Echinoid regulates Flamingo endocytosis to control ommatidial rotation in the Drosophila eye

Development. 2010 Mar;137(5):745-54. doi: 10.1242/dev.040238. Epub 2010 Jan 28.

Abstract

Planar cell polarity (PCP) refers to a second polarity axis orthogonal to the apicobasal axis in the plane of the epithelium. The molecular link between apicobasal polarity and PCP is largely unknown. During Drosophila eye development, differentiated photoreceptors form clusters that rotate independently of the surrounding interommatidial cells (ICs). Here, we demonstrate that both Echinoid (Ed), an adherens junction-associated cell adhesion molecule, and Flamingo (Fmi), a PCP determinant, are endocytosed via a clathrin-mediated pathway in ICs. Interestingly, we found that Ed binds the AP-2 adaptor and is required for the internalization of Fmi into ICs. Loss of ed led to increased amounts of Fmi on the cell membrane of non-rotating ICs and also to the misrotation of photoreceptor clusters. Importantly, overexpression of fmi in ICs alone was sufficient to cause misrotation of the adjacent photoreceptor clusters. Together, we propose that Ed, when internalized by AP-2, undergoes co-endocytosis with, and thereby decreases, Fmi levels on non-rotating ICs to permit correct rotation of ommatidial clusters. Thus, co-endocytosis of Ed and Fmi provides a link between apicobasal polarity and PCP.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Body Patterning* / genetics
  • Cadherins / metabolism*
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism
  • Cell Adhesion Molecules / physiology*
  • Cell Polarity / genetics
  • Cell Polarity / physiology
  • Drosophila / genetics
  • Drosophila / growth & development*
  • Drosophila / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila Proteins / physiology*
  • Endocytosis / genetics
  • ErbB Receptors / metabolism
  • Eye / growth & development*
  • Eye / metabolism
  • Receptors, Invertebrate Peptide / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Repressor Proteins / physiology*

Substances

  • Cadherins
  • Cell Adhesion Molecules
  • Drosophila Proteins
  • ED protein, Drosophila
  • Receptors, Invertebrate Peptide
  • Repressor Proteins
  • stan protein, Drosophila
  • Egfr protein, Drosophila
  • ErbB Receptors