A combination of trastuzumab and BAG-1 inhibition synergistically targets HER2 positive breast cancer cells

Oncotarget. 2016 Apr 5;7(14):18851-64. doi: 10.18632/oncotarget.7944.

Abstract

Treatment of HER2+ breast cancer with trastuzumab is effective and combination anti-HER2 therapies have demonstrated benefit over monotherapy in the neoadjuvant and metastatic settings. This study investigated the therapeutic potential of targeting the BAG-1 protein co-chaperone in trastuzumab-responsive or -resistant cells. In the METABRIC dataset, BAG-1 mRNA was significantly elevated in HER2+ breast tumors and predicted overall survival in a multivariate analysis (HR = 0.81; p = 0.022). In a breast cell line panel, BAG-1 protein was increased in HER2+ cells and was required for optimal growth as shown by siRNA knockdown. Overexpression of BAG-1S in HER2+ SKBR3 cells blocked growth inhibition by trastuzumab, whereas overexpression of a mutant BAG-1S protein (BAG-1S H3AB), defective in binding HSC70, potentiated the effect of trastuzumab. Injection of a Tet-On SKBR3 clone, induced to overexpress myc-BAG-1S into the mammary fat pads of immunocompromised mice, resulted in 2-fold larger tumors compared to uninduced controls. Induction of myc-BAG-1S expression in two Tet-On SKBR3 clones attenuated growth inhibition by trastuzumab in vitro. Targeting endogenous BAG-1 by siRNA enhanced growth inhibition of SKBR3 and BT474 cells by trastuzumab, while BAG-1 protein-protein interaction inhibitor (Thio-S or Thio-2) plus trastuzumab combination treatment synergistically attenuated growth. In BT474 cells this reduced protein synthesis, caused G1/S cell cycle arrest and targeted the ERK and AKT signaling pathways. In a SKBR3 subpopulation with acquired resistance to trastuzumab BAG-1 targeting remained effective and either Thio-2 or BAG-1 siRNA reduced growth more compared to trastuzumab-responsive parental cells. In summary, targeting BAG-1 function in combination with anti-HER2 therapy might prove beneficial.

Keywords: BAG-1; HER2; breast cancer; resistance; trastuzumab.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aniline Compounds / administration & dosage
  • Aniline Compounds / pharmacology
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Benzothiazoles / administration & dosage
  • Benzothiazoles / pharmacology
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / enzymology
  • Breast Neoplasms / pathology
  • Cell Proliferation / drug effects
  • Combined Modality Therapy
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drug Synergism
  • Female
  • Humans
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • RNA, Small Interfering / administration & dosage
  • RNA, Small Interfering / genetics
  • Receptor, ErbB-2 / biosynthesis*
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transfection
  • Trastuzumab / administration & dosage
  • Trastuzumab / pharmacology*
  • Xenograft Model Antitumor Assays

Substances

  • Aniline Compounds
  • BCL2-associated athanogene 1 protein
  • Benzothiazoles
  • DNA-Binding Proteins
  • N-ethyl-4-(6-methylbenzo(d)thiazol-2-yl)aniline
  • RNA, Small Interfering
  • Transcription Factors
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • Trastuzumab