Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells

Curr Biol. 2006 Jan 24;16(2):140-9. doi: 10.1016/j.cub.2005.11.068.

Abstract

Background: In a specialized epithelial cell such as the Drosophila photoreceptor, a conserved set of proteins is essential for the establishment of polarity, its maintenance, or both--in Drosophila, these proteins include the apical factors Bazooka, D-atypical protein kinase C, and D-Par6 together with D-Ecadherin. However, little is known about the mechanisms by which such apical factors might regulate the differentiation of the apical membrane into functional domains such as an apical-most stack of microvilli or more lateral sub-apical membrane.

Results: We show that in photoreceptors Bazooka (D-Par3) recruits the tumor suppressor lipid phosphatase PTEN to developing cell-cell junctions (Zonula Adherens, za). za-localized PTEN controls the spatially restricted accumulation of optimum levels of the lipid PtdIns(3,4,5)P3 within the apical membrane domain. This in turn finely tunes activation of Akt1, a process essential for proper morphogenesis of the light-gathering organelle, consisting of a stack of F-actin rich microvilli within the apical membrane.

Conclusions: Spatially localized PtdIns(3,4,5)P3 mediates directional sensing during neutrophil and Dictyostelium chemotaxis. We conclude that a conserved mechanism also operates during photoreceptor epithelial cell morphogenesis in order to achieve normal differentiation of the apical membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adherens Junctions / metabolism
  • Animals
  • Cell Membrane / ultrastructure*
  • Cell Polarity*
  • Drosophila / cytology
  • Drosophila / growth & development*
  • Drosophila / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / physiology*
  • Epithelial Cells / cytology
  • Gene Expression Regulation, Developmental
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Intracellular Signaling Peptides and Proteins / physiology
  • Microvilli / metabolism
  • Models, Biological
  • Morphogenesis
  • PTEN Phosphohydrolase / metabolism
  • PTEN Phosphohydrolase / physiology
  • Phosphatidylinositol Phosphates / analysis
  • Phosphatidylinositol Phosphates / metabolism
  • Phosphatidylinositol Phosphates / physiology*
  • Photoreceptor Cells, Invertebrate / cytology*
  • Photoreceptor Cells, Invertebrate / growth & development
  • Protein-Serine-Threonine Kinases / metabolism

Substances

  • Drosophila Proteins
  • Intracellular Signaling Peptides and Proteins
  • Phosphatidylinositol Phosphates
  • baz protein, Drosophila
  • phosphatidylinositol 3,4,5-triphosphate
  • Protein-Serine-Threonine Kinases
  • PTEN Phosphohydrolase
  • PTEN protein, Drosophila