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Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis

Author

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  • Katsuhiko Sato

    (Laboratory for Physical Biology, RIKEN Center for Developmental Biology
    Present address: Research Institute for Electronic Science, Hokkaido University, Sapporo 001-0020, Japan.)

  • Tetsuya Hiraiwa

    (Laboratory for Physical Biology, RIKEN Center for Developmental Biology
    Present address: Department of Physics, Graduate School of Science, University of Tokyo, Hongo, Tokyo 113-0033, Japan.)

  • Emi Maekawa

    (Laboratory for Histogenetic Dynamics, RIKEN Center for Developmental Biology)

  • Ayako Isomura

    (Laboratory for Histogenetic Dynamics, RIKEN Center for Developmental Biology)

  • Tatsuo Shibata

    (Laboratory for Physical Biology, RIKEN Center for Developmental Biology
    Present address: Laboratory for Physical Biology, RIKEN Quantitative Biology Center, Kobe 650-0047, Japan.)

  • Erina Kuranaga

    (Laboratory for Histogenetic Dynamics, RIKEN Center for Developmental Biology
    Laboratory of Molecular Cell Biology and Development, Graduate School of Biostudies, Kyoto University
    Laboratory for Tissue Development Dynamics, Graduate School of Biological Sciences, Nara Institute of Science and Technology
    Laboratory for Histogenetic Dynamics, Graduate School of Life Sciences, Tohoku University)

Abstract

Morphogenetic epithelial movement occurs during embryogenesis and drives complex tissue formation. However, how epithelial cells coordinate their unidirectional movement while maintaining epithelial integrity is unclear. Here we propose a novel mechanism for collective epithelial cell movement based on Drosophila genitalia rotation, in which epithelial tissue rotates clockwise around the genitalia. We found that this cell movement occurs autonomously and requires myosin II. The moving cells exhibit repeated left–right-biased junction remodelling, while maintaining adhesion with their neighbours, in association with a polarized myosin II distribution. Reducing myosinID, known to cause counter-clockwise epithelial-tissue movement, reverses the myosin II distribution. Numerical simulations revealed that a left–right asymmetry in cell intercalation is sufficient to induce unidirectional cellular movement. The cellular movement direction is also associated with planar cell-shape chirality. These findings support a model in which left–right asymmetric cell intercalation within an epithelial sheet drives collective cellular movement in the same direction.

Suggested Citation

  • Katsuhiko Sato & Tetsuya Hiraiwa & Emi Maekawa & Ayako Isomura & Tatsuo Shibata & Erina Kuranaga, 2015. "Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis," Nature Communications, Nature, vol. 6(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms10074
    DOI: 10.1038/ncomms10074
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    Cited by:

    1. Su Ee Tan & David Strutt, 2025. "Tissue shear as a cue for aligning planar polarity in the developing Drosophila wing," Nature Communications, Nature, vol. 16(1), pages 1-23, December.

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