Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades

  1. Lars Hering  Is a corresponding author
  2. Jamal-Eddine Bouameur
  3. Julian Reichelt
  4. Thomas M Magin
  5. Georg Mayer
  1. University of Kassel, Germany
  2. University of Leipzig, Germany

Abstract

Intermediate filament (IF) proteins, including nuclear lamins and cytoplasmic IF proteins, are essential cytoskeletal components of bilaterian cells. Despite their important role in protecting tissues against mechanical force, no cytoplasmic IF proteins have been convincingly identified in arthropods. Here we show that the ancestral cytoplasmic IF protein gene was lost in the entire panarthropod (onychophoran + tardigrade + arthropod) rather than arthropod lineage and that nuclear, lamin-derived proteins instead acquired new cytoplasmic roles at least three times independently in collembolans, copepods, and tardigrades. Transcriptomic and genomic data revealed three IF-protein genes in the tardigrade Hypsibius dujardini, one of which (cytotardin) occurs exclusively in the cytoplasm of epidermal and foregut epithelia, where it forms belt-like filaments around each epithelial cell. These results suggest that a lamin derivative has been co-opted to enhance tissue stability in tardigrades, a function otherwise served by cytoplasmic IF proteins in all other bilaterians.

Article and author information

Author details

  1. Lars Hering

    Department of Zoology, Institute of Biology, University of Kassel, Kassel, Germany
    For correspondence
    lars.hering@uni-kassel.de
    Competing interests
    The authors declare that no competing interests exist.
  2. Jamal-Eddine Bouameur

    Institute of Biology and Translational Center for Regenerative Medicine, University of Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Julian Reichelt

    Department of Zoology, Institute of Biology, University of Kassel, Kassel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Thomas M Magin

    Institute of Biology and Translational Center for Regenerative Medicine, University of Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Georg Mayer

    Department of Zoology, Institute of Biology, University of Kassel, Kassel, Germany
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Harald Herrmann, Deutsches Krebsforschungszentrum, Germany

Version history

  1. Received: August 25, 2015
  2. Accepted: February 2, 2016
  3. Accepted Manuscript published: February 3, 2016 (version 1)
  4. Accepted Manuscript updated: February 5, 2016 (version 2)
  5. Version of Record published: March 3, 2016 (version 3)

Copyright

© 2016, Hering 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. Lars Hering
  2. Jamal-Eddine Bouameur
  3. Julian Reichelt
  4. Thomas M Magin
  5. Georg Mayer
(2016)
Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades
eLife 5:e11117.
https://doi.org/10.7554/eLife.11117

Share this article

https://doi.org/10.7554/eLife.11117

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