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Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation

Author

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  • Claire Bertet

    (CNRS-INSERM-Université de la Méditerranée, Campus de Luminy, case 907)

  • Lawrence Sulak

    (CNRS-INSERM-Université de la Méditerranée, Campus de Luminy, case 907)

  • Thomas Lecuit

    (CNRS-INSERM-Université de la Méditerranée, Campus de Luminy, case 907)

Abstract

Shaping a developing organ or embryo relies on the spatial regulation of cell division and shape. However, morphogenesis also occurs through changes in cell-neighbourhood relationships produced by intercalation1,2. Intercalation poses a special problem in epithelia because of the adherens junctions, which maintain the integrity of the tissue. Here we address the mechanism by which an ordered process of cell intercalation directs polarized epithelial morphogenesis during germ-band elongation, the developmental elongation of the Drosophila embryo. Intercalation progresses because junctions are spatially reorganized in the plane of the epithelium following an ordered pattern of disassembly and reassembly. The planar remodelling of junctions is not driven by external forces at the tissue boundaries but depends on local forces at cell boundaries. Myosin II is specifically enriched in disassembling junctions, and its planar polarized localization and activity are required for planar junction remodelling and cell intercalation. This simple cellular mechanism provides a general model for polarized morphogenesis in epithelial organs.

Suggested Citation

  • Claire Bertet & Lawrence Sulak & Thomas Lecuit, 2004. "Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation," Nature, Nature, vol. 429(6992), pages 667-671, June.
    • Handle: RePEc:nat:nature:v:429:y:2004:i:6992:d:10.1038_nature02590
    DOI: 10.1038/nature02590
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    Cited by:

    1. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Daniel Sánchez-Gutiérrez & Aurora Sáez & Alberto Pascual & Luis M Escudero, 2013. "Topological Progression in Proliferating Epithelia Is Driven by a Unique Variation in Polygon Distribution," PLOS ONE, Public Library of Science, vol. 8(11), pages 1-8, November.
    3. 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.
    4. 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.
    5. João Firmino & Jean-Yves Tinevez & Elisabeth Knust, 2013. "Crumbs Affects Protein Dynamics In Anterior Regions Of The Developing Drosophila Embryo," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-10, March.
    6. Guilherme Ventura & Aboutaleb Amiri & Raghavan Thiagarajan & Mari Tolonen & Amin Doostmohammadi & Jakub Sedzinski, 2022. "Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. 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.
    8. Shun Li & Zong-Yuan Liu & Hao Li & Sijia Zhou & Jiaying Liu & Ningwei Sun & Kai-Fu Yang & Vanessa Dougados & Thomas Mangeat & Karine Belguise & Xi-Qiao Feng & Yiyao Liu & Xiaobo Wang, 2024. "Basal actomyosin pulses expand epithelium coordinating cell flattening and tissue elongation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Hiroyuki Uechi & Kazuki Fukushima & Ryota Shirasawa & Sayaka Sekine & Erina Kuranaga, 2022. "Inhibition of negative feedback for persistent epithelial cell–cell junction contraction by p21-activated kinase 3," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Tomer Stern & Stanislav Y Shvartsman & Eric F Wieschaus, 2020. "Template-based mapping of dynamic motifs in tissue morphogenesis," PLOS Computational Biology, Public Library of Science, vol. 16(8), pages 1-20, August.
    11. Sanjay Karki & Mehdi Saadaoui & Valentin Dunsing & Stephen Kerridge & Elise Silva & Jean-Marc Philippe & Cédric Maurange & Thomas Lecuit, 2023. "Serotonin signaling regulates actomyosin contractility during morphogenesis in evolutionarily divergent lineages," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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