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Subcellular analysis of pigeon hair cells implicates vesicular trafficking in cuticulosome formation and maintenance

  1. Simon Nimpf
  2. Erich Pascal Malkemper
  3. Mattias Lauwers
  4. Lyubov Ushakova
  5. Gregory Nordmann
  6. Andrea Wenninger-Weinzierl
  7. Thomas R Burkard
  8. Sonja Jacob
  9. Thomas Heuser
  10. Guenter P Resch
  11. David A Keays  Is a corresponding author
  1. Research Institute of Molecular Pathology, Austria
  2. Campus Science Support Facilities GmbH, Austria
  3. Nexperion, Austria
Research Article
  • Cited 5
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Cite this article as: eLife 2017;6:e29959 doi: 10.7554/eLife.29959

Abstract

Hair cells are specialized sensors located in the inner ear that enable the transduction of sound, motion, and gravity into neuronal impulses. In birds some hair cells contain an iron-rich organelle, the cuticulosome, that has been implicated in the magnetic sense. Here, we exploit histological, transcriptomic and tomographic methods to investigate the development of cuticulosomes, as well as the molecular and subcellular architecture of cuticulosome positive hair cells. We show that this organelle forms rapidly after hatching in a process that involves vesicle fusion and nucleation of ferritin nanoparticles. We further report that transcripts involved in endocytosis, extracellular exosomes, and metal ion binding are differentially expressed in cuticulosome positive hair cells. These data suggest that the cuticulosome and the associated molecular machinery regulate the concentration of iron within the labyrinth of the inner ear, which might indirectly tune a magnetic sensor that relies on electromagnetic induction.

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Author details

  1. Simon Nimpf

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6522-6172

  2. Erich Pascal Malkemper

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  3. Mattias Lauwers

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  4. Lyubov Ushakova

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  5. Gregory Nordmann

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  6. Andrea Wenninger-Weinzierl

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  7. Thomas R Burkard

    Research Institute of Molecular Pathology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  8. Sonja Jacob

    Electron Microscopy Facility, Campus Science Support Facilities GmbH, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  9. Thomas Heuser

    Electron Microscopy Facility, Campus Science Support Facilities GmbH, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  10. Guenter P Resch

    Nexperion, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

  11. David A Keays

    Research Institute of Molecular Pathology, Vienna, Austria
    For correspondence
    keays@imp.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8343-8002

Funding

Austrian Science Fund (Y726)

  • Thomas R Burkard

Horizon 2020 Framework Programme (336724)

  • David A Keays

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

Ethics

Animal experimentation: All experiments were conducted in accordance with an existing ethical framework GZ: 214635/2015/20 granted by the City of Vienna (Magistratsabteilung 58).

Reviewing Editor

  1. Jeremy Nathans, Johns Hopkins University School of Medicine, United States

Publication history

  1. Received: June 27, 2017
  2. Accepted: November 11, 2017
  3. Accepted Manuscript published: November 15, 2017 (version 1)
  4. Version of Record published: November 22, 2017 (version 2)
  5. Version of Record updated: November 23, 2017 (version 3)

Copyright

© 2017, Nimpf 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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