Sustained Inhibition of HER3 and EGFR Is Necessary to Induce Regression of HER2-Amplified Gastrointestinal Carcinomas

Clin Cancer Res. 2015 Dec 15;21(24):5519-31. doi: 10.1158/1078-0432.CCR-14-3066. Epub 2015 Aug 21.

Abstract

Purpose: Preclinical studies in HER2-amplified gastrointestinal cancer models have shown that cotargeting HER2 with a monoclonal antibody and a small molecule is superior to monotherapy with either inhibitor, but the underlying cooperative mechanisms remain unexplored. We investigated the molecular underpinnings of this synergy to identify key vulnerabilities susceptible to alternative therapeutic opportunities.

Experimental design: The phosphorylation/activation of HER2, HER3, EGFR (HER receptors), and downstream transducers was evaluated in HER2-overexpressing colorectal and gastric cancer cell lines by Western blotting and/or multiplex phosphoproteomics. The in vivo outcome of antibody-mediated HER2 blockade by trastuzumab, reversible HER2 inhibition by lapatinib, and irreversible HER2 inhibition by afatinib was assessed in patient-derived tumorgrafts and cell-line xenografts by monitoring tumor growth curves and by using antibody-based proximity assays.

Results: Trastuzumab monotherapy reduced HER3 phosphorylation, with minor consequences on downstream transducers. Lapatinib alone acutely inhibited all HER receptors and effectors but led to delayed rephosphorylation of HER3 and EGFR and partial restoration of ERK and AKT activity. When combined with lapatinib, trastuzumab prevented HER3/EGFR reactivation and caused prolonged inhibition of ERK/AKT. Afatinib alone was also very effective in counteracting the reinstatement of HER3, EGFR, and downstream signaling activation. In vivo, the combination of trastuzumab and lapatinib-or, importantly, monotherapy with afatinib-resulted in overt tumor shrinkage.

Conclusions: Only prolonged inhibition of HER3 and EGFR, achievable by dual blockade with trastuzumab and lapatinib or irreversible HER2 inhibition by single-agent afatinib, led to regression of HER2-amplified gastrointestinal carcinomas. Clin Cancer Res; 21(24); 5519-31. ©2015 AACR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afatinib
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Carcinoma / drug therapy
  • Carcinoma / genetics*
  • Carcinoma / metabolism*
  • Carcinoma / pathology
  • Cell Line, Tumor
  • Disease Models, Animal
  • Drug Synergism
  • Drug Therapy, Combination
  • ErbB Receptors / antagonists & inhibitors*
  • ErbB Receptors / metabolism
  • Gastrointestinal Neoplasms / drug therapy
  • Gastrointestinal Neoplasms / genetics*
  • Gastrointestinal Neoplasms / metabolism*
  • Gastrointestinal Neoplasms / pathology
  • Gene Amplification
  • Gene Expression
  • Gene Knockdown Techniques
  • Humans
  • Lapatinib
  • Mice
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology*
  • Quinazolines / administration & dosage
  • Quinazolines / pharmacology
  • Receptor, ErbB-2 / genetics*
  • Receptor, ErbB-2 / metabolism
  • Receptor, ErbB-3 / antagonists & inhibitors*
  • Receptor, ErbB-3 / genetics
  • Receptor, ErbB-3 / metabolism
  • Signal Transduction / drug effects
  • Trastuzumab / administration & dosage
  • Trastuzumab / pharmacology
  • Tumor Burden / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Protein Kinase Inhibitors
  • Quinazolines
  • Lapatinib
  • Afatinib
  • ErbB Receptors
  • Receptor, ErbB-2
  • Receptor, ErbB-3
  • Trastuzumab