A Daple-Akt feed-forward loop enhances noncanonical Wnt signals by compartmentalizing β-catenin

Mol Biol Cell. 2017 Dec 1;28(25):3709-3723. doi: 10.1091/mbc.E17-06-0405. Epub 2017 Oct 11.

Abstract

Cellular proliferation is antagonistically regulated by canonical and noncanonical Wnt signals; their dysbalance triggers cancers. We previously showed that a multimodular signal transducer, Daple, enhances PI3-K→Akt signals within the noncanonical Wnt signaling pathway and antagonistically inhibits canonical Wnt responses. Here we demonstrate that the PI3-K→Akt pathway serves as a positive feedback loop that further enhances noncanonical Wnt signals by compartmentalizing β-catenin. By phosphorylating the phosphoinositide- (PI) binding domain of Daple, Akt abolishes Daple's ability to bind PI3-P-enriched endosomes that engage dynein motor complex for long-distance trafficking of β-catenin/E-cadherin complexes to pericentriolar recycling endosomes (PCREs). Phosphorylation compartmentalizes Daple/β-catenin/E-cadherin complexes to cell-cell contact sites, enhances noncanonical Wnt signals, and thereby suppresses colony growth. Dephosphorylation compartmentalizes β-catenin on PCREs, a specialized compartment for prolonged unopposed canonical Wnt signaling, and enhances colony growth. Cancer-associated Daple mutants that are insensitive to Akt mimic a constitutively dephosphorylated state. This work not only identifies Daple as a platform for cross-talk between Akt and the noncanonical Wnt pathway but also reveals the impact of such cross-talk on tumor cell phenotypes that are critical for cancer initiation and progression.

MeSH terms

  • Cadherins / metabolism
  • Cell Proliferation / physiology
  • Centrosome
  • Feedback, Physiological
  • Frizzled Receptors / metabolism
  • HeLa Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Microfilament Proteins / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Signal Transduction
  • Trans-Activators / metabolism
  • Wnt Proteins / metabolism
  • Wnt Signaling Pathway / physiology*
  • beta Catenin / metabolism

Substances

  • CCDC88C protein, human
  • Cadherins
  • Frizzled Receptors
  • Intracellular Signaling Peptides and Proteins
  • Microfilament Proteins
  • Trans-Activators
  • Wnt Proteins
  • beta Catenin
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt