Murine Frizzled-1 behaves as an antagonist of the canonical Wnt/beta-catenin signaling

J Biol Chem. 2004 Feb 13;279(7):5725-33. doi: 10.1074/jbc.M309233200. Epub 2003 Nov 24.

Abstract

Activation of the Wnt signaling cascade provides key signals during development and in disease. Wnt signals are transduced by seven-transmembrane Frizzleds (Fzs) and the single transmembrane low density lipoprotein receptor-related proteins 5 or 6. In the course of the analysis of genes regulated by bone morphogenetic protein 2 in mesenchymal cells we found a significant induction of murine Frizzled-1 (mFz1) gene expression. Unexpectedly overexpression of mFz1 dramatically repressed the induction of alkaline phosphatase mediated by either bone morphogenetic protein 2 or Wnt3a in these cells. Moreover mFz1 overexpression significantly repressed both beta-catenin translocation into the nucleus and T cell factor signaling mediated by Wnt3a. Importantly microinjection of mFz1 transcript in Xenopus embryo inhibited the ability of Wnt1 to induce the expression of the Wnt/beta-catenin target gene Siamois in animal cap assay and secondary axis formation in whole embryo. By using chimeric constructs in which N- and C-terminal segments of mFz1 were replaced by the corresponding parts of Xfz3 we demonstrated that the antagonistic activity resides in the cysteine-rich domain of the N-terminal part. The antagonist activity of mFz1 could be prevented by overexpression of Galphaq-(305-359), which specifically uncouples Gq-coupled receptors, suggesting that Galphaq signaling contributes to the inhibition of Wnt/beta-catenin pathway by mFz1. This is the first time that a Frizzled receptor has been reported to antagonize Wnt/beta-catenin.

MeSH terms

  • Active Transport, Cell Nucleus
  • Alkaline Phosphatase / metabolism
  • Animals
  • Bone Morphogenetic Protein 2
  • Bone Morphogenetic Proteins / metabolism
  • COS Cells
  • Cell Line
  • Cell Nucleus / metabolism
  • Culture Media, Conditioned / pharmacology
  • Cystine / chemistry
  • Cytoskeletal Proteins / antagonists & inhibitors*
  • Enzyme Activation
  • Frizzled Receptors
  • GTP-Binding Protein alpha Subunits, Gq-G11 / metabolism
  • Genetic Vectors
  • Green Fluorescent Proteins
  • Immunoblotting
  • Luciferases / metabolism
  • Luminescent Proteins / metabolism
  • Mice
  • Microscopy, Confocal
  • Protein Structure, Tertiary
  • Proteins / metabolism
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Receptors, G-Protein-Coupled
  • Receptors, Neurotransmitter / metabolism
  • Receptors, Neurotransmitter / physiology*
  • Recombinant Fusion Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Time Factors
  • Trans-Activators / antagonists & inhibitors*
  • Transfection
  • Transforming Growth Factor beta*
  • Wnt Proteins
  • Wnt1 Protein
  • Wnt3 Protein
  • Wnt3A Protein
  • Xenopus
  • Xenopus Proteins*
  • Zebrafish Proteins*
  • beta Catenin

Substances

  • Bmp2 protein, mouse
  • Bone Morphogenetic Protein 2
  • Bone Morphogenetic Proteins
  • CTNNB1 protein, Xenopus
  • CTNNB1 protein, mouse
  • Culture Media, Conditioned
  • Cytoskeletal Proteins
  • FZD1 protein, Xenopus
  • Frizzled Receptors
  • Fzd1 protein, mouse
  • Luminescent Proteins
  • Proteins
  • Proto-Oncogene Proteins
  • Receptors, G-Protein-Coupled
  • Receptors, Neurotransmitter
  • Recombinant Fusion Proteins
  • Trans-Activators
  • Transforming Growth Factor beta
  • WNT1 protein, Xenopus
  • WNT3A protein, Xenopus
  • Wnt Proteins
  • Wnt1 Protein
  • Wnt1 protein, mouse
  • Wnt3 Protein
  • Wnt3A Protein
  • Wnt3a protein, mouse
  • Xenopus Proteins
  • Zebrafish Proteins
  • beta Catenin
  • Green Fluorescent Proteins
  • Cystine
  • Luciferases
  • Alkaline Phosphatase
  • GTP-Binding Protein alpha Subunits, Gq-G11