Motor processivity and speed determine structure and dynamics of microtubule-motor assemblies
- California Institute of Technology, United States
- 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.
Article and author information
Author details
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
- Karsten Kruse, University of Geneva, Switzerland
Version history
- Preprint posted: October 23, 2021 (view preprint)
- Received: April 11, 2022
- Accepted: February 7, 2023
- Accepted Manuscript published: February 8, 2023 (version 1)
- 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.
Metrics
-
- 1,023
- views
-
- 175
- downloads
-
- 3
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Motor processivity and speed determine structure and dynamics of microtubule-motor assemblies
eLife 12:e79402.
https://doi.org/10.7554/eLife.79402
Further reading
-
- Developmental Biology
- Physics of Living Systems
Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.
-
- Computational and Systems Biology
- Physics of Living Systems
Locomotion is a fundamental behavior of Caenorhabditis elegans (C. elegans). Previous works on kinetic simulations of animals helped researchers understand the physical mechanisms of locomotion and the muscle-controlling principles of neuronal circuits as an actuator part. It has yet to be understood how C. elegans utilizes the frictional forces caused by the tension of its muscles to perform sequenced locomotive behaviors. Here, we present a two-dimensional rigid body chain model for the locomotion of C. elegans by developing Newtonian equations of motion for each body segment of C. elegans. Having accounted for friction-coefficients of the surrounding environment, elastic constants of C. elegans, and its kymogram from experiments, our kinetic model (ElegansBot) reproduced various locomotion of C. elegans such as, but not limited to, forward-backward-(omega turn)-forward locomotion constituting escaping behavior and delta-turn navigation. Additionally, ElegansBot precisely quantified the forces acting on each body segment of C. elegans to allow investigation of the force distribution. This model will facilitate our understanding of the detailed mechanism of various locomotive behaviors at any given friction-coefficients of the surrounding environment. Furthermore, as the model ensures the performance of realistic behavior, it can be used to research actuator-controller interaction between muscles and neuronal circuits.
