Smurf1 protein negatively regulates interferon-γ signaling through promoting STAT1 protein ubiquitination and degradation

J Biol Chem. 2012 May 18;287(21):17006-17015. doi: 10.1074/jbc.M112.341198. Epub 2012 Apr 2.

Abstract

Interferons are important cytokines that mediate antiviral, antiproliferative, antitumor, and immunoregulatory activities. However, uncontrolled IFN signaling may lead to autoimmune diseases. Here we identified Smurf1 as a negative regulator for IFN-γ signaling by targeting STAT1 for ubiquitination and proteasomal degradation. Smurf1 interacted with STAT1 through the WW domains of Smurf1 and the PY motif in STAT1 and catalyzed K48-linked polyubiquitination of STAT1. Interestingly, the Smurf1-mediated ubiquitination and degradation did not require STAT1 tyrosine and serine phosphorylation. Subsequently, overexpression of Smurf1 attenuated IFN-γ-mediated STAT1 activation and antiviral immune responses, whereas knockdown of Smurf1 enhanced IFN-γ-mediated STAT1 activation, expression of STAT1 target genes, and antiviral immune responses. Furthermore, IFN-γ stimulation led to enhanced expression of Smurf1. Therefore, our results demonstrate that Smurf1 is a negative feedback regulator for IFN-γ signaling by targeting STAT1 for ubiquitination and proteasomal degradation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Animals
  • HEK293 Cells
  • Humans
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism*
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism*
  • Mice
  • NIH 3T3 Cells
  • Proteasome Endopeptidase Complex / immunology
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Structure, Tertiary
  • Proteolysis*
  • STAT1 Transcription Factor / immunology
  • STAT1 Transcription Factor / metabolism*
  • Ubiquitin-Protein Ligases / immunology
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination / physiology*
  • Virus Diseases / immunology
  • Virus Diseases / metabolism

Substances

  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Stat1 protein, mouse
  • Interferon-gamma
  • SMURF1 protein, human
  • Smurf1 protein, mouse
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex