Positive and negative regulation of high affinity IgE receptor signaling by Src homology region 2 domain-containing phosphatase 1

J Immunol. 2008 Oct 15;181(8):5414-24. doi: 10.4049/jimmunol.181.8.5414.

Abstract

Src homology region 2 domain-containing phosphatase 1 (SHP-1), a cytoplasmic protein tyrosine phosphatase, plays an important role for the regulation of signaling from various hematopoietic cell receptors. Although SHP-1 is shown to be a negative signal modulator in mast cells, its precise molecular mechanisms are not well defined. To elucidate how SHP-1 regulates mast cell signaling, we established bone marrow-derived mast cells from SHP-1-deficient motheaten and wild-type mice and analyzed downstream signals induced by cross-linking of high affinity IgE receptor, Fc epsilonRI. Upon Fc epsilonRI ligation, motheaten-derived bone marrow-derived mast cells showed enhanced tyrosine phosphorylation of Src homology region 2 domain-containing leukocyte protein of 76 kDa (SLP-76) and linker for activation of T cells, activation of mitogen-activated protein kinases and gene transcription and production of cytokine. Because the activity of Syk, responsible for the phosphorylation of SLP-76 and linker for activation of T cells, is comparable irrespective of SHP-1, both molecules might be substrates of SHP-1 in mast cells. Interestingly, the absence of SHP-1 expression disrupted the association between SLP-76 and phospholipase Cgamma, which resulted in the decreased phospholipase Cgamma phosphorylation, calcium mobilization, and degranulation. Collectively, these results suggest that SHP-1 regulates Fc epsilonRI-induced downstream signaling events both negatively and positively by functioning as a protein tyrosine phosphatase and as an adaptor protein contributing to the formation of signaling complex, respectively.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Calcium / immunology
  • Calcium / metabolism
  • Cell Degranulation / genetics
  • Cell Degranulation / immunology*
  • Extracellular Signal-Regulated MAP Kinases
  • Gene Expression Regulation, Enzymologic / genetics
  • Gene Expression Regulation, Enzymologic / immunology*
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / immunology
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Mast Cells / enzymology
  • Mast Cells / immunology*
  • Mice
  • Mice, Mutant Strains
  • Phospholipase C gamma / genetics
  • Phospholipase C gamma / immunology
  • Phosphoproteins / genetics
  • Phosphoproteins / immunology
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / immunology*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / metabolism
  • Protein-Tyrosine Kinases / genetics
  • Protein-Tyrosine Kinases / immunology
  • Protein-Tyrosine Kinases / metabolism
  • Receptors, IgE / genetics
  • Receptors, IgE / immunology*
  • Receptors, IgE / metabolism
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Syk Kinase
  • T-Lymphocytes / enzymology
  • T-Lymphocytes / immunology

Substances

  • Adaptor Proteins, Signal Transducing
  • Intracellular Signaling Peptides and Proteins
  • Phosphoproteins
  • Receptors, IgE
  • SLP-76 signal Transducing adaptor proteins
  • Protein-Tyrosine Kinases
  • Syk Kinase
  • Syk protein, mouse
  • Extracellular Signal-Regulated MAP Kinases
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Ptpn6 protein, mouse
  • Phospholipase C gamma
  • Calcium