Existing actin filaments orient new filament growth to provide structural memory of filament alignment during cytokinesis

Abstract

During cytokinesis, animal cells rapidly remodel the equatorial cortex to build an aligned array of actin filaments called the contractile ring. Local reorientation of filaments by equatorial contraction is thought to underlie the emergence of filament alignment during ring assembly.Here, combining single molecule analysis and modeling in one-cell C. elegans embryos, we show that filaments turnover is far too fast for reorientation of single filaments by equatorial contraction/cortex compression to explain the observed alignment, even if favorably oriented filaments are selectively stabilized. Instead, by tracking single Formin/CYK-1::GFP speckles to monitor local filament assembly, we identify a mechanism that we call filament-guided filament assembly (FGFA), in which existing filaments serve as templates to guide/orient the growth of new filaments. We show that FGFA sharply increases the effective lifetime of filament orientation, providing structural memory that allows slow equatorial contraction to build and maintain highly aligned filament arrays, despite rapid turnover of individual filaments.

Septins and a formin have distinct functions in anaphase chiral cortical rotation in theCaenorhabditis eleganszygote

“…Accumulated stress is overcome by actomyosin contractility and relieved by chiral displacement of initially-radial bundles (Tee et al, 2015). Rotation speed in the C. elegans zygote is intermediate to that of NMMII movement and CYK-1 formin single molecule movement thought to be in concert with F-actin polymerization (Higashida et al, 2004;Li and Munro, 2020;Melli et al, 2018). This further supports the idea that chiral movement is not purely driven by NMMII motoring, but rather results from the release of torsional stresses in the network.…”

Calponin-Homology Domain mediated bending of membrane associated actin filaments

“…Our work recapitulates that this minimal set of proteins can indeed generate and stabilize actin filaments of the right curvature to form the cytokinetic ring along the short axis of S. pombe. Even though electron microscopy data of the cytokinetic ring does not provide clear evidence of bent actin filaments (Swulius et al, 2018), this mechanism could work together with other processes such as cross-linkers ensuring the binding of fresh actin filaments along existing ones (Li & Munro, 2020) to drive robust formation of cytokinetic rings.…”

Going with the flow: insights fromCaenorhabditis eleganszygote polarization

“…The biophysical basis underlying these processes is an area of active research, where both physical studies and mathematical modelling are greatly aiding our understanding of how cytoskeleton dynamics and cytoplasmic movements are impacting patterning systems [22]. Evolving technologies are supporting investigation of these spatio-temporally-dependent processes in vivo, such as in studies examining cortical dynamics upon laser ablation [76], the creation of artificial flows by FLUCS [81], live super-resolution imaging in combination with methods that manipulate protein function and localization [54][55][56][57]173,205,266] and synthetic biology approaches, studying minimal systems [75,149,150].…”

“…Contrary to the above described work a very recent publication indicates that flows cannot mediate actin filament alignment, due to the rapid turn-over of these filaments. Alternatively, the mechanism proposed is that equatorially aligned filaments serve as templates to guide the growth of new ones [265] (Li, Munro 2020). Prevalence of equatorial alignment might be supported by other mechanisms.…”