Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction

  1. Sylvia Dyballa
  2. Thierry Savy
  3. Philipp Germann
  4. Karol Mikula
  5. Mariana Remesikova
  6. Róbert Špir
  7. Andrea Zecca
  8. Nadine Peyriéras
  9. Cristina Pujades  Is a corresponding author
  1. Universitat Pompeu Fabra, Spain
  2. USR3695 CNRS, France
  3. Center for Genomic Regulation, Spain
  4. Slovak University of Technology, Slovakia

Abstract

Reconstructing the lineage of cells is central to understanding how the wide diversity of cell types develops. Here, we provide the neurosensory lineage reconstruction of a complex sensory organ, the inner ear, by imaging zebrafish embryos in vivo over an extended timespan, combining cell tracing and cell fate marker expression over time. We deliver the first dynamic map of early neuronal and sensory progenitor pools in the whole otic vesicle. It highlights the remodeling of the neuronal progenitor domain upon neuroblast delamination, and reveals that the order and place of neuroblasts' delamination from the otic epithelium prefigure their position within the SAG. Sensory and non-sensory domains harbor different proliferative activity contributing distinctly to the overall growth of the structure. Therefore, the otic vesicle case exemplifies a generic morphogenetic process where spatial and temporal cues regulate cell fate and functional organization of the rudiment of the definitive organ.

Article and author information

Author details

  1. Sylvia Dyballa

    Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Thierry Savy

    Multilevel Dynamics in Morphogenesis Unit, USR3695 CNRS, Gif sur Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Philipp Germann

    Systems Biology Unit, Center for Genomic Regulation, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2057-4883
  4. Karol Mikula

    Department of Mathematics, Slovak University of Technology, Bratislava, Slovakia
    Competing interests
    The authors declare that no competing interests exist.
  5. Mariana Remesikova

    Department of Mathematics, Slovak University of Technology, Bratislava, Slovakia
    Competing interests
    The authors declare that no competing interests exist.
  6. Róbert Špir

    Department of Mathematics, Slovak University of Technology, Bratislava, Slovakia
    Competing interests
    The authors declare that no competing interests exist.
  7. Andrea Zecca

    Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Nadine Peyriéras

    Multilevel Dynamics in Morphogenesis Unit, USR3695 CNRS, Gif sur Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Cristina Pujades

    Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
    For correspondence
    cristina.pujades@upf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6423-7451

Funding

Ministerio de Economía y Competitividad (BFU2012-31994)

  • Cristina Pujades

Unidad de Excelencia María de Maetzu (2015-19 MDM-2014-0370 to DCEXS-UPF)

  • Sylvia Dyballa
  • Andrea Zecca
  • Cristina Pujades

Centro de Excelencia Severo Ochoa (2013-17 SEV-2012-0208 to CRG)

  • Philipp Germann

Agence Nationale de la Recherche (ANR-10-INBS-04)

  • Nadine Peyriéras

Agence Nationale de la Recherche (ANR-11-EQPX-0029)

  • Nadine Peyriéras

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (SINERGIA CRSII3 141918)

  • Philipp Germann

Becas de la Generalitat de Catalunya (Predoctoral FI-fellowship)

  • Sylvia Dyballa
  • Andrea Zecca

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

Ethics

Animal experimentation: This study was performed in strict accordance with the European Regulations. Zebrafish embryos were obtained by mating of adult fish using standard methods. All fish strains were maintained individually as inbred lines. All protocols used have been approved by the Institutional Animal Care and Use Ethic Committee (PRBB-IACUEC), and implemented according to national and European regulations. All experiments were carried out in accordance with the principles of the 3Rs. All our experiments were carried out using the CPC16-008/9125 protocol approved by the Generalitat of Catalonia.

Reviewing Editor

  1. Tanya T Whitfield, University of Sheffield, United Kingdom

Publication history

  1. Received: October 11, 2016
  2. Accepted: December 23, 2016
  3. Accepted Manuscript published: January 4, 2017 (version 1)
  4. Accepted Manuscript updated: January 12, 2017 (version 2)
  5. Version of Record published: January 18, 2017 (version 3)

Copyright

© 2017, Dyballa 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. Sylvia Dyballa
  2. Thierry Savy
  3. Philipp Germann
  4. Karol Mikula
  5. Mariana Remesikova
  6. Róbert Špir
  7. Andrea Zecca
  8. Nadine Peyriéras
  9. Cristina Pujades
(2017)
Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction
eLife 6:e22268.
https://doi.org/10.7554/eLife.22268
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