The mechanics of a microscopic mixer: microtubules and cytoplasmic streaming in Drosophila oocytes

Large scale motion of cytoplasm called cytoplasmic streaming occurs in some large eukaryotic cells to stir the cell's constituents. In Drosophila oocytes, microtubules have been observed to undergo undulating motion, curving to form travelling waves during cytoplasmic streaming. Here we show that this wave-like motion can be understood physically as due to the hydrodynamic drag of streaming impellers attached to kinesin motors moving toward the plus-ends of microtubules whose minus ends are anchored to the cell cortex. The tangential forces applied to such microtubules by kinesin give rise to bending and leads to chiral symmetry breaking causing the microtubules to propagate long travelling waves. The waves are reminiscent of those seen in flagellar motion but of a much longer time scale and by a different physical mechanism. We show how kinesin movement can produce a bulk flow of cytoplasm surrounding a microtubule with the range of flow greatly enhanced by the effect of hydrodynamic coupling between impellers. That is, a relatively small number of motors can move a large amount of fluid. The chaotic nature of the fluid motion of cytoplasm caused by kinesin movement along constantly changing microtubule trajectories is important as it greatly enhances the efficiency of mixing. Existing data on in vitro microtubule gliding assays also show this chiral instability in two dimensions and an analysis of this gives quantitative estimates for the forces exerted by motors and the drag coefficient.