Microtubules provide directional information for core PCP function

Elife. 2014 Aug 14:3:e02893. doi: 10.7554/eLife.02893.

Abstract

Planar cell polarity (PCP) signaling controls the polarization of cells within the plane of an epithelium. Two molecular modules composed of Fat(Ft)/Dachsous(Ds)/Four-jointed(Fj) and a 'PCP-core' including Frizzled(Fz) and Dishevelled(Dsh) contribute to polarization of individual cells. How polarity is globally coordinated with tissue axes is unresolved. Consistent with previous results, we find that the Ft/Ds/Fj-module has an effect on a MT-cytoskeleton. Here, we provide evidence for the model that the Ft/Ds/Fj-module provides directional information to the core-module through this MT organizing function. We show Ft/Ds/Fj-dependent initial polarization of the apical MT-cytoskeleton prior to global alignment of the core-module, reveal that the anchoring of apical non-centrosomal MTs at apical junctions is polarized, observe that directional trafficking of vesicles containing Dsh depends on Ft, and demonstrate the feasibility of this model by mathematical simulation. Together, these results support the hypothesis that Ft/Ds/Fj provides a signal to orient core PCP function via MT polarization.

Keywords: fat cadherin; microtubules; planar cell polarity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Algorithms*
  • Animals
  • Animals, Genetically Modified
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism
  • Cell Polarity / genetics
  • Cell Polarity / physiology*
  • Cytoskeleton / metabolism
  • Cytoskeleton / ultrastructure
  • Dishevelled Proteins
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Frizzled Receptors / genetics
  • Frizzled Receptors / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Microscopy, Confocal
  • Microscopy, Electron, Transmission
  • Microtubules / metabolism*
  • Microtubules / ultrastructure
  • Models, Biological*
  • Mutation
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Pupa / cytology
  • Pupa / genetics
  • Pupa / metabolism
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Time-Lapse Imaging
  • Wings, Animal / cytology
  • Wings, Animal / metabolism
  • Wings, Animal / ultrastructure

Substances

  • Adaptor Proteins, Signal Transducing
  • Cadherins
  • Cell Adhesion Molecules
  • Dishevelled Proteins
  • Drosophila Proteins
  • Frizzled Receptors
  • Membrane Glycoproteins
  • Phosphoproteins
  • ds protein, Drosophila
  • dsh protein, Drosophila
  • fj protein, Drosophila
  • ft protein, Drosophila
  • fz protein, Drosophila