Apical contacts stemming from incomplete delamination guide progenitor cell allocation through a dragging mechanism

  1. Eduardo Pulgar
  2. Cornelia Schwayer
  3. Néstor Guerrero
  4. Loreto López
  5. Susana Márquez
  6. Steffen Härtel
  7. Rodrigo Soto
  8. Carl-Philipp Heisenberg
  9. Miguel Concha  Is a corresponding author
  1. Universidad de Chile, Chile
  2. Institute of Science and Technology Austria (IST Austria), Austria
  3. Institute of Science and Technology Austria, Austria

Abstract

The developmental strategies used by progenitor cells to allow a safe journey from their induction place towards the site of terminal differentiation are still poorly understood. Here we uncovered a mechanism of progenitor cell allocation that stems from an incomplete process of epithelial delamination that allows progenitors to coordinate their movement with adjacent extra-embryonic tissues. Progenitors of the zebrafish laterality organ originate from the superficial epithelial enveloping layer by an apical constriction process of cell delamination. During this process, progenitors retain long-lasting apical contacts that enable the epithelial layer to pull a subset of progenitors on their way to the vegetal pole. The remaining delaminated cells follow the movement of apically attached progenitors by a protrusion-dependent cell-cell contact mechanism, avoiding sequestration by the adjacent endoderm, ensuring their collective fate and allocation at the site of differentiation. Thus, we reveal that incomplete delamination serves as a cellular platform for coordinated tissue movements during development.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 2, 3, 4, 5, 6, 7 and 8.

Article and author information

Author details

  1. Eduardo Pulgar

    Institute of Biomedical Sciences, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  2. Cornelia Schwayer

    no Department, Institute of Science and Technology Austria (IST Austria), Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Néstor Guerrero

    Institute of Biomedical Sciences, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  4. Loreto López

    Institute of Biomedical Sciences, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  5. Susana Márquez

    Physics Department, FCFM, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  6. Steffen Härtel

    Institute of Biomedical Sciences, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  7. Rodrigo Soto

    Physics Department, FCFM, Universidad de Chile, Santiago, Chile
    Competing interests
    The authors declare that no competing interests exist.
  8. Carl-Philipp Heisenberg

    Life Sciences, Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0912-4566
  9. Miguel Concha

    Institute of Biomedical Sciences, Universidad de Chile, Santiago, Chile
    For correspondence
    miguelconcha@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3353-9398

Funding

Fondo Nacional de Desarrollo Científico y Tecnológico (1190806)

  • Eduardo Pulgar
  • Steffen Härtel
  • Miguel Concha

Comisión Nacional de Investigación Científica y Tecnológica (REDES170212,REDES130020)

  • Eduardo Pulgar
  • Steffen Härtel
  • Miguel Concha

H2020 European Research Council (Advanced grant 742573)

  • Carl-Philipp Heisenberg

Fondo Nacional de Desarrollo Científico y Tecnológico (1161274,1181823)

  • Steffen Härtel
  • Miguel Concha

Instituto Milenio de Neurociencia Biomedica (ICN09_015)

  • Eduardo Pulgar
  • Steffen Härtel
  • Miguel Concha

Millennium Nucleus Physics of Active Matter from ANID (ANID)

  • Susana Márquez
  • Rodrigo Soto
  • Miguel Concha

Fondo de Equipamiento Cientifico y Tecnologico (EQM130051)

  • Steffen Härtel
  • Miguel Concha

Fondo de Financiamiento de Centros de Investigacion en Areas Prioritarias (15150012)

  • Miguel Concha

Fondo Nacional de Desarrollo Científico y Tecnológico (3160478)

  • Eduardo Pulgar

Comisión Nacional de Investigación Científica y Tecnológica (PIA ACT-1402)

  • Steffen Härtel
  • Miguel Concha

Comisión Nacional de Investigación Científica y Tecnológica (PIA ACT192015)

  • Miguel Concha

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

Ethics

Animal experimentation: Fish care and procedures were approved by the Ethical Review Committee and comply with the Animals Scientific Procedures Act 0466 (Protocol CBA#0466 FMUCH).

Copyright

© 2021, Pulgar 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. Eduardo Pulgar
  2. Cornelia Schwayer
  3. Néstor Guerrero
  4. Loreto López
  5. Susana Márquez
  6. Steffen Härtel
  7. Rodrigo Soto
  8. Carl-Philipp Heisenberg
  9. Miguel Concha
(2021)
Apical contacts stemming from incomplete delamination guide progenitor cell allocation through a dragging mechanism
eLife 10:e66483.
https://doi.org/10.7554/eLife.66483

Share this article

https://doi.org/10.7554/eLife.66483

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