Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases

J Biol Chem. 2005 Jun 10;280(23):22115-23. doi: 10.1074/jbc.M414027200. Epub 2005 Apr 6.

Abstract

Smad4 mediates signaling by the transforming growth factor-beta (TGF-beta) superfamily of cytokines. Smad signaling is negatively regulated by inhibitory (I) Smads and ubiquitin-mediated processes. Known mechanisms of proteasomal degradation of Smads depend on the direct interaction of specific E3 ligases with Smads. Alternatively, I-Smads elicit degradation of the TGF-beta receptor by recruiting the WW and HECT domain E3 ligases, Smurfs, WWP1, or NEDD4-2. We describe an equivalent mechanism of degradation of Smad4 by the above E3 ligases, via formation of ternary complexes between Smad4 and Smurfs, mediated by R-Smads (Smad2) or I-Smads (Smad6/7), acting as adaptors. Smurfs, which otherwise cannot directly bind to Smad4, mediated poly-ubiquitination of Smad4 in the presence of Smad6 or Smad7. Smad4 co-localized with Smad7 and Smurf1 primarily in the cytoplasm and in peripheral cell protrusions. Smad2 or Smad7 mutants defective in Smad4 interaction failed to induce Smurf1-mediated down-regulation of Smad4. A Smad4 mutant defective in Smad2 or Smad7 interaction could not be effectively down-regulated by Smurf1. We propose that Smad4 is targeted for degradation by multiple ubiquitin ligases that can simultaneously act on R-Smads and signaling receptors. Such mechanisms of down-regulation of TGF-beta signaling may be critical for proper physiological response to this pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / metabolism
  • Cell Line
  • Cytoplasm / metabolism
  • DNA-Binding Proteins / chemistry*
  • DNA-Binding Proteins / metabolism
  • Down-Regulation
  • Endosomal Sorting Complexes Required for Transport
  • Genetic Vectors
  • Glutathione Transferase / metabolism
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Microscopy, Fluorescence
  • Mutation
  • Nedd4 Ubiquitin Protein Ligases
  • Plasmids / metabolism
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction*
  • Smad2 Protein
  • Smad4 Protein
  • Smad7 Protein
  • Trans-Activators / chemistry*
  • Trans-Activators / metabolism
  • Transfection
  • Transforming Growth Factor beta / metabolism
  • Ubiquitin / chemistry
  • Ubiquitin / metabolism
  • Ubiquitin-Protein Ligases / chemistry*
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • DNA-Binding Proteins
  • Endosomal Sorting Complexes Required for Transport
  • Receptors, Transforming Growth Factor beta
  • SMAD2 protein, human
  • SMAD4 protein, human
  • SMAD7 protein, human
  • Smad2 Protein
  • Smad4 Protein
  • Smad7 Protein
  • Trans-Activators
  • Transforming Growth Factor beta
  • Ubiquitin
  • Green Fluorescent Proteins
  • Nedd4 Ubiquitin Protein Ligases
  • Nedd4 protein, human
  • Nedd4L protein, human
  • SMURF1 protein, human
  • SMURF2 protein, human
  • WWP1 protein, human
  • Ubiquitin-Protein Ligases
  • Glutathione Transferase
  • Proteasome Endopeptidase Complex