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.

[1]  J. Shih,et al.  The cellular basis of the convergence and extension of the Xenopus neural plate , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[2]  M. Mlodzik,et al.  The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. , 2008, Developmental cell.

[3]  D. Grifoni,et al.  The tumor suppressor gene fat modulates the EGFR-mediated proliferation control in the imaginal tissues of Drosophila melanogaster , 2005, Mechanisms of Development.

[4]  A. Hudspeth,et al.  Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish. , 2004, Developmental cell.

[5]  Matias Simons,et al.  Planar cell polarity signaling: from fly development to human disease. , 2008, Annual review of genetics.

[6]  A. Garcı́a-Bellido,et al.  Cell behaviour of Drosophila fat cadherin mutations in wing development , 2000, Mechanisms of Development.

[7]  R. Maeda,et al.  An optimized transgenesis system for Drosophila using germ-line-specific φC31 integrases , 2007, Proceedings of the National Academy of Sciences.

[8]  A. Giangrande,et al.  Imaging Drosophila pupal wing morphogenesis. , 2008, Methods in molecular biology.

[9]  Frank Jülicher,et al.  The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing , 2007, Current Biology.

[10]  S. Tsukita,et al.  Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dα-catenin-GFP fusion protein , 1999, Development Genes and Evolution.

[11]  L. Mahadevan,et al.  Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension , 2009, Nature Cell Biology.

[12]  Alessandro Abate,et al.  Cell packing influences planar cell polarity signaling , 2008, Proceedings of the National Academy of Sciences.

[13]  Peter A Lawrence,et al.  Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity , 2006, Development.

[14]  S. Haase,et al.  Microtubule Organization: Cell Shape Is Destiny , 2007, Current Biology.

[15]  C. Tomlin,et al.  Mathematical Modeling of Planar Cell Polarity to Understand Domineering Nonautonomy , 2005, Science.

[16]  P. Lawrence,et al.  Planar cell polarity: one or two pathways? , 2007, Nature Reviews Genetics.

[17]  J. Lis,et al.  Structure and expression of ubiquitin genes of Drosophila melanogaster , 1988, Molecular and cellular biology.

[18]  David Strutt,et al.  Nonautonomous planar polarity patterning in Drosophila: dishevelled-independent functions of frizzled. , 2002, Developmental cell.

[19]  D. Tree,et al.  A three-tiered mechanism for regulation of planar cell polarity. , 2002, Seminars in cell & developmental biology.

[20]  Pierre-François Lenne,et al.  Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis , 2008, Nature Cell Biology.

[21]  Jennifer A Zallen,et al.  Planar Polarity and Tissue Morphogenesis , 2007, Cell.

[22]  Jeffrey D. Axelrod,et al.  Fidelity in planar cell polarity signalling , 2003, Nature.

[23]  Jennifer A Zallen,et al.  Multicellular rosette formation links planar cell polarity to tissue morphogenesis. , 2006, Developmental cell.

[24]  S. Eaton,et al.  Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. , 2005, Developmental cell.

[25]  Luc Vincent,et al.  Watersheds in Digital Spaces: An Efficient Algorithm Based on Immersion Simulations , 1991, IEEE Trans. Pattern Anal. Mach. Intell..

[26]  Paul Skoglund,et al.  The forces that shape embryos: physical aspects of convergent extension by cell intercalation , 2008, Physical biology.

[27]  K. Irvine,et al.  Action of fat, four-jointed, dachsous and dachs in distal-to-proximal wing signaling , 2004, Development.

[28]  M. Scott,et al.  Prickle Mediates Feedback Amplification to Generate Asymmetric Planar Cell Polarity Signaling , 2002, Cell.

[29]  J. Axelrod,et al.  Progress and challenges in understanding planar cell polarity signaling. , 2009, Seminars in cell & developmental biology.

[30]  S. Akira,et al.  Mathematical Modeling of Planar Cell Polarity to Understand Domineering Nonautonomy , 2005 .

[31]  Yoram Burak,et al.  Order and Stochastic Dynamics in Drosophila Planar Cell Polarity , 2009, PLoS Comput. Biol..

[32]  K. Irvine,et al.  Four-jointed Is a Golgi Kinase That Phosphorylates a Subset of Cadherin Domains , 2008, Science.

[33]  H. Strutt,et al.  Differential Stability of Flamingo Protein Complexes Underlies the Establishment of Planar Polarity , 2008, Current Biology.

[34]  N. Perrimon,et al.  Multiple roles for four-jointed in planar polarity and limb patterning. , 2000, Developmental biology.

[35]  R. Nusse,et al.  Asymmetric Homotypic Interactions of the Atypical Cadherin Flamingo Mediate Intercellular Polarity Signaling , 2008, Cell.

[36]  M. Mlodzik,et al.  A Quest for the Mechanism Regulating Global Planar Cell Polarity of Tissues , 2022 .

[37]  P J Bryant,et al.  Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. , 1988, Developmental biology.

[38]  Jennifer A Zallen,et al.  Patterned gene expression directs bipolar planar polarity in Drosophila. , 2004, Developmental cell.

[39]  L. Sulak,et al.  Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation , 2004, Nature.

[40]  Frank Jülicher,et al.  Hydrodynamic theory for multi-component active polar gels , 2007 .

[41]  J. Axelrod,et al.  Planar cell polarity signaling: the developing cell's compass. , 2009, Cold Spring Harbor perspectives in biology.

[42]  T. Uemura,et al.  Breaking cellular symmetry along planar axes in Drosophila and vertebrates. , 2003, Journal of biochemistry.

[43]  Antonio Baonza,et al.  The Orientation of Cell Divisions Determines the Shape of Drosophila Organs , 2005, Current Biology.

[44]  R. Daga,et al.  Interphase microtubule bundles use global cell shape to guide spindle alignment in fission yeast , 2008, Journal of Cell Science.

[45]  J. Villano,et al.  four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. , 1995, Development.

[46]  J. Charlton,et al.  Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. , 1998, Development.

[47]  H. Strutt,et al.  Long‐range coordination of planar polarity in Drosophila , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  Hugo J. Bellen,et al.  P[acman]: A BAC Transgenic Platform for Targeted Insertion of Large DNA Fragments in D. melanogaster , 2006, Science.

[49]  M. Mlodzik,et al.  Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility , 2007, Nature Reviews Genetics.

[50]  Microtubule self-organisation by reaction-diffusion processes in miniature cell-sized containers and phospholipid vesicles. , 2006, Biophysical chemistry.

[51]  P. Adler,et al.  Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila , 1987, Nature.

[52]  Michel Kerszberg,et al.  Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: A computer model , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[53]  C. Goodman,et al.  Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. , 1995, Genes & development.

[54]  S. Blair,et al.  Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing , 2004, Development.

[55]  David Strutt,et al.  Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. , 2006, Developmental cell.

[56]  N. Papalopulu,et al.  A default mechanism of spindle orientation based on cell shape is sufficient to generate cell fate diversity in polarised Xenopus blastomeres , 2006, Development.

[57]  D. Strutt.  Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. , 2001, Molecular cell.

[58]  Xi Lin,et al.  Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway , 2005, Nature Genetics.