Tumor microenvironmental growth factors induce long-term estrogen deprivation resistance in breast cancer

Breast Cancer. 2019 Nov;26(6):748-757. doi: 10.1007/s12282-019-00978-z. Epub 2019 May 22.

Abstract

Background: Hormonal therapy is an effective treatment for luminal-like breast cancer. Aromatase inhibitor (AI) is widely used for estrogen receptor-positive, postmenopausal breast cancers. However, resistance is occurred and becomes a serious clinical concern. In general, progression of cancer strongly depends on tumor microenvironment, which may, therefore, also contribute to the development of AI resistance.

Methods: We evaluated tumor microenvironment-derived factors with respect to AI resistance using typical estrogen receptor-positive breast cancer cell lines. We established tumor microenvironment-dependent AI-resistant models and elucidated the underlying mechanisms.

Results: T-47D cells had a higher dependence on microenvironment-derived factors, such as estrogen or growth factors, for survival than MCF-7 cells. We, therefore, evaluated tumor microenvironment growth factors with respect to AI resistance using T-47D cells. We established three resistant cell lines (V1, V2, and V3) that survived estrogen deprivation and growth factor-supplemented conditions. These cell lines were deficient in estrogen receptor α expression and estrogen-dependent growth. Among six representative growth factors, epidermal growth factor was the most influential. In these models, HER2 protein was overexpressed without gene amplification and intracellular phosphorylation pathways were activated compared to parental cell lines. Molecular targeting inhibitors revealed that V1 and V2 primarily rely on the PI3 K pathway for survival, whereas V3 relies on the MAPK pathway.

Conclusions: This study demonstrates the importance of tumor microenvironment-derived factors for the development of AI resistance. These resistant models did not utilize the same resistance mechanism, suggesting that flexible strategies are essential in conquering resistance.

Keywords: Aromatase inhibitor; Breast cancer; Hormonal therapy resistance; Tumor microenvironment.

MeSH terms

  • Aromatase Inhibitors / adverse effects
  • Aromatase Inhibitors / therapeutic use
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm*
  • Epidermal Growth Factor / metabolism*
  • Estrogen Receptor alpha / genetics
  • Estrogen Receptor alpha / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • MCF-7 Cells
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors / pharmacology
  • Receptor, ErbB-2 / metabolism
  • Thiazoles / pharmacology
  • Transfection
  • Tumor Microenvironment*

Substances

  • Aromatase Inhibitors
  • ESR1 protein, human
  • Estrogen Receptor alpha
  • Phosphoinositide-3 Kinase Inhibitors
  • Thiazoles
  • Alpelisib
  • Epidermal Growth Factor
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • Mitogen-Activated Protein Kinases