SHP-2 is a dual-specificity phosphatase involved in Stat1 dephosphorylation at both tyrosine and serine residues in nuclei

J Biol Chem. 2002 Dec 6;277(49):47572-80. doi: 10.1074/jbc.M207536200. Epub 2002 Sep 22.

Abstract

Signal transducer and activator of transcription (STAT) proteins are both tyrosine- and serine-phosphorylated, mediating signal transduction and gene regulation. Following gene regulation, STAT activity in the nucleus is then terminated by a nuclear protein phosphatase(s), which remains unidentified. Using novel antibody arrays to screen the Stat1-specific protein phosphatase(s), we identified a SHP-2-Stat1 interaction in the A431 cell nucleus. SHP-2 and Stat1 nuclear localization and their association in response to either epidermal growth factor or interferon-gamma (IFNgamma) were confirmed by immunofluorescent staining and affinity precipitation assays. The SHP-2 C-terminal region containing protein-tyrosine phosphatase activity interacted with the C-terminal SH2 transcriptional activation domain of Stat1. In SHP-2-/- mouse fibroblast cells, Stat1 phosphorylation at both the tyrosine residue Tyr(701) and the serine residue Ser(727) by IFNgamma was enhanced and prolonged. Consistently, purified GST-SHP-2 dephosphorylated Stat1 at both tyrosine and serine residues when immunoprecipitated phospho-Stat1 or a peptide corresponding to the sequence surrounding Tyr(P)(701) or Ser(P)(727) of Stat1 was used as the substrate. Overexpression of SHP-2 in 293T cells inhibited IFNgamma-dependent Stat1 phosphorylation and suppressed Stat1-dependent induction of luciferase activity. Our findings demonstrate that SHP-2 is a dual-specificity protein phosphatase involved in Stat1 dephosphorylation at both tyrosine and serine residues and plays an important role in modulating STAT function in gene regulation.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Amino Acid Sequence
  • Animals
  • Cell Line
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • DNA / metabolism
  • DNA, Complementary / metabolism
  • DNA-Binding Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Electrophoresis, Polyacrylamide Gel
  • Fibroblasts / metabolism
  • Gene Expression Regulation
  • Glutathione Transferase / metabolism
  • Humans
  • Interferon-gamma / metabolism
  • Intracellular Signaling Peptides and Proteins
  • Luciferases / metabolism
  • Mice
  • Microscopy, Fluorescence
  • Molecular Sequence Data
  • Phosphorylation
  • Precipitin Tests
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / metabolism*
  • Protein Tyrosine Phosphatases / physiology*
  • STAT1 Transcription Factor
  • Sequence Homology, Amino Acid
  • Serine / chemistry*
  • Serine / metabolism
  • Time Factors
  • Trans-Activators / metabolism*
  • Tumor Cells, Cultured
  • Tyrosine / chemistry*
  • Tyrosine / metabolism

Substances

  • DNA, Complementary
  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Stat1 protein, mouse
  • Trans-Activators
  • Tyrosine
  • Serine
  • Interferon-gamma
  • DNA
  • Luciferases
  • Glutathione Transferase
  • PTPN11 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse