Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition

Nat Cell Biol. 2004 Oct;6(10):931-40. doi: 10.1038/ncb1173. Epub 2004 Sep 26.

Abstract

The phenotypic changes of increased motility and invasiveness of cancer cells are reminiscent of the epithelial-mesenchymal transition (EMT) that occurs during embryonic development. Snail, a zinc-finger transcription factor, triggers this process by repressing E-cadherin expression; however, the mechanisms that regulate Snail remain elusive. Here we find that Snail is highly unstable, with a short half-life about 25 min. We show that GSK-3beta binds to and phosphorylates Snail at two consensus motifs to dually regulate the function of this protein. Phosphorylation of the first motif regulates its beta-Trcp-mediated ubiquitination, whereas phosphorylation of the second motif controls its subcellular localization. A variant of Snail (Snail-6SA), which abolishes these phosphorylations, is much more stable and resides exclusively in the nucleus to induce EMT. Furthermore, inhibition of GSK-3beta results in the upregulation of Snail and downregulation of E-cadherin in vivo. Thus, Snail and GSK-3beta together function as a molecular switch for many signalling pathways that lead to EMT.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Motifs
  • Binding Sites
  • Breast Neoplasms / pathology
  • Cadherins / metabolism
  • Cell Line, Tumor
  • Cell Nucleus / chemistry
  • Consensus Sequence
  • Cysteine Endopeptidases / metabolism
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / drug effects
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism*
  • Gene Expression Regulation, Neoplastic*
  • Glycogen Synthase Kinase 3 / metabolism*
  • Glycogen Synthase Kinase 3 beta
  • Humans
  • Leupeptins / pharmacology
  • Lithium / pharmacology
  • Mesoderm / cytology
  • Mesoderm / metabolism*
  • Multienzyme Complexes / metabolism
  • Mutation
  • Phosphorylation
  • Proteasome Endopeptidase Complex
  • Protein Binding
  • Snail Family Transcription Factors
  • Substrate Specificity
  • Transcription Factors / chemistry
  • Transcription Factors / drug effects
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Zinc Fingers

Substances

  • Cadherins
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • Leupeptins
  • Multienzyme Complexes
  • Snail Family Transcription Factors
  • Transcription Factors
  • Lithium
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Glycogen Synthase Kinase 3
  • Cysteine Endopeptidases
  • Proteasome Endopeptidase Complex
  • benzyloxycarbonylleucyl-leucyl-leucine aldehyde