Docking protein Gab2 is phosphorylated by ZAP-70 and negatively regulates T cell receptor signaling by recruitment of inhibitory molecules

J Biol Chem. 2001 Nov 30;276(48):45175-83. doi: 10.1074/jbc.M105384200. Epub 2001 Sep 25.

Abstract

To maintain various T cell responses and immune equilibrium, activation signals triggered by T cell antigen receptor (TCR) must be regulated by inhibitory signals. Gab2, an adaptor protein of the insulin receptor substrate-1 family, has been shown to be involved in the downstream signaling from cytokine receptors. We investigated the functional role of Gab2 in TCR-mediated signal transduction. Gab2 was phosphorylated by ZAP-70 and co-precipitated with phosphoproteins, such as ZAP-70, LAT, and CD3zeta, upon TCR stimulation. Overexpression of Gab2 in Jurkat cells or antigen-specific T cell hybridomas resulted in the inhibition of NF-AT activation, interleukin-2 production, and tyrosine phosphorylation. The structure-function relationship of Gab2 was analyzed by mutants of Gab2. The Gab2 mutants lacking SHP-2-binding sites mostly abrogated the inhibitory activity of Gab2, but its inhibitory function was restored by fusing to active SHP-2 as a chimeric protein. A mutant with defective phosphatidylinositol 3-kinase binding capacity also impaired the inhibitory activity, and the pleckstrin homology domain-deletion mutant revealed a crucial function of the pleckstrin homology domain for localization to the plasma membrane. These results suggest that Gab2 is a substrate of ZAP-70 and functions as a switch molecule toward inhibition of TCR signal transduction by mediating the recruitment of inhibitory molecules to the TCR signaling complex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing*
  • Animals
  • Antigens, CD / biosynthesis
  • Antigens, Differentiation, T-Lymphocyte / biosynthesis
  • Binding Sites
  • Blotting, Western
  • CD3 Complex / metabolism
  • Carrier Proteins / metabolism
  • Cell Line
  • Cytokines / metabolism
  • DNA / metabolism
  • Dose-Response Relationship, Drug
  • Flow Cytometry
  • Humans
  • Hybridomas / metabolism
  • Interleukin-2 / biosynthesis
  • Intracellular Signaling Peptides and Proteins
  • Jurkat Cells
  • Lectins, C-Type
  • Luciferases / metabolism
  • Lymphocyte Activation
  • Membrane Proteins*
  • Mice
  • Mutation
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoproteins / metabolism*
  • Phosphorylation*
  • Precipitin Tests
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases / metabolism
  • Protein-Tyrosine Kinases / metabolism*
  • Receptors, Antigen, T-Cell / metabolism*
  • SH2 Domain-Containing Protein Tyrosine Phosphatases
  • Signal Transduction*
  • Structure-Activity Relationship
  • Transfection
  • Tyrosine / metabolism
  • ZAP-70 Protein-Tyrosine Kinase
  • src Homology Domains

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD3 Complex
  • CD3 antigen, zeta chain
  • CD69 antigen
  • Carrier Proteins
  • Cytokines
  • GAB2 protein, human
  • Gab2 protein, mouse
  • Interleukin-2
  • Intracellular Signaling Peptides and Proteins
  • LAT protein, human
  • Lat protein, mouse
  • Lectins, C-Type
  • Membrane Proteins
  • Phosphoproteins
  • Receptors, Antigen, T-Cell
  • Tyrosine
  • DNA
  • Luciferases
  • Phosphatidylinositol 3-Kinases
  • Protein-Tyrosine Kinases
  • ZAP-70 Protein-Tyrosine Kinase
  • ZAP70 protein, human
  • Zap70 protein, mouse
  • PTPN11 protein, human
  • PTPN6 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse
  • Ptpn6 protein, mouse
  • SH2 Domain-Containing Protein Tyrosine Phosphatases