1. Physics of Living Systems
  2. Developmental Biology
Download icon

Unified quantitative characterization of epithelial tissue development

  1. Boris Guirao
  2. Stéphane U 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
Tools and Resources
  • Cited 79
  • Views 5,312
  • Annotations
Cite this article as: eLife 2015;4:e08519 doi: 10.7554/eLife.08519

Abstract

Understanding the mechanisms regulating development requires a quantitative characterization of cell divisions, rearrangements, cell size and shape changes, and apoptoses. We developed a multiscale formalism that relates the characterizations of each cell process to tissue growth and morphogenesis. Having validated the formalism on computer simulations, we quantifed separately all morphogenetic events in the Drosophila wing and dorsal thorax pupal epithelia to obtain comprehensive statistical maps linking cell and tissue scale dynamics. While globally cell shape changes, rearrangements and divisions all signifcantly participate in tissue morphogenesis, locally, their relative participations display major variations in space and time. By blocking division we analyzed the impact of division on rearrangements, cell shape changes and tissue morphogenesis. Finally, by combining the formalism with mechanical stress measurement, we evidenced unexpected interplays between patterns of tissue elongation, cell division and stress. 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 U 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.

Metrics

  • 5,312
    Page views
  • 1,519
    Downloads
  • 79
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Categories and tags

Research organism

Further reading

    1. Cell Biology
    2. Physics of Living Systems

    Exceptional stability of a perilipin on lipid droplets depends on its polar residues, suggesting multimeric assembly

    Manuel Giménez-Andrés et al.
    Research Article

    Numerous proteins target lipid droplets (LDs) through amphipathic helices (AHs). It is generally assumed that AHs insert bulky hydrophobic residues in packing defects at the LD surface. However, this model does not explain the targeting of perilipins, the most abundant and specific amphipathic proteins of LDs, which are weakly hydrophobic. A striking example is Plin4, whose gigantic and repetitive AH lacks bulky hydrophobic residues. Using a range of complementary approaches, we show that Plin4 forms a remarkably immobile and stable protein layer at the surface of cellular or in vitro generated oil droplets, and decreases LD size. Plin4 AH stability on LDs is exquisitely sensitive to the nature and distribution of its polar residues. These results suggest that Plin4 forms stable arrangements of adjacent AHs via polar/electrostatic interactions, reminiscent of the organization of apolipoproteins in lipoprotein particles, thus pointing to a general mechanism of AH stabilization via lateral interactions.

    1. Physics of Living Systems

    Ligand sensing enhances bacterial flagellar motor output via stator recruitment

    Farha Naaz et al.
    Research Article

    It is well known that flagellated bacteria, such as Escherichia coli, sense chemicals in their environment by a chemoreceptor and relay signals via a well-characterised signalling pathway to the flagellar motor. It is widely accepted that the signals change the rotation bias of the motor without influencing the motor speed. Here, we present results to the contrary and show that the bacteria is also capable of modulating motor speed on merely sensing a ligand. Step changes in concentration of non-metabolisable ligand cause temporary recruitment of stator units leading to a momentary increase in motor speeds. For metabolisable ligand, the combined effect of sensing and metabolism leads to higher motor speeds for longer durations. Experiments performed with mutant strains delineate the role of metabolism and sensing in the modulation of motor speed and show how speed changes along with changes in bias can significantly enhance response to changes in its environment.

    1. Computational and Systems Biology
    2. Physics of Living Systems

    Topological signatures in regulatory network enable phenotypic heterogeneity in small cell lung cancer

    Lakshya Chauhan et al.
    Research Article Updated

    Phenotypic (non-genetic) heterogeneity has significant implications for the development and evolution of organs, organisms, and populations. Recent observations in multiple cancers have unraveled the role of phenotypic heterogeneity in driving metastasis and therapy recalcitrance. However, the origins of such phenotypic heterogeneity are poorly understood in most cancers. Here, we investigate a regulatory network underlying phenotypic heterogeneity in small cell lung cancer, a devastating disease with no molecular targeted therapy. Discrete and continuous dynamical simulations of this network reveal its multistable behavior that can explain co-existence of four experimentally observed phenotypes. Analysis of the network topology uncovers that multistability emerges from two teams of players that mutually inhibit each other, but members of a team activate one another, forming a ‘toggle switch’ between the two teams. Deciphering these topological signatures in cancer-related regulatory networks can unravel their ‘latent’ design principles and offer a rational approach to characterize phenotypic heterogeneity in a tumor.