Co-occurring gain-of-function mutations in HER2 and HER3 modulate HER2/HER3 activation, oncogenesis, and HER2 inhibitor sensitivity

Cancer Cell. 2021 Aug 9;39(8):1099-1114.e8. doi: 10.1016/j.ccell.2021.06.001. Epub 2021 Jun 24.

Abstract

Activating mutations in HER2 (ERBB2) drive the growth of a subset of breast and other cancers and tend to co-occur with HER3 (ERBB3) missense mutations. The HER2 tyrosine kinase inhibitor neratinib has shown clinical activity against HER2-mutant tumors. To characterize the role of HER3 mutations in HER2-mutant tumors, we integrate computational structural modeling with biochemical and cell biological analyses. Computational modeling predicts that the frequent HER3E928G kinase domain mutation enhances the affinity of HER2/HER3 and reduces binding of HER2 to its inhibitor neratinib. Co-expression of mutant HER2/HER3 enhances HER2/HER3 co-immunoprecipitation and ligand-independent activation of HER2/HER3 and PI3K/AKT, resulting in enhanced growth, invasiveness, and resistance to HER2-targeted therapies, which can be reversed by combined treatment with PI3Kα inhibitors. Our results provide a mechanistic rationale for the evolutionary selection of co-occurring HER2/HER3 mutations and the recent clinical observations that HER3 mutations are associated with a poor response to neratinib in HER2-mutant cancers.

Keywords: HER2; HER3; PI3K; Rosetta; breast cancer; molecular dynamics; neratinib; personalized structural biology; precision oncology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminopyridines / administration & dosage
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics
  • Female
  • Gain of Function Mutation*
  • Humans
  • Mice
  • Mice, Nude
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Morpholines / administration & dosage
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors / administration & dosage
  • Protein Multimerization
  • Quinolines / administration & dosage
  • Quinolines / chemistry
  • Quinolines / metabolism
  • Quinolines / pharmacology*
  • Receptor, ErbB-2 / antagonists & inhibitors
  • Receptor, ErbB-2 / chemistry
  • Receptor, ErbB-2 / genetics*
  • Receptor, ErbB-2 / metabolism
  • Receptor, ErbB-3 / chemistry
  • Receptor, ErbB-3 / genetics*
  • Receptor, ErbB-3 / metabolism
  • Trastuzumab / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Aminopyridines
  • Morpholines
  • NVP-BKM120
  • Phosphoinositide-3 Kinase Inhibitors
  • Quinolines
  • ERBB2 protein, human
  • ERBB3 protein, human
  • Receptor, ErbB-2
  • Receptor, ErbB-3
  • neratinib
  • Trastuzumab