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Genetic induction and mechanochemical propagation of a morphogenetic wave

Author

Listed:
  • Anaïs Bailles

    (IBDM–UMR7288
    Turing Centre for Living Systems)

  • Claudio Collinet

    (IBDM–UMR7288
    Turing Centre for Living Systems)

  • Jean-Marc Philippe

    (IBDM–UMR7288
    Turing Centre for Living Systems)

  • Pierre-François Lenne

    (IBDM–UMR7288
    Turing Centre for Living Systems)

  • Edwin Munro

    (University of Chicago)

  • Thomas Lecuit

    (IBDM–UMR7288
    Turing Centre for Living Systems
    Collège de France)

Abstract

Tissue morphogenesis arises from coordinated changes in cell shape driven by actomyosin contractions. Patterns of gene expression regionalize cell behaviours by controlling actomyosin contractility. Here we report two modes of control over Rho1 and myosin II (MyoII) activation in the Drosophila endoderm. First, Rho1–MyoII are induced in a spatially restricted primordium via localized transcription of the G-protein-coupled receptor ligand Fog. Second, a tissue-scale wave of Rho1–MyoII activation and cell invagination progresses anteriorly away from the primordium. The wave does not require sustained gene transcription, and is not governed by regulated Fog delivery. Instead, MyoII inhibition blocks Rho1 activation and propagation, revealing a mechanical feedback driven by MyoII. We find that MyoII activation and invagination in each row of cells drives adhesion to the vitelline membrane mediated by integrins, apical spreading, MyoII activation and invagination in the next row. Endoderm morphogenesis thus emerges from local transcriptional initiation and a mechanically driven cycle of cell deformation.

Suggested Citation

  • Anaïs Bailles & Claudio Collinet & Jean-Marc Philippe & Pierre-François Lenne & Edwin Munro & Thomas Lecuit, 2019. "Genetic induction and mechanochemical propagation of a morphogenetic wave," Nature, Nature, vol. 572(7770), pages 467-473, August.
    • Handle: RePEc:nat:nature:v:572:y:2019:i:7770:d:10.1038_s41586-019-1492-9
    DOI: 10.1038/s41586-019-1492-9
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    Cited by:

    1. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Julia Eckert & Benoît Ladoux & René-Marc Mège & Luca Giomi & Thomas Schmidt, 2023. "Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    3. Julien Fierling & Alphy John & Barthélémy Delorme & Alexandre Torzynski & Guy B. Blanchard & Claire M. Lye & Anna Popkova & Grégoire Malandain & Bénédicte Sanson & Jocelyn Étienne & Philippe Marmottan, 2022. "Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Stefan Harmansa & Alexander Erlich & Christophe Eloy & Giuseppe Zurlo & Thomas Lecuit, 2023. "Growth anisotropy of the extracellular matrix shapes a developing organ," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Özge Özgüç & Ludmilla de Plater & Varun Kapoor & Anna Francesca Tortorelli & Andrew G Clark & Jean-Léon Maître, 2022. "Cortical softening elicits zygotic contractility during mouse preimplantation development," PLOS Biology, Public Library of Science, vol. 20(3), pages 1-23, March.

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