Epidermal growth factor receptor and HER-3 restrict cell response to sorafenib in hepatocellular carcinoma cells

J Hepatol. 2012 Jul;57(1):108-15. doi: 10.1016/j.jhep.2012.02.019. Epub 2012 Mar 10.

Abstract

Background & aims: Sorafenib is the standard of care for the treatment of advanced hepatocellular carcinoma (HCC). However, primary and acquired resistance is observed in patients. We examined whether gefitinib, which inhibits both epidermal growth factor receptor (EGFR) and HER-3 phosphorylation, could improve HCC cell response to sorafenib.

Methods: Sorafenib and gefitinib were tested in HCC tumor xenografts and in sorafenib-sensitive and sorafenib-resistant HCC cell lines. Biomarkers relevant to the HER system were analyzed by Western blotting and ELISA. RNA interference was used to downregulate the HER system. Amphiregulin concentrations were measured by ELISA in sera from patients under sorafenib treatment.

Results: Sorafenib combined with gefitinib significantly inhibited tumor growth in mice and reduced cell viability in vitro compared to single agents. In cell lines cultured in 10% serum or treated with EGF, sorafenib alone inhibited phospho-STAT3 while it maintained or even increased phospho-ERK and/or phospho-AKT. The paradoxical effects of sorafenib were prevented by gefitinib or by downregulation of EGFR and HER-3 expression. In cells with acquired resistance to sorafenib, aberrant activation of EGFR/HER-3 receptors as well as overexpression of several EGFR ligands were observed. These enhanced autocrine/paracrine loops led to the constitutive activation of ERK and AKT and conferred increased sensitivity to gefitinib. Increased serum concentrations of amphiregulin were observed in 10 out of 14 patients under sorafenib treatment compared to baselines.

Conclusions: Signaling pathways controlled by EGFR and HER-3 restrict sorafenib effects both in naive and sorafenib-resistant HCC cells. Consequently, gefitinib cooperates with sorafenib to increase antiproliferative response and to prevent resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Amphiregulin
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Benzenesulfonates / pharmacology*
  • Benzenesulfonates / therapeutic use
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Hepatocellular / drug therapy*
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Cell Division / drug effects
  • Cell Division / physiology
  • Drug Resistance, Neoplasm / physiology
  • EGF Family of Proteins
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / metabolism*
  • Female
  • Gefitinib
  • Glycoproteins / metabolism
  • Hep G2 Cells
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Liver Neoplasms, Experimental / drug therapy*
  • Liver Neoplasms, Experimental / metabolism
  • Liver Neoplasms, Experimental / pathology
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology
  • Male
  • Mice
  • Mice, Nude
  • Middle Aged
  • Niacinamide / analogs & derivatives
  • Phenylurea Compounds
  • Pyridines / pharmacology*
  • Pyridines / therapeutic use
  • Quinazolines / pharmacology
  • Receptor, ErbB-3 / metabolism*
  • Sorafenib
  • Xenograft Model Antitumor Assays

Substances

  • AREG protein, human
  • Amphiregulin
  • Antineoplastic Agents
  • Areg protein, mouse
  • Benzenesulfonates
  • Biomarkers, Tumor
  • EGF Family of Proteins
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Phenylurea Compounds
  • Pyridines
  • Quinazolines
  • Niacinamide
  • Sorafenib
  • ErbB Receptors
  • Receptor, ErbB-3
  • Gefitinib