1. Developmental Biology
  2. Neuroscience
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Stretching of the retinal pigment epithelium contributes to zebrafish optic cup morphogenesis

Research Article
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Cite this article as: eLife 2021;10:e63396 doi: 10.7554/eLife.63396

Abstract

The vertebrate eye-primordium consists of a pseudostratified neuroepithelium, the optic vesicle (OV), in which cells acquire neural retina or retinal pigment epithelium (RPE) fates. As these fates arise, the OV assumes a cup-shape, influenced by mechanical forces generated within the neural retina. Whether the RPE passively adapts to retinal changes or actively contributes to OV morphogenesis remains unexplored. We generated a zebrafish Tg(E1-bhlhe40:GFP) line to track RPE morphogenesis and interrogate its participation in OV folding. We show that, in virtual absence of proliferation, RPE cells stretch and flatten, thereby matching the retinal curvature and promoting OV folding. Localized interference with the RPE cytoskeleton disrupts tissue stretching and OV folding. Thus, extreme RPE flattening and accelerated differentiation are efficient solutions adopted by fast-developing species to enable timely optic cup formation. This mechanism differs in amniotes, in which proliferation drives RPE expansion with a much-reduced need of cell flattening.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all the graphs shown in the study

Article and author information

Author details

  1. Tania Moreno-Mármol

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Mario Ledesma-Terrón

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Noemi Tabanera

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Maria Jesús Martin-Bermejo

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Marcos J Cardozo

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Florencia Cavodeassi

    Institute of medical and Biomedical Education, St George's University, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4609-6258
  7. Paola Bovolenta

    Centro de Biología Molecular Severo Ochoa., CSIC-UAM, Cantoblanco, Spain
    For correspondence
    pbovolenta@cbm.csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1870-751X

Funding

Agencia Estatal de Investigación (PID2019-104186RB-100)

  • Paola Bovolenta

Ministerio de Economía, Industria y Competitividad, Gobierno de España (RED2018-102553-T)

  • Paola Bovolenta

Ministerio de Economía, Industria y Competitividad, Gobierno de España (BFU2016-75412-R)

  • Paola Bovolenta

Ministerio de Economía, Industria y Competitividad, Gobierno de España (BFU2014-55918-P)

  • Florencia Cavodeassi

BBVA Foundation (N[16]_BBM_BAS_0078)

  • Florencia Cavodeassi

Fundación Ramon Areces-2016 (no number)

  • Paola Bovolenta

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 E Bronner, California Institute of Technology, United States

Publication history

  1. Received: September 23, 2020
  2. Accepted: September 20, 2021
  3. Accepted Manuscript published: September 21, 2021 (version 1)

Copyright

© 2021, Moreno-Mármol 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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