TY - JOUR
T1 - Left-right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis
AU - Sato, Katsuhiko
AU - Hiraiwa, Tetsuya
AU - Maekawa, Emi
AU - Isomura, Ayako
AU - Shibata, Tatsuo
AU - Kuranaga, Erina
N1 - Funding Information:
Mochizuki for helpful comments and critical reading of the manuscript; and members of the Kuranaga, Hayashi, Nishimura and Wang laboratories for discussions. This work was supported by grants from the Japanese Ministry of Education, Science, Sports, Culture and Technology and by grants from the Uehara Memorial Foundation, the Kanae Foundation for the Promotion of Medical Science, the Takeda Science Foundation and the Mitsubishi Foundation.
PY - 2015/12/10
Y1 - 2015/12/10
N2 - 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.
AB - 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.
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U2 - 10.1038/ncomms10074
DO - 10.1038/ncomms10074
M3 - Article
C2 - 26656655
AN - SCOPUS:84949669162
SN - 2041-1723
VL - 6
JO - Nature Communications
JF - Nature Communications
M1 - 10074
ER -