Transient junction anisotropies orient annular cell polarization in the Drosophila airway tubes

Nat Cell Biol. 2015 Dec;17(12):1569-76. doi: 10.1038/ncb3267. Epub 2015 Nov 9.

Abstract

In contrast to planes, three-dimensional (3D) structures such as tubes are physically anisotropic. Tubular organs exhibit a striking orientation of landmarks according to the physical anisotropy of the 3D shape, in addition to planar cell polarization. However, the influence of 3D tissue topography on the constituting cells remains underexplored. Here, we identify a regulatory network polarizing cellular biochemistry according to the physical anisotropy of the 3D tube geometry (tube cell polarization) by a genome-wide, tissue-specific RNAi screen. During Drosophila airway remodelling, each apical cellular junction is equipotent to establish perpendicular actomyosin cables, irrespective of the longitudinal or transverse tube axis. A dynamic transverse enrichment of atypical protein kinase C (aPKC) shifts the balance and transiently targets activated small GTPase RhoA, myosin phosphorylation and Rab11 vesicle trafficking to longitudinal junctions. We propose that the PAR complex translates tube physical anisotropy into longitudinal junctional anisotropy, where cell-cell communication aligns the contractile cytoskeleton of neighbouring cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Airway Remodeling
  • Animals
  • Animals, Genetically Modified
  • Anisotropy
  • Cell Communication
  • Cell Polarity*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / embryology
  • Embryo, Nonmammalian / metabolism
  • Female
  • Gene Regulatory Networks
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Intercellular Junctions / metabolism*
  • Larva / cytology
  • Larva / metabolism
  • Male
  • Microscopy, Confocal
  • Myosins / genetics
  • Myosins / metabolism
  • Phosphorylation
  • Protein Kinase C / genetics
  • Protein Kinase C / metabolism
  • RNA Interference
  • Respiratory System / cytology*
  • Respiratory System / embryology
  • Respiratory System / metabolism
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / metabolism
  • rhoA GTP-Binding Protein / genetics
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Actins
  • Drosophila Proteins
  • Green Fluorescent Proteins
  • PKC-3 protein
  • Protein Kinase C
  • Rab11 protein, Drosophila
  • Myosins
  • rab GTP-Binding Proteins
  • rhoA GTP-Binding Protein