The polarity protein VANG-1 antagonizes Wnt signaling by facilitating Frizzled endocytosis

Development. 2018 Dec 17;145(24):dev168666. doi: 10.1242/dev.168666.

Abstract

Signaling that instructs the migration of neurons needs to be tightly regulated to ensure precise positioning of neurons and subsequent wiring of the neuronal circuits. Wnt-Frizzled signaling controls neuronal migration in metazoans, in addition to many other aspects of neural development. We show that Caenorhabditis elegans VANG-1, a membrane protein that acts in the planar cell polarity (PCP) pathway, antagonizes Wnt signaling by facilitating endocytosis of the Frizzled receptors. Mutations of vang-1 suppress migration defects of multiple classes of neurons in the Frizzled mutants, and overexpression of vang-1 causes neuronal migration defects similar to those of the Frizzled mutants. Our genetic experiments suggest that VANG-1 facilitates Frizzled endocytosis through β-arrestin2. Co-immunoprecipitation experiments indicate that Frizzled proteins and VANG-1 form a complex, and this physical interaction requires the Frizzled cysteine-rich domain. Our work reveals a novel mechanism mediated by the PCP protein VANG-1 that downregulates Wnt signaling through Frizzled endocytosis.

Keywords: C. elegans; Endocytosis; Frizzled; Neuronal migration; Planar polarity; Wnt signaling.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Caenorhabditis elegans / cytology*
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Movement
  • Cell Polarity*
  • Endocytosis*
  • Frizzled Receptors / metabolism*
  • Larva / cytology
  • Multiprotein Complexes / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Phosphoproteins / chemistry
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Wnt Signaling Pathway*

Substances

  • Caenorhabditis elegans Proteins
  • Frizzled Receptors
  • Multiprotein Complexes
  • Phosphoproteins
  • Vang-1 protein, C elegans