A molecular model for the mechanism of acquired tamoxifen resistance in breast cancer

Eur J Cancer. 2014 Nov;50(16):2866-76. doi: 10.1016/j.ejca.2014.08.011. Epub 2014 Sep 6.

Abstract

Purpose: Oestrogen (E2)-stimulated growth re-emerges after a c-Src inhibitor blocking E2-induced apoptosis. A resulting cell line, MCF-7:PF, is selected with features of functional oestrogen receptor (ER) and over-expression of insulin-like growth factor-1 receptor beta (IGF-1Rβ). We addressed the question of whether the selective ER modulator (SERM), 4-hydroxytamoxifen (4-OHT) or other SERMs could target ER to prevent E2-stimulated growth in MCF-7:PF cells.

Methods: Protein levels of receptors and signalling pathways were examined by immunoblotting. Expression of mRNA was measured through real-time RT-PCR. Recruitment of ER or nuclear receptor coactivator 3 (SRC3) to the promoter of ER-target gene was detected by chromatin-immunoprecipitation (ChIP).

Results: 4-OHT and other SERMs stimulated cell growth in an ER-dependent manner. However, unlike E2, 4-OHT suppressed classical ER-target genes as does the pure antioestrogen ICI 182,780 (ICI). ChIP assay indicated that 4-OHT did not recruit ER or SRC3 to the promoter of ER-target gene, pS2. Paradoxically, 4-OHT reduced total IGF-1Rβ but increased phosphorylation of IGF-1Rβ. Mechanistic studies revealed that 4-OHT functioned as an agonist to enhance the non-genomic activity of ER and activate focal adhesion molecules to further increase phosphorylation of IGF-1Rβ. Disruption of membrane-associated signalling, IGF-1R and focal adhesion kinase (FAK), completely abolished 4-OHT-stimulated cell growth.

Conclusions: This study is the first to recapitulate a cellular model in vitro of acquired tamoxifen resistance developed in athymic mice in vivo. Importantly, it provides a rationale that membrane-associated pathways may be valuable therapeutic targets for tamoxifen resistant patients in clinic.

Keywords: Focal adhesion molecules; Insulin-like growth factor-1 receptor beta (IGF-1Rβ); Non-genomic pathway; Resistance; Selective oestrogen receptor modulator (SERM).

Publication types

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

MeSH terms

  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / pathology*
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm*
  • Estrogen Receptor Modulators / therapeutic use
  • Estrogens / chemistry
  • Female
  • Humans
  • MCF-7 Cells
  • Phosphorylation
  • Receptor, IGF Type 1 / metabolism
  • Receptors, Estrogen / metabolism
  • Selective Estrogen Receptor Modulators / therapeutic use
  • Signal Transduction
  • Tamoxifen / administration & dosage*
  • Tamoxifen / analogs & derivatives
  • Tamoxifen / therapeutic use

Substances

  • Estrogen Receptor Modulators
  • Estrogens
  • Receptors, Estrogen
  • Selective Estrogen Receptor Modulators
  • Tamoxifen
  • afimoxifene
  • Receptor, IGF Type 1