c-Cbl is involved in Met signaling in B cells and mediates hepatocyte growth factor-induced receptor ubiquitination

J Immunol. 2002 Oct 1;169(7):3793-800. doi: 10.4049/jimmunol.169.7.3793.

Abstract

Hepatocyte growth factor/scatter factor (HGF) and its receptor tyrosine kinase Met are key regulators of epithelial motility and morphogenesis. Recent studies indicate that the HGF/Met pathway also plays a role in B cell differentiation, whereas uncontrolled Met signaling may lead to B cell neoplasia. These observations prompted us to explore HGF/Met signaling in B cells. In this study, we demonstrate that HGF induces strong tyrosine phosphorylation of the proto-oncogene product c-Cbl in B cells and increases Cbl association with the Src family tyrosine kinases Fyn and Lyn, as well as with phosphatidylinositol-3 kinase and CrkL. In addition, we demonstrate that c-Cbl mediates HGF-induced ubiquitination of Met. This requires the juxtamembrane tyrosine Y1001 (Y2) of Met, but not the multifunctional docking site (Y14/15) or any additional C-terminal tyrosine residues (Y13-16). In contrast to wild-type c-Cbl, the transforming mutants v-Cbl and 70Z/3 Cbl, which lack the ubiquitin ligase RING finger domain, suppress Met ubiquitination. Our findings identify c-Cbl as a negative regulator of HGF/Met signaling in B cells, mediating ubiquitination and, consequently, proteosomal degradation of Met, and suggest a role for Cbl in Met-mediated tumorigenesis.

MeSH terms

  • Adaptor Proteins, Signal Transducing*
  • Animals
  • B-Lymphocytes / enzymology
  • B-Lymphocytes / metabolism*
  • COS Cells
  • Cell Membrane / enzymology
  • Cell Membrane / metabolism
  • Hepatocyte Growth Factor / physiology*
  • Humans
  • Ligases / metabolism
  • Nuclear Proteins / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation
  • Phosphotyrosine / metabolism
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins / physiology*
  • Proto-Oncogene Proteins c-cbl
  • Proto-Oncogene Proteins c-fyn
  • Proto-Oncogene Proteins c-met / metabolism
  • Proto-Oncogene Proteins c-met / physiology*
  • Signal Transduction* / immunology
  • Substrate Specificity
  • Tumor Cells, Cultured
  • Ubiquitin-Protein Ligases
  • Ubiquitins / metabolism*
  • src-Family Kinases / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • CRKL protein
  • MAS1 protein, human
  • Nuclear Proteins
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins
  • Ubiquitins
  • Phosphotyrosine
  • Hepatocyte Growth Factor
  • Proto-Oncogene Proteins c-cbl
  • Ubiquitin-Protein Ligases
  • Proto-Oncogene Proteins c-met
  • FYN protein, human
  • Proto-Oncogene Proteins c-fyn
  • lyn protein-tyrosine kinase
  • src-Family Kinases
  • Ligases
  • CBL protein, human