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Tissue elongation requires oscillating contractions of a basal actomyosin network

Nature Cell Biology volume 12, pages 1133–1142 (2010)Cite this article

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Abstract

Understanding how molecular dynamics leads to cellular behaviours that ultimately sculpt organs and tissues is a major challenge not only in basic developmental biology but also in tissue engineering and regenerative medicine. Here we use live imaging to show that the basal surfaces of Drosophila follicle cells undergo a series of directional, oscillating contractions driven by periodic myosin accumulation on a polarized actin network. Inhibition of the actomyosin contractions or their coupling to extracellular matrix (ECM) blocked elongation of the whole tissue, whereas enhancement of the contractions exaggerated it. Myosin accumulated in a periodic manner before each contraction and was regulated by the small GTPase Rho, its downstream kinase, ROCK, and cytosolic calcium. Disrupting the link between the actin cytoskeleton and the ECM decreased the amplitude and period of the contractions, whereas enhancing cell–ECM adhesion increased them. In contrast, disrupting cell–cell adhesions resulted in loss of the actin network. Our findings reveal a mechanism controlling organ shape and an experimental model for the study of the effects of oscillatory actomyosin activity within a coherent cell sheet.

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Figure 1: Stage-9 follicle cells undergo rapid periodic contractions and myosin accumulation.
Figure 2: Quantification of basal periodic contraction and comparison with apical activity.
Figure 3: Accumulation of basal myosin on stable actin filaments precedes the basal membrane contraction.
Figure 4: Global change in basal myosin during egg chamber development.
Figure 5: Basal actomyosin contractions control tissue shape.
Figure 6: Rho, ROCK and cell adhesion regulate basal myosin accumulation and organ shape.
Figure 7: Cell autonomy of myosin oscillation and pathways affecting its magnitude and period.
Figure 8: Model of tissue elongation controlled by basal actomyosin contraction.

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Acknowledgements

We thank Doug Robinson for invaluable discussions, critical reading of the manuscript and help with writing the discussion of the myosin oscillation mechanism. Nick Brown and Eric Wieschaus generously donated reagents. This work was supported by grants to D.J.M. from the National Institute of General Medical Sciences including R01 GM46425, GM73164 and the Cell Migration Consortium. Bloomington Drosophila Stock Center and Vienna Drosophila RNAi Center resources contributed to this work. FlyBase provided important information used in this work. Clones provided by the Berkeley Drosophila Genome Project and distributed by Drosophila Genetic Resource Center were used.

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  1. Li He and Xiaobo Wang: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Chemistry, Center for Cell Dynamics, Johns Hopkins School of Medicine, 855 North Wolfe Street, Baltimore, 21205, Maryland, USA

    Li He, Xiaobo Wang, Ho Lam Tang & Denise J. Montell

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  1. Li He
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Contributions

L.H. and X.W. performed the image acquisition and mutant analysis. L.H. processed and analysed images. H.L.T. conducted inhibitor treatments and calcium-related experiments. D.J.M. prepared the manuscript. All authors participated in the interpretation of the data and the production of the final manuscript.

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Correspondence to Denise J. Montell.

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The authors declare no competing financial interests.

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He, L., Wang, X., Tang, H. et al. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat Cell Biol 12, 1133–1142 (2010). https://doi.org/10.1038/ncb2124

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