A tug of war between filament treadmilling and myosin induced contractility generates actin ring

Abstract

In most eukaryotic cells, actin filaments assemble into a shell-like actin cortex under the plasma membrane, controlling cellular morphology, mechanics, and signaling. The actin cortex is highly polymorphic, adopting diverse forms such as the ring-like structures found in podosomes, axonal rings, and immune synapses. The biophysical principles that underlie the formation of actin rings and cortices remain unknown. Using a molecular simulation platform, called MEDYAN, we discovered that varying the filament treadmilling rate and myosin concentration induces a finite size phase transition in actomyosin network structures. We found that actomyosin networks condense into clusters at low treadmilling rates or high myosin concentration but form ring-like or cortex-like structures at high treadmilling rates and low myosin concentration. This mechanism is supported by our corroborating experiments on live T cells, which exhibit ring-like actin networks upon activation by stimulatory antibody. Upon disruption of filament treadmilling or enhancement of myosin activity, the pre-existing actin rings are disrupted into actin clusters or collapse towards the network center respectively. Our analyses suggest that the ring-like actin structure is a preferred state of low mechanical energy, which is, importantly, only reachable at sufficiently high treadmilling rates.

Data availability

Source Data files for experiments and the modeling code are available in Digital Repository at the University of Maryland(DRUM): https://doi.org/10.13016/9t26-ovid.

Article and author information

Author details

  1. Qin Ni

    Department of Chemical and Biomolecular Engineering, University of Maryland, College Park, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kaustubh Wagh

    Department of Physics, University of Maryland, College Park, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8514-027X
  3. Aashli Pathni

    Biological Sciences Graduate Program, University of Maryland, College Park, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4196-890X
  4. Haoran Ni

    Biophysics Program, University of Maryland, College Park, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Vishavdeep Vashisht

    Biophysics Program, University of Maryland, College Park, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Arpita Upadhyaya

    Department of Physics, University of Maryland, College Park, College Park, United States
    For correspondence
    arpitau@umd.edu
    Competing interests
    The authors declare that no competing interests exist.
  7. Garegin A Papoian

    Institute for Physical Science and Technology, University of Maryland, College Park, College Park, United States
    For correspondence
    gpapoian@umd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8580-3790

Funding

National Science Foundation (CHE-1800418)

  • Garegin A Papoian

National Science Foundation (PHY-1806903)

  • Garegin A Papoian

National Science Foundation (PHY-1607645)

  • Arpita Upadhyaya

National Institutes of Health (R01 GM131054)

  • Arpita Upadhyaya

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

Reviewing Editor

  1. Alphee Michelot, Institut de Biologie du Développement, France

Version history

  1. Preprint posted: June 6, 2021 (view preprint)
  2. Received: August 12, 2022
  3. Accepted: October 6, 2022
  4. Accepted Manuscript published: October 21, 2022 (version 1)
  5. Version of Record published: November 21, 2022 (version 2)

Copyright

© 2022, Ni 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. Qin Ni
  2. Kaustubh Wagh
  3. Aashli Pathni
  4. Haoran Ni
  5. Vishavdeep Vashisht
  6. Arpita Upadhyaya
  7. Garegin A Papoian
(2022)
A tug of war between filament treadmilling and myosin induced contractility generates actin ring
eLife 11:e82658.
https://doi.org/10.7554/eLife.82658

Share this article

https://doi.org/10.7554/eLife.82658

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