The ShcA PTB domain functions as a biological sensor of phosphotyrosine signaling during breast cancer progression

Cancer Res. 2013 Jul 15;73(14):4521-32. doi: 10.1158/0008-5472.CAN-12-4178. Epub 2013 May 21.

Abstract

ShcA (SHC1) is an adapter protein that possesses an SH2 and a PTB phosphotyrosine-binding motif. ShcA generally uses its PTB domain to engage activated receptor tyrosine kinases (RTK), but there has not been a definitive determination of the role of this domain in tumorigenesis. To address this question, we employed a ShcA mutant (R175Q) that no longer binds phosphotyrosine residues via its PTB domain. Here, we report that transgenic expression of this mutant delays onset of mammary tumors in the MMTV-PyMT mouse model of breast cancer. Paradoxically, we observed a robust increase in the growth and angiogenesis of mammary tumors expressing ShcR175Q, which displayed increased secretion of fibronectin and expression of integrin α5/β1, the principal fibronectin receptor. Sustained integrin engagement activated Src, which in turn phosphorylated proangiogenic RTKs, including platelet-derived growth factor receptor, fibroblast growth factor receptor, and Met, leading to increased VEGF secretion from ShcR175Q-expressing breast cancer cells. We defined a ShcR175Q-dependent gene signature that could stratify breast cancer patients with a high microvessel density. This study offers the first in vivo evidence of a critical role for intracellular signaling pathways downstream of the ShcA PTB domain, which both positively and negatively regulate tumorigenesis during various stages of breast cancer progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / blood supply
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Disease Progression
  • Female
  • Fibronectins / metabolism
  • Humans
  • Integrin alpha5beta1 / metabolism
  • Mammary Neoplasms, Experimental / blood supply
  • Mammary Neoplasms, Experimental / genetics
  • Mammary Neoplasms, Experimental / metabolism
  • Mammary Neoplasms, Experimental / pathology
  • Mice
  • Mice, Transgenic
  • Mutation
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / metabolism
  • Phosphotyrosine / metabolism*
  • Protein Structure, Tertiary
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Shc Signaling Adaptor Proteins / genetics
  • Shc Signaling Adaptor Proteins / metabolism*
  • Signal Transduction
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Fibronectins
  • Integrin alpha5beta1
  • Shc Signaling Adaptor Proteins
  • Vascular Endothelial Growth Factor A
  • Phosphotyrosine
  • Receptor Protein-Tyrosine Kinases