Abstract

Actin cables are linear cytoskeletal structures that serve as tracks for myosin-based intracellular transport of vesicles and organelles in both yeast and mammalian cells. In a yeast cell undergoing budding, cables are in constant dynamic turnover yet some cables grow from the bud neck toward the back of the mother cell until their length roughly equals the diameter of the mother cell. This raises the question: how is the length of these cables controlled? Here we describe a novel molecular mechanism for cable length control inspired by recent experimental observations in cells. This “antenna mechanism” involves three key proteins: formins, which polymerize actin, Smy1 proteins, which bind formins and inhibit actin polymerization, and myosin motors, which deliver Smy1 to formins, leading to a length-dependent actin polymerization rate. We compute the probability distribution of cable lengths as a function of several experimentally tuneable parameters such as the formin-binding affinity of Smy1 and the concentration of myosin motors delivering Smy1. These results provide testable predictions of the antenna mechanism of actin-cable length control.

Highlights

  • Eukaryotic cells have a complex cytoskeleton that includes vast arrays of microtubules and actin filaments, which governs the internal positioning and movement of cellular substructures such as vesicles and organelles, and dynamic changes in cell polarity, shape, and movement.Many of these processes require the length of the cytoskeletal structures to be tightly controlled.For example, during cell division, the microtubule-based mitotic spindle maintains a remarkably constant size despite undergoing highly dynamic turnover [1,2,3,4]

  • Based on published cell experiments, we propose a novel mechanism of length control of actin cables in budding yeast cells

  • The key feature of this “antenna mechanism” is negative feedback of the cable length on the activity of formins, which are proteins that attach to the growing ends of actin filaments and catalyse their polymerization

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Summary

Introduction

Eukaryotic cells have a complex cytoskeleton that includes vast arrays of microtubules and actin filaments, which governs the internal positioning and movement of cellular substructures such as vesicles and organelles, and dynamic changes in cell polarity, shape, and movement Many of these processes require the length of the cytoskeletal structures to be tightly controlled. During cell division, the microtubule-based mitotic spindle maintains a remarkably constant size despite undergoing highly dynamic turnover [1,2,3,4] Another example of cellular structures whose lengths are regulated are cilia, which are used for motility and sensation [5,6,7,8].

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