin-driven cortex contractions [15,52] and shape deformations [8,25]. Myosin-motors, in turn, may be advected by the flow and their activity is controlled by signaling proteins such as GTPases and kinases [53].…”

“…By elementary algebra using the assumptions D c > D m and f c > 0 made above, it follows that A(q) is positive when s nc < 0. As Equation (8) in Section 3.3 shows, the condition s nc < 0 is necessary for a band of unstable modes to exist. Therefore, A(q) is positive for all unstable modes.…”

“…Pattern formation resulting from the interplay of reactions and diffusion has been widely studied since Turing's seminal work [6]. In addition to diffusion, proteins can be transported by fluid flows in the cytoplasm [7][8][9] and along cytoskeletal structures (vesicle trafficking, cortical contractions) driven by molecular motors [10][11][12]. These processes lead to advective transport of proteins.…”