Length control emerges from cytoskeletal network geometry

Author:

McInally Shane G.1ORCID,Reading Alexander J. B.2ORCID,Rosario Aldric3,Jelenkovic Predrag R.4,Goode Bruce L.2ORCID,Kondev Jane3

Affiliation:

1. Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, MA 01609

2. Department of Biology, Brandeis University, Waltham, MA 02454

3. Department of Physics, Brandeis University, Waltham, MA 02454

4. Department of Electrical Engineering, Columbia University, New York, NY 10027

Abstract

Many cytoskeletal networks consist of individual filaments that are organized into elaborate higher-order structures. While it is appreciated that the size and architecture of these networks are critical for their biological functions, much of the work investigating control over their assembly has focused on mechanisms that regulate the turnover of individual filaments through size-dependent feedback. Here, we propose a very different, feedback-independent mechanism to explain how yeast cells control the length of their actin cables. Our findings, supported by quantitative cell imaging and mathematical modeling, indicate that actin cable length control is an emergent property that arises from the cross-linked and bundled organization of the filaments within the cable. Using this model, we further dissect the mechanisms that allow cables to grow longer in larger cells and propose that cell length–dependent tuning of formin activity allows cells to scale cable length with cell length. This mechanism is a significant departure from prior models of cytoskeletal filament length control and presents a different paradigm to consider how cells control the size, shape, and dynamics of higher-order cytoskeletal structures.

Funder

NSF

Simons Foundation

HHS | NIH | National Institute of General Medical Sciences

Publisher

Proceedings of the National Academy of Sciences

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