Unified quantitative characterization of epithelial tissue development

  1. Boris Guirao
  2. Stéphane Rigaud
  3. Floris Bosveld
  4. Anaïs Bailles
  5. Jesus Lopez-Gay
  6. Shuji Ishihara
  7. Kaoru Sugimura
  8. François Graner
  9. Yohanns Bellaïche  Is a corresponding author
  1. Institut Curie, France
  2. Aix Marseille Université, France
  3. Meiji University, Japan
  4. Kyoto University, Japan
  5. Univsersité Paris-Diderot, France

Abstract

Understanding the mechanisms regulating development requires a quantitative characterization of cell processes including cell divisions, rearrangements, cell size and shape changes, and apoptoses. We developed a multiscale formalism that unifies and relates the characterizations of each individual cell process and of epithelial tissue growth and morphogenesis during development. We applied this formalism to two Drosophila proliferative tissues and by analyzing more than 9 million cell contours, we obtained comprehensive statistical maps of morphogenetic events linking cell and tissue scale dynamics. By quantifying each cell process separately in both wild-type and mutant conditions, we analyzed the roles of cell proliferation and its interplay with cell rearrangements and cell shape changes. Furthermore, by combining the formalism with mechanical stress measurement, we uncovered unexpected interplays between the patterns of tissue elongation, cell division orientation and stress orientations. Collectively, our formalism provides a novel and rigorous approach to uncover mechanisms governing tissue development.

Article and author information

Author details

  1. Boris Guirao

    Polarity, Division and Morphogenesis Team, Génétique et biologie du développement, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Stéphane Rigaud

    Polarity, Division and Morphogenesis Team, Génétique et biologie du développement, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Floris Bosveld

    Polarity, Division and Morphogenesis Team, Génétique et biologie du développement, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Anaïs Bailles

    Institut de Biologie du Développement de Marseille, Aix Marseille Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Jesus Lopez-Gay

    Polarity, Division and Morphogenesis Team, Génétique et biologie du développement, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Shuji Ishihara

    Department of Physics, School of Science and Technology, Meiji University, Kanagawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Kaoru Sugimura

    Institute for Integrated Cell-Material Sceinces, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. François Graner

    Laboratoire Matière et Systèmes Complexes, Univsersité Paris-Diderot, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Yohanns Bellaïche

    Polarity, Division and Morphogenesis Team, Génétique et biologie du développement, Institut Curie, Paris, France
    For correspondence
    yohanns.bellaiche@curie.fr
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Publication history

  1. Received: May 6, 2015
  2. Accepted: November 3, 2015
  3. Accepted Manuscript published: December 12, 2015 (version 1)
  4. Accepted Manuscript updated: December 15, 2015 (version 2)
  5. Version of Record published: March 22, 2016 (version 3)

Copyright

© 2015, Guirao 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. Boris Guirao
  2. Stéphane Rigaud
  3. Floris Bosveld
  4. Anaïs Bailles
  5. Jesus Lopez-Gay
  6. Shuji Ishihara
  7. Kaoru Sugimura
  8. François Graner
  9. Yohanns Bellaïche
(2015)
Unified quantitative characterization of epithelial tissue development
eLife 4:e08519.
https://doi.org/10.7554/eLife.08519

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