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Cycling State that Can Lead to Glassy Dynamics in Intracellular Transport

Monika Scholz, Stanislav Burov, Kimberly L. Weirich, Björn J. Scholz, S. M. Ali Tabei, Margaret L. Gardel, and Aaron R. Dinner
Phys. Rev. X 6, 011037 – Published 31 March 2016
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Abstract

Power-law dwell times have been observed for molecular motors in living cells, but the origins of these trapped states are not known. We introduce a minimal model of motors moving on a two-dimensional network of filaments, and simulations of its dynamics exhibit statistics comparable to those observed experimentally. Analysis of the model trajectories, as well as experimental particle tracking data, reveals a state in which motors cycle unproductively at junctions of three or more filaments. We formulate a master equation for these junction dynamics and show that the time required to escape from this vortexlike state can account for the power-law dwell times. We identify trends in the dynamics with the motor valency for further experimental validation. We demonstrate that these trends exist in individual trajectories of myosin II on an actin network. We discuss how cells could regulate intracellular transport and, in turn, biological function by controlling their cytoskeletal network structures locally.

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  • Received 31 March 2015

DOI:https://doi.org/10.1103/PhysRevX.6.011037

This article is available under the terms of the Creative Commons Attribution 3.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.

Published by the American Physical Society

Authors & Affiliations

Monika Scholz1,2, Stanislav Burov3, Kimberly L. Weirich1,2, Björn J. Scholz4,5,6, S. M. Ali Tabei7, Margaret L. Gardel1,2,6, and Aaron R. Dinner1,2,8,*

  • 1James Franck Institute, the University of Chicago, Chicago, Illinois 60637, USA
  • 2Institute for Biophysical Dynamics, the University of Chicago, Chicago, Illinois 60637, USA
  • 3Department of Physics, Bar-Ilan University, Ramat-Gan 5290002, Israel
  • 4Enrico Fermi Institute, the University of Chicago, Chicago, Illinois 60637, USA
  • 5Kavli Institute for Cosmological Physics, the University of Chicago, Chicago, Illinois 60637, USA
  • 6Department of Physics, the University of Chicago, Chicago, Illinois 60637, USA
  • 7Physics Department, University of Northern Iowa, Cedar Falls, Iowa 50614, USA
  • 8Department of Chemistry, the University of Chicago, Chicago, Illinois 60637, USA

  • *To whom all correspondence should be addressed. dinner@uchicago.edu

Popular Summary

Certain proteins known as molecular motors bind to cytoskeletal filaments within cells and move along these filaments. This motion impacts the kinetics of many biological processes. The complex dynamics observed with these molecular motors are believed to affect cellular function. Molecular motors can move seemingly randomly, steadily along filaments, and haltingly; they can also become trapped for long periods of time. Here, using simulations and quantitative analyses of experimental imaging data for actomyosin assemblies, we propose that motors can become trapped for long periods of time by cycling at filament junctions.

We conduct simulations of molecular motors consuming cellular energy stores and traveling along a two-dimensional network of filaments. In our simulations, the motors can associate with filaments within a defined binding radius (on the order of nanometers). We recover vortexlike trajectories (i.e., unproductive cycling) when the motors encounter intersections of filaments that form closed loops. We demonstrate that this mechanism operates in well-controlled experimental systems comprised of purified cytoskeletal components. To the best of our knowledge, reports of this cycling have been absent from the literature. However, this motion may have implications for biological regulation.

We expect that our results will pave the way for additional investigations of how the movement of molecular motors impacts intracellular transport and biological function.

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Vol. 6, Iss. 1 — January - March 2016

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