Cytoplasmic flows in starfish oocytes are fully determined by cortical contractions.

Nils Klughammer,Andrea Callegari,Nikolas D Schnellbächer,Johanna Bischof,Ulrich S Schwarz,Péter Lénárt,Anand R Asthagiri

doi:10.1371/journal.pcbi.1006588

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.

Highlights

The three most important cellular processes that drive animal development are cell division, cell shape changes and cell migration, which are all mediated by the cytoskeleton [1, 2]
More directed transport processes are needed on cellular scales, including transport by molecular motors or by hydrodynamic flows
We recently showed that the polar body is generated even if the surface contraction waves (SCWs) is strongly reduced by myosin II inhibition [21], but our earlier study did not address hydrodynamic flows

Summary

Introduction

The three most important cellular processes that drive animal development are cell division, cell shape changes and cell migration, which are all mediated by the cytoskeleton [1, 2]. The biological function of such waves ranges from global coordination of cell division to localising cellular structures or molecular components [10,11,12]. Cytoplasmic flows have been shown to have important functions in development, and have been proposed to mediate intracellular transport [13,14,15], intracellular mixing [16], force distribution [17, 18] and pattern formation [19]. The relation between wavelike cell shape changes and cytoplasmic flows has rarely been investigated in quantitative detail in a developmental model system, mainly due to experimental technical limitations

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Discussion

Conclusion