Catalytic-dependent and -independent roles of SHP-2 tyrosine phosphatase in interleukin-3 signaling

Oncogene. 2003 Sep 4;22(38):5995-6004. doi: 10.1038/sj.onc.1206846.

Abstract

SHP-2 tyrosine phosphatase is highly expressed in hematopoietic cells, however, the function of SHP-2 in hematopoietic cell signaling is not well understood. Here we focus on the role of SHP-2 phosphatase in the signal transduction of interleukin (IL)-3, a cytokine involved in hematopoietic cell survival, proliferation, and differentiation. We established immortalized SHP-2(-/-) hematopoietic cell pools and showed that IL-3-induced proliferative response was diminished in SHP-2(-/-) cells. Moreover, inhibition of the catalytic activity of SHP-2 in wild-type (WT) bone marrow hematopoietic progenitor cells and Ba/F3 cells by overexpression of catalytically inactive SHP-2 mutant suppressed their differentiative and proliferative responses to IL-3, demonstrating an important positive role for SHP-2 in IL-3 signal transduction. Further biochemical analyses revealed that IL-3-induced Jak/Stat, Erk, and PI3 kinase pathways in SHP-2(-/-) cells were impaired and reintroduction of WT SHP-2 into mutant cells partially restored IL-3 signaling. Interestingly, in catalytically inactive SHP-2-overexpressing Ba/F3 cells, although IL-3-induced activation of Jak2 and Erk kinases was reduced and shortened, PI3 kinase activation remained unaltered. Taken together, these results suggest that SHP-2 tyrosine phosphatase plays multiple roles in IL-3 signal transduction, functioning in both catalytic-dependent and -independent manners in the Jak/Stat, Erk, and PI3 kinase pathways.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Catalysis
  • Cell Division / drug effects
  • Cell Line, Transformed
  • Cells, Cultured
  • DNA-Binding Proteins / metabolism
  • Gene Transfer Techniques
  • Hematopoietic Stem Cells / drug effects
  • Hematopoietic Stem Cells / metabolism
  • Homeodomain Proteins / genetics
  • Interleukin-3 / metabolism*
  • Interleukin-3 / pharmacology
  • Intracellular Signaling Peptides and Proteins
  • Janus Kinase 2
  • Mice
  • Mice, Mutant Strains
  • Milk Proteins*
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation
  • Oncogene Proteins / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / genetics
  • Protein Tyrosine Phosphatases / metabolism*
  • Protein-Tyrosine Kinases / metabolism
  • Proto-Oncogene Proteins*
  • Receptors, Interleukin-3 / metabolism
  • STAT5 Transcription Factor
  • Signal Transduction / physiology*
  • Trans-Activators / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • DNA-Binding Proteins
  • Gab1 protein, mouse
  • Homeodomain Proteins
  • Interleukin-3
  • Intracellular Signaling Peptides and Proteins
  • Milk Proteins
  • Oncogene Proteins
  • Phosphoproteins
  • Proto-Oncogene Proteins
  • Receptors, Interleukin-3
  • STAT5 Transcription Factor
  • Tlx1 protein, mouse
  • Trans-Activators
  • Protein-Tyrosine Kinases
  • Jak2 protein, mouse
  • Janus Kinase 2
  • Mitogen-Activated Protein Kinases
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse