Temporal regulation of EGF signalling networks by the scaffold protein Shc1

Nature. 2013 Jul 11;499(7457):166-71. doi: 10.1038/nature12308.

Abstract

Cell-surface receptors frequently use scaffold proteins to recruit cytoplasmic targets, but the rationale for this is uncertain. Activated receptor tyrosine kinases, for example, engage scaffolds such as Shc1 that contain phosphotyrosine (pTyr)-binding (PTB) domains. Using quantitative mass spectrometry, here we show that mammalian Shc1 responds to epidermal growth factor (EGF) stimulation through multiple waves of distinct phosphorylation events and protein interactions. After stimulation, Shc1 rapidly binds a group of proteins that activate pro-mitogenic or survival pathways dependent on recruitment of the Grb2 adaptor to Shc1 pTyr sites. Akt-mediated feedback phosphorylation of Shc1 Ser 29 then recruits the Ptpn12 tyrosine phosphatase. This is followed by a sub-network of proteins involved in cytoskeletal reorganization, trafficking and signal termination that binds Shc1 with delayed kinetics, largely through the SgK269 pseudokinase/adaptor protein. Ptpn12 acts as a switch to convert Shc1 from pTyr/Grb2-based signalling to SgK269-mediated pathways that regulate cell invasion and morphogenesis. The Shc1 scaffold therefore directs the temporal flow of signalling information after EGF stimulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast / cytology
  • Cell Line
  • Epidermal Growth Factor / metabolism*
  • Epithelial Cells / cytology
  • ErbB Receptors / agonists
  • ErbB Receptors / metabolism
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Feedback, Physiological
  • GRB2 Adaptor Protein / deficiency
  • GRB2 Adaptor Protein / genetics
  • GRB2 Adaptor Protein / metabolism
  • Humans
  • Mice
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / metabolism
  • Phosphorylation
  • Protein Binding
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Shc Signaling Adaptor Proteins / deficiency
  • Shc Signaling Adaptor Proteins / genetics
  • Shc Signaling Adaptor Proteins / metabolism*
  • Signal Transduction*
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Time Factors

Substances

  • GRB2 Adaptor Protein
  • Multiprotein Complexes
  • Shc Signaling Adaptor Proteins
  • Shc1 protein, mouse
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Epidermal Growth Factor
  • ErbB Receptors
  • PEAK1 protein, human
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases