Calponin-homology domain mediated bending of membrane associated actin filaments

  1. Saravanan Palani
  2. Sayantika Ghosh
  3. Esther Ivorra-Molla
  4. Scott Clarke
  5. Andrejus Suchenko
  6. Mohan K Balasubramanian  Is a corresponding author
  7. Darius Vasco Köster  Is a corresponding author
  1. Indian Institute of Science Bangalore, India
  2. University of Warwick, United Kingdom

Abstract

Actin filaments are central to numerous biological processes in all domains of life. Driven by the interplay with molecular motors, actin binding and actin modulating proteins, the actin cytoskeleton exhibits a variety of geometries. This includes structures with a curved geometry such as axon-stabilizing actin rings, actin cages around mitochondria and the cytokinetic actomyosin ring, which are generally assumed to be formed by short linear filaments held together by actin cross-linkers. However, whether individual actin filaments in these structures could be curved and how they may assume a curved geometry remains unknown. Here, we show that 'curly', a region from the IQGAP family of proteins from three different organisms, comprising the actin-binding calponin-homology domain and a C-terminal unstructured domain, stabilizes individual actin filaments in a curved geometry when anchored to lipid membranes. Whereas F-actin is semi-flexible with a persistence length of ~10 mm, binding of mobile curly within lipid membranes generates actin filament arcs and full rings of high curvature with radii below 1 mm. Higher rates of fully formed actin rings are observed in the presence of the actin-binding coiled-coil protein tropomyosin and when actin is directly polymerized on lipid membranes decorated with curly. Strikingly, curly induced actin filament rings contract upon the addition of muscle myosin II filaments and expression of curly in mammalian cells leads to highly curved actin structures in the cytoskeleton. Taken together, our work identifies a new mechanism to generate highly curved actin filaments, which opens a range of possibilities to control actin filament geometries, that can be used, for example, in designing synthetic cytoskeletal structures.

Data availability

All data generated or analysed during the study are included in the manuscript and supporting files. Source data files for the actin curvature measurements (Figures 1-4) have been deposited and are freely availabe on Dyrad.

The following data sets were generated

Article and author information

Author details

  1. Saravanan Palani

    Biochemistry, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1893-6777
  2. Sayantika Ghosh

    University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  3. Esther Ivorra-Molla

    University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  4. Scott Clarke

    University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  5. Andrejus Suchenko

    University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  6. Mohan K Balasubramanian

    University of Warwick, Coventry, United Kingdom
    For correspondence
    m.k.balasubramanian@warwick.ac.uk
    Competing interests
    Mohan K Balasubramanian, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1292-8602
  7. Darius Vasco Köster

    University of Warwick, Coventry, United Kingdom
    For correspondence
    D.Koester@warwick.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8530-5476

Funding

Wellcome Trust (WT 101885MA)

  • Mohan K Balasubramanian

H2020 European Research Council (ERC-2014-ADG N{degree sign} 671083)

  • Mohan K Balasubramanian

Wellcome Trust (ISSF-Warwick QBP RMRCB0058)

  • Darius Vasco Köster

Department of Biotechnology, Ministry of Science and Technology, India (DBT-IISc partnership grant)

  • Saravanan Palani

University of Warwick (Research development fund - RD19012)

  • Scott Clarke

University of Warwick (International Chancellor's Fellowship)

  • Sayantika Ghosh

University of Warwick (ARAP fellowship)

  • Esther Ivorra-Molla

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

Reviewing Editor

  1. Pekka Lappalainen, University of Helsinki, Finland

Version history

  1. Preprint posted: July 10, 2020 (view preprint)
  2. Received: July 15, 2020
  3. Accepted: July 15, 2021
  4. Accepted Manuscript published: July 16, 2021 (version 1)
  5. Version of Record published: July 27, 2021 (version 2)

Copyright

© 2021, Palani 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. Saravanan Palani
  2. Sayantika Ghosh
  3. Esther Ivorra-Molla
  4. Scott Clarke
  5. Andrejus Suchenko
  6. Mohan K Balasubramanian
  7. Darius Vasco Köster
(2021)
Calponin-homology domain mediated bending of membrane associated actin filaments
eLife 10:e61078.
https://doi.org/10.7554/eLife.61078

Share this article

https://doi.org/10.7554/eLife.61078

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