Microtubules provide directional information for core PCP function.

Maja Matis,Claire J Tomlin,Jeffrey D Axelrod,David A Russler-Germain,Qie Hu

doi:10.7554/elife.02893

Maja Matis, Claire J Tomlin + Show 3 more

Open Access

https://doi.org/10.7554/elife.02893

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Journal: eLife	Publication Date: Aug 14, 2014
Citations: 133	License type: CC BY 4.0

Affiliation: Stanford University, University of California, Berkeley

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.

Highlights

In Drosophila and in vertebrates, six proteins constituting a ‘core’ Planar cell polarity (PCP) module acquire asymmetric distributions to polarize epithelial cells along a planar axis (Goodrich and Strutt, 2011)
It is proposed that the Ft/Ds/Fj system, comprising the atypical cadherins Ft (Yang et al, 2002), Ds (Adler et al, 1998) and the Golgi-resident protein Fj (Zeidler et al, 1999), acts as a ‘global’ PCP module, transducing tissue level directional cues encoded by opposing Ds and Fj expression gradients, to orient the core PCP module (Yang et al, 2002; Ma et al, 2003)
Our findings support the hypothesis that a polarized MT cytoskeleton orients PCP throughout wing development by directing the trafficking of Dsh containing vesicles. They confirm that the Ft/Ds/Fj PCP module directs orientation of this apical MT cytoskeleton, at least in the proximal central portion of the wing

Summary

Introduction

In Drosophila and in vertebrates, six proteins constituting a ‘core’ PCP module acquire asymmetric distributions to polarize epithelial cells along a planar axis (Goodrich and Strutt, 2011). Preferential interactions between Fmi/Fz and Fmi/Vang complexes across cell boundaries (Lawrence et al, 2004; Chen et al, 2008; Strutt and Strutt, 2008) and intercellular feedback loops (Tree et al, 2002; Amonlirdviman et al, 2005) can account for intracellular segregation of these complexes and coordinated alignment among neighboring cells. It remains unclear how this local polarity is globally oriented with respect to the tissue axes. Though a mechanism that might transmit a directional signal from the Ft/Ds/Fj module to the core module is suggested by existing observations, important additional data are needed to support the model

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