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

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.

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Figure 1: Polarized junction remodelling underlies planar intercalation.
Figure 2: Myosin II-polarized localization.
Figure 3: Myosin II is required for junction remodelling.
Figure 4: Role of Rok during intercalation.

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Acknowledgements

We thank J. M. Philippe and J. Della Rovere for their technical help; A. Pelissier for the staining shown in Fig. 2c; R. Karess, D. Kiehart and H. Oda for sending key reagents; F. Pilot and C. Henderson for insights; F. Schweisguth for a useful suggestion; and S. Cohen, J. Ewbank, C. Henderson, S. Kerridge, F. Pilot, O. Pourquié and J. Pradel for comments on the manuscript. Research in the Lecuit laboratory is supported by an ATIP grant from the CNRS, by the Fondation pour la Recherche Médicale, the Association pour la Recherche contre le Cancer and the EMBO Young Investigator Programme.

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Correspondence to Thomas Lecuit.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

Cell intercalation is not controlled by posterior-midgut invagination. (JPG 136 kb)

Supplementary Movie

Time-lapse confocal images of an embryo expressing E-cadherin-GFP at low levels during cell intercalation. (MP4 186 kb)

Supplementary Figure & Movie Legends (DOC 21 kb)

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Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667–671 (2004). https://doi.org/10.1038/nature02590

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