Curvature-induced expulsion of actomyosin bundles during cytokinetic ring contraction.

Junqi Huang,Nicholas J Carter,Ying Gu,Robert Anthony Cross,Ting Gang Chew,Saravanan Palani,Douglas S Martin,Snezhana Oliferenko,Mohan K Balasubramanian,Anton Kamnev

doi:10.7554/elife.21383

Junqi Huang, Nicholas J Carter + Show 8 more

Open Access

https://doi.org/10.7554/elife.21383

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Abstract

Many eukaryotes assemble a ring-shaped actomyosin network that contracts to drive cytokinesis. Unlike actomyosin in sarcomeres, which cycles through contraction and relaxation, the cytokinetic ring disassembles during contraction through an unknown mechanism. Here we find in Schizosaccharomyces japonicus and Schizosaccharomyces pombe that, during actomyosin ring contraction, actin filaments associated with actomyosin rings are expelled as micron-scale bundles containing multiple actomyosin ring proteins. Using functional isolated actomyosin rings we show that expulsion of actin bundles does not require continuous presence of cytoplasm. Strikingly, mechanical compression of actomyosin rings results in expulsion of bundles predominantly at regions of high curvature. Our work unprecedentedly reveals that the increased curvature of the ring itself promotes its disassembly. It is likely that such a curvature-induced mechanism may operate in disassembly of other contractile networks.

Highlights

Many eukaryotes assemble a dynamic actomyosin-based contractile ring to divide one cell into two (Pollard and Wu, 2010)
We find in Schizosaccharomyces japonicus and Schizosaccharomyces pombe that, during actomyosin ring contraction, actin filaments associated with actomyosin rings are expelled as micron-scale bundles containing multiple actomyosin ring proteins
The exact mechanism governing disassembly of actomyosin rings and whether and how the ring disassembly is coordinated to ring contraction have remained unknown so far. To address these gaps in our knowledge, we studied the dynamics of actomyosin ring contraction and disassembly in the fission yeasts Schizosaccharomyces japonicus and Schizosaccharomyces pombe

Summary

Introduction

Many eukaryotes assemble a dynamic actomyosin-based contractile ring to divide one cell into two (Pollard and Wu, 2010). During ring contraction, ring components continuously disassemble while maintaining ring contractility (Pollard and Wu, 2010) This is in stark contrast to other actomyosin machineries, the thick and thin filament based sarcomeres in muscle fibers, which undergo contraction and relaxation cycles without disassembly (Murrell et al, 2015). ADF1/Cofilin together with Coronin and WD-repeat protein Aip modulate actin turnover by severing actin bundles in many types of actin networks (Jansen et al, 2015). Their involvement in actomyosin ring contraction and disassembly is still unclear (Chen and Pollard, 2011). We test the curvature-dependence of the actomyosin ring disassembly by physically deforming protoplasts to defined geometries

Results and discussion

Materials and methods

Funding Funder Wellcome Trust