The axonal actin-spectrin lattice acts as a tension buffering shock absorber

  1. Sushil Dubey
  2. Nishita Bhembre
  3. Shivani Bodas
  4. Sukh Veer
  5. Aurnab Ghose
  6. Andrew Callan-Jones  Is a corresponding author
  7. Pramod Pullarkat  Is a corresponding author
  1. Raman Research Institute, India
  2. Indian Institute of Science Education and Research, India
  3. Indian Institute of Science Education and Research, India
  4. Paris Diderot University, France

Abstract

Axons span extreme distances and are subjected to significant stretch deformations during limb movements or sudden head movements, especially during impacts. Yet, axon biomechanics, and its relation to the ultrastructure that allows axons to withstand mechanical stress, is poorly understood. Using a custom developed force apparatus, we demonstrate that chick dorsal root ganglion axons exhibit a tension buffering or strain-softening response, where its steady state elastic modulus decreases with increasing strain. We then explore the contributions from the various cytoskeletal components of the axon to show that the recently discovered membrane-associated actin-spectrin scaffold plays a prominent mechanical role. Finally, using a theoretical model, we argue that the actin-spectrin skeleton acts as an axonal tension buffer by reversibly unfolding repeat domains of the spectrin tetramers to release excess mechanical stress. Our results revise the current view point that microtubules and their associated proteins are the only significant load-bearing elements in axons.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Sushil Dubey

    Soft Condensed Matter Group, Raman Research Institute, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Nishita Bhembre

    Soft Condensed Matter, Raman Research Institute, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  3. Shivani Bodas

    Department of Biology, Indian Institute of Science Education and Research, Pune, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Sukh Veer

    Soft Condensed Matter Group, Raman Research Institute, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  5. Aurnab Ghose

    Biology, Indian Institute of Science Education and Research, Pune, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2053-3918
  6. Andrew Callan-Jones

    Laboratory of complex materials systems, Paris Diderot University, Paris, France
    For correspondence
    andrew.callan-jones@univ-paris-diderot.fr
    Competing interests
    The authors declare that no competing interests exist.
  7. Pramod Pullarkat

    Soft Condensed Matter Group, Raman Research Institute, Bangalore, India
    For correspondence
    pramod@rri.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2716-7575

Funding

Department of Biotechnology , Ministry of Science and Technology (BT/PR13244/GBD/27/245/2009)

  • Pramod Pullarkat

Department of Biotechnology , Ministry of Science and Technology (BT/PR13244/GBD/27/245/2009)

  • Aurnab Ghose

Science and Engineering Research Board (EMR/2016/003730)

  • Aurnab Ghose

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

Reviewing Editor

  1. Pierre Sens, Institut Curie, PSL Research University, CNRS, France

Publication history

  1. Received: September 10, 2019
  2. Accepted: April 6, 2020
  3. Accepted Manuscript published: April 8, 2020 (version 1)
  4. Version of Record published: April 29, 2020 (version 2)
  5. Version of Record updated: April 30, 2020 (version 3)

Copyright

© 2020, Dubey 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. Sushil Dubey
  2. Nishita Bhembre
  3. Shivani Bodas
  4. Sukh Veer
  5. Aurnab Ghose
  6. Andrew Callan-Jones
  7. Pramod Pullarkat
(2020)
The axonal actin-spectrin lattice acts as a tension buffering shock absorber
eLife 9:e51772.
https://doi.org/10.7554/eLife.51772

Further reading

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