Asymmetric Localization of Frizzled and the Determination of Notch-Dependent Cell Fate in the Drosophila Eye

Curr Biol. 2002 May 14;12(10):813-24. doi: 10.1016/s0960-9822(02)00841-2.

Abstract

Background: During patterning of the Drosophila eye, a critical step is the Notch-mediated cell fate decision that determines the identities of the R3/R4 photoreceptor pair in each ommatidium. Depending on the decision taken, the ommatidium adopts either the dorsal or ventral chiral form. This decision is directed by the activity of the planar polarity genes, and, in particular, higher activity of the receptor Frizzled confers R3 fate.

Results: We present evidence that Frizzled does not modulate Notch activity via Rho GTPases and a JNK cascade as previously proposed. We find that the planar polarity proteins Frizzled, Dishevelled, Flamingo, and Strabismus adopt asymmetric protein localizations in the developing photoreceptors. These protein localizations correlate with the bias of Notch activity between R3/R4, suggesting that they are necessary to modulate Notch activity between these cells. Additional data support a mechanism for regulation of Notch activity that could involve direct interactions between Dishevelled and Notch at the cell cortex.

Conclusions: In the light of our findings, we conclude that Rho GTPases/JNK cascades are not major effectors of planar polarity in the Drosophila eye. We propose a new model for the control of R3/R4 photoreceptor fate by Frizzled, whereby asymmetric protein localization is likely to be a critical step in modulation of Notch activity. This modulation may occur via direct interactions between Notch and Dishevelled.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Body Patterning / genetics
  • Cell Differentiation*
  • Cell Lineage*
  • Dishevelled Proteins
  • Drosophila / cytology
  • Drosophila / embryology*
  • Drosophila / genetics
  • Drosophila / metabolism*
  • Drosophila Proteins / chemistry
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Eye / cytology*
  • Eye / embryology*
  • Eye / metabolism
  • Frizzled Receptors
  • Genes, Insect / genetics
  • JNK Mitogen-Activated Protein Kinases
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mitogen-Activated Protein Kinases / metabolism
  • Mosaicism / genetics
  • Mutation / genetics
  • Phenotype
  • Phosphoproteins / metabolism
  • Photoreceptor Cells, Invertebrate / cytology
  • Photoreceptor Cells, Invertebrate / embryology
  • Photoreceptor Cells, Invertebrate / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein Transport
  • Receptors, G-Protein-Coupled
  • Receptors, Notch
  • Signal Transduction
  • rho GTP-Binding Proteins / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Dishevelled Proteins
  • Drosophila Proteins
  • Frizzled Receptors
  • Membrane Proteins
  • N protein, Drosophila
  • Phosphoproteins
  • Receptors, G-Protein-Coupled
  • Receptors, Notch
  • Vang protein, Drosophila
  • dsh protein, Drosophila
  • fz protein, Drosophila
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases
  • rho GTP-Binding Proteins