Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan

Dev Cell. 2011 Aug 16;21(2):245-56. doi: 10.1016/j.devcel.2011.06.026.

Abstract

Basement membranes (BMs) are resilient polymer structures that surround organs in all animals. Tissues, however, undergo extensive morphological changes during development. It is not known whether the assembly of BM components plays an active morphogenetic role. To study in vivo the biogenesis and assembly of Collagen IV, the main constituent of BMs, we used a GFP-based RNAi method (iGFPi) designed to knock down any GFP-trapped protein in Drosophila. We found with this method that Collagen IV is synthesized by the fat body, secreted to the hemolymph (insect blood), and continuously incorporated into the BMs of the larva. We also show that incorporation of Collagen IV determines organ shape, first by mechanically constricting cells and second through recruitment of Perlecan, which counters constriction by Collagen IV. Our results uncover incorporation of Collagen IV and Perlecan into BMs as a major determinant of organ shape and animal form.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Basement Membrane / metabolism
  • Cell Shape / physiology*
  • Collagen Type IV / genetics
  • Collagen Type IV / metabolism*
  • Drosophila
  • Drosophila Proteins / genetics
  • Fat Body / cytology*
  • Fat Body / metabolism*
  • Fat Body / ultrastructure
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology
  • Green Fluorescent Proteins / genetics
  • Heparan Sulfate Proteoglycans / metabolism*
  • Larva
  • Microscopy, Confocal
  • Microscopy, Electron, Transmission
  • Models, Biological
  • RNA Interference / physiology
  • Wings, Animal / growth & development*
  • Wings, Animal / ultrastructure

Substances

  • Collagen Type IV
  • Drosophila Proteins
  • Heparan Sulfate Proteoglycans
  • perlecan
  • Green Fluorescent Proteins