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Planar Polarity Specification through Asymmetric Subcellular Localization of Fat and Dachsous

1 , 2 , 1 , 2 , 1 , 2 ,

Current Biology

Cell Press

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      Summary

      Two pathways regulate planar polarity: the core proteins and the Fat-Dachsous-Four-jointed (Ft-Ds-Fj) system. Morphogens specify complementary expression patterns of Ds and Fj that potentially act as polarizing cues. It has been suggested that Ft-Ds-Fj-mediated cues are weak and that the core proteins amplify them [ 1, 2]. Another view is that the two pathways act independently to generate and propagate polarity [ 3, 4]: if correct, this raises the question of how gradients of Ft and Ds expression or activity might be interpreted to provide strong cellular polarizing cues and how such cues are propagated from cell to cell. Here, we demonstrate that the complementary expression of Ds and Fj results in biased Ft and Ds protein distribution across cells, with Ft and Ds accumulating on opposite edges. Furthermore, boundaries of Ft and Ds expression result in subcellular asymmetries in protein distribution that are transmitted to neighboring cells, and asymmetric Ds localization results in a corresponding asymmetric distribution of the myosin Dachs. We show that the generation of subcellular asymmetries of Ft and Ds and the core proteins is largely independent in the wing disc and additionally that ommatidial polarity in the eye can be determined without input from the Ft-Ds-Fj system, consistent with the two pathways acting in parallel.

      Highlights

      ► Ft and Ds become asymmetrically localized during planar polarity specification ► Ft and Ds asymmetry can be propagated from cell to cell ► Ft and Ds asymmetry promotes Dachs asymmetry and regulates polarity in the proximal wing ► Ft and Ds provide a partial polarity cue in the eye where they can act without Dachs

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      Most cited references 29

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      Hippo signaling: growth control and beyond.

      The Hippo pathway has emerged as a conserved signaling pathway that is essential for the proper regulation of organ growth in Drosophila and vertebrates. Although the mechanisms of signal transduction of the core kinases Hippo/Mst and Warts/Lats are relatively well understood, less is known about the upstream inputs of the pathway and about the downstream cellular and developmental outputs. Here, we review recently discovered mechanisms that contribute to the dynamic regulation of Hippo signaling during Drosophila and vertebrate development. We also discuss the expanding diversity of Hippo signaling functions during development, discoveries that shed light on a complex regulatory system and provide exciting new insights into the elusive mechanisms that regulate organ growth and regeneration.
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        Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila.

        Planar cell polarity (PCP) proteins form polarized cortical domains that govern polarity of external structures such as hairs and cilia in both vertebrate and invertebrate epithelia. The mechanisms that globally orient planar polarity are not understood, and are investigated here in the Drosophila wing using a combination of experiment and theory. Planar polarity arises during growth and PCP domains are initially oriented toward the well-characterized organizer regions that control growth and patterning. At pupal stages, the wing hinge contracts, subjecting wing-blade epithelial cells to anisotropic tension in the proximal-distal axis. This results in precise patterns of oriented cell elongation, cell rearrangement and cell division that elongate the blade proximo-distally and realign planar polarity with the proximal-distal axis. Mutation of the atypical Cadherin Dachsous perturbs the global polarity pattern by altering epithelial dynamics. This mechanism utilizes the cellular movements that sculpt tissues to align planar polarity with tissue shape. Copyright 2010 Elsevier Inc. All rights reserved.
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          Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway.

          The mechanisms that order cellular packing geometry are critical for the functioning of many tissues, but they are poorly understood. Here, we investigate this problem in the developing wing of Drosophila. The surface of the wing is decorated by hexagonally packed hairs that are uniformly oriented by the planar cell polarity pathway. They are constructed by a hexagonal array of wing epithelial cells. Wing epithelial cells are irregularly arranged throughout most of development, but they become hexagonally packed shortly before hair formation. During the process, individual cell boundaries grow and shrink, resulting in local neighbor exchanges, and Cadherin is actively endocytosed and recycled through Rab11 endosomes. Hexagonal packing depends on the activity of the planar cell polarity proteins. We propose that these proteins polarize trafficking of Cadherin-containing exocyst vesicles during junction remodeling. This may be a common mechanism for the action of planar cell polarity proteins in diverse systems.
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            Author and article information

            Affiliations
            [1 ]MRC Centre for Developmental and Biomedical Genetics, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
            [2 ]Department of Biomedical Science, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
            Author notes
            []Corresponding author d.strutt@ 123456sheffield.ac.uk
            Contributors
            Journal
            Curr Biol
            Curr. Biol
            Current Biology
            Cell Press
            0960-9822
            1879-0445
            22 May 2012
            22 May 2012
            : 22
            : 10
            : 907-914
            22503504
            3362735
            CURBIO9504
            10.1016/j.cub.2012.03.053
            © 2012 ELL & Excerpta Medica.

            This document may be redistributed and reused, subject to certain conditions.

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