Heregulin-expressing HER2-positive breast and gastric cancer exhibited heterogeneous susceptibility to the anti-HER2 agents lapatinib, trastuzumab and T-DM1

Oncotarget. 2016 Dec 20;7(51):84860-84871. doi: 10.18632/oncotarget.12743.

Abstract

Background: Overexpression of heregulin, a HER3 ligand, is one mechanism that confers resistance to the anti-HER2 agents trastuzumab and lapatinib. We investigated the impact of heregulin expression on the efficacy of HER2-targeted therapeutic agents, including trastuzumab, trastuzumab emtansine (T-DM1) and lapatinib, in vitro and in vivo and evaluated the heregulin messenger RNA (mRNA) levels in specimens from patients with HER2-positive breast or gastric cancer.

Results: Cell proliferation and apoptosis assays demonstrated that heregulin conferred robust resistance to lapatinib and trastuzumab via HER3-Akt pathway activation followed by survivin overexpression; however, heregulin conferred minimal or no resistance to T-DM1 and paclitaxel. The heregulin mRNA level of one of 10 patients was up-regulated after the acquisition of resistance to trastuzumab-based therapy.

Materials and methods: SK-BR-3, NCI-N87, BT-474, MDA-MB-453, HCC1954, SNU-216 and 4-1ST cells were pharmacologically treated with recombinant heregulin or transfected with the heregulin gene. We also assessed the expression of heregulin mRNA in HER2-positive breast or gastric cancer samples before and after trastuzumab-based therapy using a RT-PCR-based method.

Conclusions: mRNA up-regulation of heregulin was observed in clinical breast cancer specimens during trastuzumab-based treatment, but heregulin overexpression had a limited effect on the sensitivity to T-DM1 in vitro and in vivo.

Keywords: HER2; T-DM1; breast cancer; heregulin; resistance.

MeSH terms

  • Ado-Trastuzumab Emtansine
  • Aged
  • Apoptosis / drug effects
  • Breast Neoplasms / drug therapy*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm
  • Female
  • Humans
  • Inhibitor of Apoptosis Proteins / genetics
  • Inhibitor of Apoptosis Proteins / metabolism
  • Lapatinib
  • Male
  • Maytansine / analogs & derivatives*
  • Maytansine / therapeutic use
  • Middle Aged
  • Neuregulin-1 / metabolism*
  • Oncogene Protein v-akt / metabolism
  • Quinazolines / therapeutic use*
  • Receptor, ErbB-2 / metabolism*
  • Receptor, ErbB-3 / metabolism
  • Signal Transduction / drug effects
  • Stomach Neoplasms / drug therapy*
  • Survivin
  • Trastuzumab / therapeutic use*

Substances

  • BIRC5 protein, human
  • Inhibitor of Apoptosis Proteins
  • Neuregulin-1
  • Quinazolines
  • Survivin
  • Lapatinib
  • Maytansine
  • ERBB2 protein, human
  • ERBB3 protein, human
  • Receptor, ErbB-2
  • Receptor, ErbB-3
  • Oncogene Protein v-akt
  • Trastuzumab
  • Ado-Trastuzumab Emtansine