RASopathy-associated CBL germline mutations cause aberrant ubiquitylation and trafficking of EGFR

Hum Mutat. 2014 Nov;35(11):1372-81. doi: 10.1002/humu.22682.

Abstract

Noonan syndrome, a congenital disorder comprising a characteristic face, short stature, heart defects, learning difficulties, and a predisposition to malignancies, is caused by heterozygous germline mutations in genes encoding components of RAS-MAPK signaling pathways. Mutations in the CBL tumor suppressor gene have been reported in patients with a Noonan syndrome-like phenotype. CBL encodes a multivalent adaptor protein with ubiquitin ligase activity, which promotes ubiquitylation and vesicle-mediated internalization and degradation of the epidermal growth factor (EGF) receptor (EGFR). We investigated the functional consequences of disease-associated CBL amino acid changes p.K382E, p.D390Y, and p.R420Q on ligand-induced EGFR trafficking. Expression of CBL(K382E), CBL(D390Y), or CBL(R420Q) in COS-7 cells resulted in increased levels of surface EGFR and reduced amounts of intracellular EGFR; both consequences indicate ineffective EGFR internalization. Accordingly, receptor-mediated uptake of EGF was decreased. Furthermore, the p.K382E, p.D390Y, and p.R420Q lesions impaired CBL-mediated EGFR ubiquitylation and degradation. Together, these data indicate that pathogenic CBL mutations severely affect vesicle-based EGFR trafficking. Since we detected enhanced ERK phosphorylation in cells expressing mutant CBL, we conclude that aberrant EGFR trafficking contributes to augmented RAS-MAPK signaling, the common trait of Noonan syndrome and related RASopathies. Thus, our data suggest that EGFR trafficking is a novel disease-relevant regulatory level in the RASopathy network.

Keywords: CBL; EGFR trafficking; Noonan syndrome; RASopathies; c-Cbl.

MeSH terms

  • Amino Acid Substitution
  • Animals
  • ErbB Receptors / metabolism*
  • Gene Expression
  • Genetic Association Studies*
  • Germ-Line Mutation*
  • Humans
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation, Missense
  • Noonan Syndrome / genetics
  • Noonan Syndrome / metabolism
  • Protein Transport
  • Proteolysis
  • Proto-Oncogene Proteins c-cbl / genetics*
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • Signal Transduction
  • Ubiquitination

Substances

  • Proto-Oncogene Proteins c-cbl
  • ErbB Receptors
  • Mitogen-Activated Protein Kinases
  • Proto-Oncogene Proteins p21(ras)