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Fidelity in planar cell polarity signalling

Nature volume 421, pages 543–547 (2003)Cite this article

Abstract

The polarity of Drosophila wing hairs displays remarkable fidelity. Each of the approximately 30,000 wing epithelial cells constructs an actin-rich prehair that protrudes from its distal vertex and points distally. The distal location and orientation of the hairs is virtually error free, thus forming a nearly perfect parallel array. This process is controlled by the planar cell polarity signalling pathway1,2,3,4. Here we show that interaction between two tiers of the planar cell polarity signalling mechanism results in the observed high fidelity. The first tier, mediated by the cadherin Fat5, dictates global orientation by transducing a directional signal to individual cells. The second tier, orchestrated by the 7-pass transmembrane receptor Frizzled6,7, aligns each cell's polarity with that of its neighbours through the action of an intercellular feedback loop, enabling polarity to propagate from cell to cell8. We show that all cells need not respond correctly to the presumably subtle signal transmitted by Fat. Subsequent action of the Frizzled feedback loop is sufficient to align all the cells cooperatively. This economical system is therefore highly robust, and produces virtually error-free arrays.

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Figure 1: Four-jointed (Fj), Dachsous (Ds) and Fat (Ft) in the pupal wing.
Figure 2: Dachsous and Ft protein localization, and dependence on Fj.
Figure 3: Fat clonal phenotypes indicate that global signalling interacts with the local alignment mechanism to achieve high fidelity.
Figure 4: Loss of Ft in a large region enhances Fz domineering non-autonomy.

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Acknowledgements

We thank D. Bilder for advice, J. Duffy and the Bloomington stock center for fly strains, and members of the Axelrod laboratory for discussions of the work and comments on the manuscript. This work was supported by the NIH (J.D.A.).

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Authors and Affiliations

  1. Department of Pathology, Stanford University School of Medicine, Stanford, USA, California, 94305-5324

    Dali Ma & Jeffrey D. Axelrod

  2. Department of Biological Sciences, Stanford University, Stanford, California, 94305, USA

    Chung-hui Yang & Michael A. Simon

  3. Cancer Research UK, London Research Institute, London, 44 Lincoln's Inn Fields, WC2A 3PX, UK

    Helen McNeill

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Correspondence to Jeffrey D. Axelrod.

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Ma, D., Yang, Ch., McNeill, H. et al. Fidelity in planar cell polarity signalling. Nature 421, 543–547 (2003). https://doi.org/10.1038/nature01366

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