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Mechanical control of neural plate folding by apical domain alteration

Author

Listed:
  • Miho Matsuda

    (Icahn School of Medicine at Mount Sinai)

  • Jan Rozman

    (University of Oxford)

  • Sassan Ostvar

    (Columbia University)

  • Karen E. Kasza

    (Columbia University)

  • Sergei Y. Sokol

    (Icahn School of Medicine at Mount Sinai)

Abstract

Vertebrate neural tube closure is associated with complex changes in cell shape and behavior, however, the relative contribution of these processes to tissue folding is not well understood. At the onset of Xenopus neural tube folding, we observed alternation of apically constricted and apically expanded cells. This apical domain heterogeneity was accompanied by biased cell orientation along the anteroposterior axis, especially at neural plate hinges, and required planar cell polarity signaling. Vertex models suggested that dispersed isotropically constricting cells can cause the elongation of adjacent cells. Consistently, in ectoderm, cell-autonomous apical constriction was accompanied by neighbor expansion. Thus, a subset of isotropically constricting cells may initiate neural plate bending, whereas a ‘tug-of-war’ contest between the force-generating and responding cells reduces its shrinking along the body axis. This mechanism is an alternative to anisotropic shrinking of cell junctions that are perpendicular to the body axis. We propose that apical domain changes reflect planar polarity-dependent mechanical forces operating during neural folding.

Suggested Citation

  • Miho Matsuda & Jan Rozman & Sassan Ostvar & Karen E. Kasza & Sergei Y. Sokol, 2023. "Mechanical control of neural plate folding by apical domain alteration," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43973-x
    DOI: 10.1038/s41467-023-43973-x
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    References listed on IDEAS

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    1. 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.
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    3. Jan Rozman & Matej Krajnc & Primož Ziherl, 2020. "Collective cell mechanics of epithelial shells with organoid-like morphologies," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    4. Soline Chanet & Callie J. Miller & Eeshit Dhaval Vaishnav & Bard Ermentrout & Lance A. Davidson & Adam C. Martin, 2017. "Actomyosin meshwork mechanosensing enables tissue shape to orient cell force," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    5. Olga Ossipova & Kyeongmi Kim & Blue B. Lake & Keiji Itoh & Andriani Ioannou & Sergei Y. Sokol, 2014. "Role of Rab11 in planar cell polarity and apical constriction during vertebrate neural tube closure," Nature Communications, Nature, vol. 5(1), pages 1-8, September.
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