Curvature-induced expulsion of actomyosin bundles during cytokinetic ring contraction

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.DOI: http://dx.doi.org/10.7554/eLife.21383.001

Capping protein regulates actin dynamics during cytokinetic midbody maturation

“…As the contractile ring ingresses rapidly, the diameter of the actin ring does not increase substantially, suggesting that actin is removed. Shortening of actin filaments (7,41) as well as filament ejection due to changes in tension forces have been implicated in the disassembly during ingression (8), but molecular details have been elusive (3).…”

“…Contractile ring assembly, ingression, and closure are regulated in part by Rho GTPase signaling, which triggers the activation of myosin and the formation of formin-based linear actin filaments (5,6). As the ring ingresses and its diameter decreases, actin filaments must disassemble to allow complete ingression and subsequent formation of the midbody (7,8). Much of our knowledge of the early steps of actin dynamics during cytokinesis has come from studies in model systems, such as fission yeast, because they are broadly conserved.…”

A low-cost DIY device for high resolution, continuous measurement of microbial growth dynamics

“…These two starter cultures were incubated overnight at 37°C and 30°C, respectively, with 150rpm shaking. Starter culture of S. pombe was prepared by picking individual colonies from YEA medium (19) agar plates, dissolving these in 100mL of YEA medium, and incubating for 48 hours at 30°C with 240rpm shaking. After the turbidity values of the starter cultures reached above 2.5, three 33mL-aliquots of each starter culture were transferred into 50mL-centrifuge tubes.…”

Molecular form and function of the cytokinetic ring

“…Intermediate layer: accessory protein network individual CR components, particularly those required for CR formation, contribute to contraction (Mishra et al, 2013;Huang et al, 2016a;Chew et al, 2017;Palani et al, 2017). These studies defined the minimal requirements for CR contraction in this system as the presence of F-actin, myosin-II ATPase activity and a balance of actin-crosslinking proteins (Mishra et al, 2013); surprisingly, the actin severer cofilin is not essential.…”

“…Previously, cofilin was proposed to be essential for F-actin filament severing during disassembly (Mendes Pinto et al, 2012), which is well-established to occur simultaneously upon contraction (Schroeder, 1972;Carvalho et al, 2009;Mavrakis et al, 2014;Huang et al, 2016a). The dispensability of cofilin for contraction in fission yeast cell ghosts indicates the existence of alternative mechanisms for F-actin disassembly, as have been previously proposed, such as myosin-IImediated actin filament breaking or a physical mechanism owing to compression by increased curvature as the CR diameter decreases (Huang et al, 2016a). It also suggests cofilin might have a different essential function, such as regulating F-actin length for proper CR formation.…”