Motor processivity and speed determine structure and dynamics of microtubule-motor assemblies

  1. Rachel A Banks
  2. Vahe Galstyan
  3. Heun Jin Lee
  4. Soichi Hirokawa
  5. Athena Ierokomos
  6. Tyler D Ross
  7. Zev Bryant
  8. Matthew Thomson
  9. Rob Phillips  Is a corresponding author
  1. California Institute of Technology, United States
  2. Stanford University, United States

Abstract

Active matter systems can generate highly ordered structures, avoiding equilibrium through the consumption of energy by individual constituents. How the microscopic parameters that characterize the active agents are translated to the observed mesoscopic properties of the assembly has remained an open question. These active systems are prevalent in living matter; for example, in cells, the cytoskeleton is organized into structures such as the mitotic spindle through the coordinated activity of many motor proteins walking along microtubules. Here, we investigate how the microscopic motor-microtubule interactions affect the coherent structures formed in a reconstituted motor-microtubule system. This question is of deeper evolutionary significance as we suspect motor and microtubule type contribute to the shape and size of resulting structures. We explore key parameters experimentally and theoretically, using a variety of motors with different speeds, processivities, and directionalities. We demonstrate that aster size depends on the motor used to create the aster, and develop a model for the distribution of motors and microtubules in steady-state asters that depends on parameters related to motor speed and processivity. Further, we show that network contraction rates scale linearly with the single-motor speed in quasi one-dimensional contraction experiments. In all, this theoretical and experimental work helps elucidate how microscopic motor properties are translated to the much larger scale of collective motor-microtubule assemblies.

Data availability

All data associated with this study are stored on the CaltechData archive at DOI 10.22002/D1.2152.

The following data sets were generated

Article and author information

Author details

  1. Rachel A Banks

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Vahe Galstyan

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Heun Jin Lee

    Department of Applied Physics, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Soichi Hirokawa

    Department of Applied Physics, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5584-2676
  5. Athena Ierokomos

    Biophysics Program, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Tyler D Ross

    Department of Computing and Mathematical Science, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Zev Bryant

    Department of Bioengi, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Matthew Thomson

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Rob Phillips

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    phillips@pboc.caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3082-2809

Funding

Foundational Questions Institute (FQXi 1816)

  • Rachel A Banks
  • Vahe Galstyan
  • Heun Jin Lee
  • Soichi Hirokawa
  • Matthew Thomson
  • Rob Phillips

John Templeton Foundation (51250)

  • Rachel A Banks
  • Vahe Galstyan
  • Heun Jin Lee
  • Soichi Hirokawa
  • Matthew Thomson
  • Rob Phillips

National Institutes of Health (1R35 GM118043-01)

  • Rachel A Banks
  • Vahe Galstyan
  • Heun Jin Lee
  • Soichi Hirokawa
  • Rob Phillips

John Templeton Foundation (60973)

  • Rachel A Banks
  • Vahe Galstyan
  • Heun Jin Lee
  • Soichi Hirokawa
  • Matthew Thomson
  • Rob Phillips

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Karsten Kruse, University of Geneva, Switzerland

Version history

  1. Preprint posted: October 23, 2021 (view preprint)
  2. Received: April 11, 2022
  3. Accepted: February 7, 2023
  4. Accepted Manuscript published: February 8, 2023 (version 1)
  5. Version of Record published: March 14, 2023 (version 2)

Copyright

© 2023, Banks et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Rachel A Banks
  2. Vahe Galstyan
  3. Heun Jin Lee
  4. Soichi Hirokawa
  5. Athena Ierokomos
  6. Tyler D Ross
  7. Zev Bryant
  8. Matthew Thomson
  9. Rob Phillips
(2023)
Motor processivity and speed determine structure and dynamics of microtubule-motor assemblies
eLife 12:e79402.
https://doi.org/10.7554/eLife.79402

Share this article

https://doi.org/10.7554/eLife.79402

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