Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a

Abstract

The mechanisms of formation of the distinct sensory organs of the inner ear and the non-sensory domains that separate them are still unclear. Here, we show that several sensory patches arise by progressive segregation from a common prosensory domain in the embryonic chicken and mouse otocyst. This process is regulated by mutually antagonistic signals: Notch signalling and Lmx1a. Notch-mediated lateral induction promotes prosensory fate. Some of the early Notch-active cells, however, are normally diverted from this fate and increasing lateral induction produces misshapen or fused sensory organs in the chick. Conversely Lmx1a (or cLmx1b in the chick) allows sensory organ segregation by antagonizing lateral induction and promoting commitment to the non-sensory fate. Our findings highlight the dynamic nature of sensory patch formation and the labile character of the sensory-competent progenitors, which could have facilitated the emergence of new inner ear organs and their functional diversification in the course of evolution.

Article and author information

Author details

  1. Zoe F Mann

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Héctor Gálvez

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. David Pedreno

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Ziqi Chen

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Elena Chrysostomou

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Magdalena Żak

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Miso Kang

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Elachumee Canden

    The Ear Institute, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Nicolas Daudet

    The Ear Institute, University College London, London, United Kingdom
    For correspondence
    n.daudet@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0441-0018

Funding

Biotechnology and Biological Sciences Research Council (BB/L003163/1 Project grant)

  • Zoe F Mann
  • Nicolas Daudet

Action on Hearing Loss (G76 Postdoc grant)

  • Magdalena Żak

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

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Ethics

Animal experimentation: All experimental procedures were carried out in accordance with the United Kingdom Scientific Procedures Act of 1986. All animals were handled according to protocols covered by a Home Office Animal Procedures Licence (PPL 70/8144) and approved by University College London local Ethics Committee.

Version history

  1. Received: November 3, 2017
  2. Accepted: December 2, 2017
  3. Accepted Manuscript published: December 4, 2017 (version 1)
  4. Version of Record published: December 11, 2017 (version 2)

Copyright

© 2017, Mann 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. Zoe F Mann
  2. Héctor Gálvez
  3. David Pedreno
  4. Ziqi Chen
  5. Elena Chrysostomou
  6. Magdalena Żak
  7. Miso Kang
  8. Elachumee Canden
  9. Nicolas Daudet
(2017)
Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a
eLife 6:e33323.
https://doi.org/10.7554/eLife.33323

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https://doi.org/10.7554/eLife.33323