DNA damage-induced G2/M checkpoint in SV40 large T antigen-immortalized embryonic fibroblast cells requires SHP-2 tyrosine phosphatase

J Biol Chem. 2003 Oct 31;278(44):42812-20. doi: 10.1074/jbc.M305075200. Epub 2003 Aug 22.

Abstract

DNA damage induced by radiation or DNA-damaging agents leads to apoptosis and cell cycle arrest. However, DNA damage-triggered signal transduction involved in these cellular responses is not well understood. We previously demonstrated an important role for SHP-2, a ubiquitously expressed SH2 domain-containing tyrosine phosphatase, in the DNA damage-induced apoptotic response. Here we report a potential role for SHP-2 in a DNA damage-activated cell cycle checkpoint. Cell cycle analysis and the mitotic index assay showed that following DNA damage induced by cisplatin or gamma-irradiation, the G2 (but not S) arrest response was diminished in SV40 large T antigen-immortalized embryonic fibroblast cells lacking functional SHP-2. Notably, reintroduction of wild-type SHP-2 into the mutant cells fully restored the DNA damage-induced G2 arrest response, suggesting a direct role of SHP-2 in the G2/M checkpoint. Further biochemical analysis revealed that SHP-2 constitutively associated with 14-3-3beta, and that Cdc25C cytoplasmic translocation induced by DNA damage was essentially blocked in SHP-2 mutant cells. Additionally, we showed that following DNA damage, activation of p38 kinase was significantly elevated, while Erk kinase activation was decreased in mutant cells, and treatment of SHP-2 mutant cells with SB203580, a selective inhibitor for p38 kinase, partially restored the DNA damage-induced G2 arrest response. These results together provide the first evidence that SHP-2 tyrosine phosphatase enhances the DNA damage G2/M checkpoint in SV40 large T antigen immortalized murine embryonic fibroblast cells.

Publication types

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

MeSH terms

  • Animals
  • Antigens, Polyomavirus Transforming / metabolism*
  • Caffeine / pharmacology
  • Cell Cycle
  • Cell Cycle Proteins / metabolism
  • Cells, Cultured
  • Cisplatin / pharmacology
  • Cytoplasm / metabolism
  • DNA / drug effects
  • DNA / radiation effects
  • DNA Damage*
  • Enzyme Inhibitors / pharmacology
  • Fibroblasts / metabolism*
  • G2 Phase*
  • Gamma Rays
  • Immunoblotting
  • Intracellular Signaling Peptides and Proteins
  • Mice
  • Mitosis*
  • Nocodazole / pharmacology
  • Precipitin Tests
  • Protein Transport
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / metabolism*
  • SH2 Domain-Containing Protein Tyrosine Phosphatases
  • Time Factors
  • cdc25 Phosphatases / metabolism
  • src Homology Domains

Substances

  • Antigens, Polyomavirus Transforming
  • Cell Cycle Proteins
  • Enzyme Inhibitors
  • Intracellular Signaling Peptides and Proteins
  • Caffeine
  • DNA
  • Cdc25c protein, mouse
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse
  • SH2 Domain-Containing Protein Tyrosine Phosphatases
  • cdc25 Phosphatases
  • Cisplatin
  • Nocodazole