Abstract

The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.

Highlights

  • In many developmental and cellular contexts, actin filaments construct complex and highly dynamic structures to accomplish cell shape changes such as in migration and cytokinesis (Munjal and Lecuit, 2014)

  • Posterior relocation of basal cortical actin rings to the equator in notochord cells To analyze the development of the equatorial actin ring, we followed the expression of actin markers Lifeact-mEGFP and mCherry-UtrCH in notochord cells from the onset of C/E

  • We examined the dynamic localization of talin, an actin-binding protein that bridges actin filaments and the adhesion apparatus at the cleavage furrow of dividing cells (Sanger et al, 1994; Critchley, 2009; Kanchanawong et al, 2010), and normally colocalized with the cortical actin ring at the equator in Ciona notochord (Sehring et al, 2014)

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Summary

Introduction

In many developmental and cellular contexts, actin filaments construct complex and highly dynamic structures to accomplish cell shape changes such as in migration and cytokinesis (Munjal and Lecuit, 2014). Correct positioning of the actin filaments is essential. Actin flows posteriorly and becomes associated with myosin II at the trailing edge to propel the cell forward (Cramer, 2010). In cytokinesis of vertebrate cells, the equatorial ring is established in many incidences by a cortical flow of actin filaments (Bray and White, 1988) driven by myosin contractility and is concentrated at the equator to ensure correct cell division (Cao and Wang, 1990; DeBiasio et al, 1996; Mayer et al, 2010). In Caenorhabditis elegans early embryogenesis, a flow of cortical myosin and F-actin towards the anterior pole carries PAR polarity proteins, which in turn modulate the actomyosin dynamics (Munro et al, 2004; Mayer et al, 2010).

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