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Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis

Nature Cell Biology volume 10, pages 1401–1410 (2008)Cite this article

Abstract

The morphogenesis of developing embryos and organs relies on the ability of cells to remodel their contacts with neighbouring cells. Using quantitative modelling and laser nano-dissection, we probed the mechanics of a morphogenetic process, the elongation of Drosophila melanogaster embryos, which results from polarized cell neighbour exchanges. We show that anisotropy of cortical tension at apical cell junctions is sufficient to drive tissue elongation. We estimated its value through comparisons between in silico and in vivo data using various tissue descriptors. Nano-dissection of the actomyosin network indicates that tension is anisotropically distributed and depends on myosin II accumulation. Junction relaxation after nano-dissection also suggests that cortical elastic forces are dominant in this process. Interestingly, fluctuations in vertex position (points where three or more cells meet) facilitate neighbour exchanges. We delineate the contribution of subcellular tensile activity polarizing junction remodelling, and the permissive role of vertex fluctuations during tissue elongation.

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Figure 1: Mechanics of local cell rearrangements during tissue elongation in Drosophila embryos.
Figure 2: Cortical elasticity and line tension models.
Figure 3: Model of tension anisotropy and cell intercalation.
Figure 4: Tension anisotropy is sufficient to drive tissue elongation.
Figure 5: Comparison of cell patterns in vivo and in silico using different descriptors.
Figure 6: Forces during cell intercalation revealed by laser nano-dissection.
Figure 7: Mechanics of high-order structures.

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Acknowledgements

We thank all the members of the Lenne and Lecuit labs for technical help, in particular M. Cavey and C. Bertet. We thank C. Bertet for Fig. 1c. We are grateful for D. Kiehart, H. Oda and C. Field for the gift of flies and antibodies. We thank everyone, especially Loic Le Goff for fruitful discussions during the course of this project. K. Brakke is acknowledged for help with Surface Evolver, F. Graner and A. Nicolas for insights and useful suggestions on the manuscript, and J. Axelrod, E. Munro, O. Pourquié and members of the Lenne and Lecuit labs for critical reading of the manuscript. Supported by the CNRS and an ANR-Blanc grant to T.L. and P.-F.L. M.R. is supported by a Bourse Région Entreprise (Amplitude Systems), and P.V. is supported by a Postdoctoral Fellowship from ANR.

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  1. Matteo Rauzi and Pascale Verant: These authors contributed equally to this work.

Authors and Affiliations

  1. Institut Fresnel, Université Aix-Marseille III, CNRS, Ecole Centrale Marseille, UMR 6133, Domaine Universitaire de St Jérôme, 13397, Marseille cedex 20, France

    Matteo Rauzi, Pascale Verant & Pierre-François Lenne

  2. IBDML, Université Aix-Marseille Université II, CNRS, UMR 6216, Campus de Luminy case 907, Marseille cedex 09, France

    Matteo Rauzi, Pascale Verant & Thomas Lecuit

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  1. Matteo Rauzi
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  2. Pascale Verant
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  4. Pierre-François Lenne
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Contributions

P.-F.L. and T.L. conceived and designed the project; P.-F.L., T.L., M.R. and P.V analysed the data; P.-F.L. and M.R. designed and built the set-up for nano-dissection experiments; M.R. performed the nano-dissection experiments; P.V. designed and wrote the image analysis tool with P.-F.L. and conducted the quantitative studies of germband elongation movies; P.-F.L. performed the simulations; P.-F.L. and T.L. wrote the paper; all authors read and edited the manuscript.

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Correspondence to Thomas Lecuit or Pierre-François Lenne.

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The authors declare no competing financial interests.

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Rauzi, M., Verant, P., Lecuit, T. et al. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol 10, 1401–1410 (2008). https://doi.org/10.1038/ncb1798

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