1. Cell Biology
  2. Developmental Biology
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Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis

  1. María Nicolás-Pérez
  2. Franz Kuchling
  3. Joaquín Letelier
  4. Rocío Polvillo
  5. Jochen Wittbrodt
  6. Juan R Martínez-Morales  Is a corresponding author
  1. Centro Andaluz de Biología del Desarrollo, Spain
  2. University of Heidelberg, Germany
Research Article
  • Cited 25
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Cite this article as: eLife 2016;5:e15797 doi: 10.7554/eLife.15797

Abstract

Contractile actomyosin networks have been shown to power tissue morphogenesis. Although the basic cellular machinery generating mechanical tension appears largely conserved, tensions propagate in unique ways within each tissue. Here we use the vertebrate eye as a paradigm to investigate how tensions are generated and transmitted during the folding of a neuroepithelial layer. We record membrane pulsatile behavior and actomyosin dynamics during zebrafish optic cup morphogenesis by live imaging. We show that retinal neuroblasts undergo fast oscillations and that myosin condensation correlates with episodic contractions that progressively reduce basal feet area. Interference with lamc1 function impairs basal contractility and optic cup folding. Mapping of tensile forces by laser cutting uncover a developmental window in which local ablations trigger the displacement of the entire tissue. Our work shows that optic cup morphogenesis is driven by a constriction mechanism and indicates that supra-cellular transmission of mechanical tension depends on ECM attachment.

Article and author information

Author details

  1. María Nicolás-Pérez

    Centro Andaluz de Biología del Desarrollo, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Franz Kuchling

    Centro Andaluz de Biología del Desarrollo, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Joaquín Letelier

    Centro Andaluz de Biología del Desarrollo, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Rocío Polvillo

    Centro Andaluz de Biología del Desarrollo, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Jochen Wittbrodt

    Centre for Organismal Studies, COS, University of Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8550-7377
  6. Juan R Martínez-Morales

    Centro Andaluz de Biología del Desarrollo, Seville, Spain
    For correspondence
    jrmarmor@upo.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4650-4293

Funding

Ministerio de Economía y Competitividad (BFU2011-22916)

  • Juan R Martínez-Morales

Ministerio de Economía y Competitividad (P11-CVI-7256)

  • Juan R Martínez-Morales

Ministerio de Economía y Competitividad (BFU2014-53765)

  • Juan R Martínez-Morales

Ministerio de Economía y Competitividad (BFU2014-55738-REDT)

  • Juan R Martínez-Morales

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 conform national (RD53/2013) and European Community standards for the use of zebrafish in experimentation . This work has been approved by three independent comittees on the Ethics of Animal Experiments at the Pablo de Olavide University, the National Reseach Council (CSIC) and the local Goverment of Andalucia (permit number 26-11-14-164).

Reviewing Editor

  1. Suzanne Eaton, Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Publication history

  1. Received: March 5, 2016
  2. Accepted: October 27, 2016
  3. Accepted Manuscript published: October 31, 2016 (version 1)
  4. Version of Record published: November 15, 2016 (version 2)

Copyright

© 2016, Nicolás-Pérez 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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