Adaptation to AI Therapy in Breast Cancer Can Induce Dynamic Alterations in ER Activity Resulting in Estrogen-Independent Metastatic Tumors

Clin Cancer Res. 2016 Jun 1;22(11):2765-77. doi: 10.1158/1078-0432.CCR-15-1583. Epub 2016 Jan 13.

Abstract

Purpose: Acquired resistance to aromatase inhibitor (AI) therapy is a major clinical problem in the treatment of breast cancer. The detailed mechanisms of how tumor cells develop this resistance remain unclear. Here, the adapted function of estrogen receptor (ER) to an estrogen-depleted environment following AI treatment is reported.

Experimental design: Global ER chromatin immuno-precipitation (ChIP)-seq analysis of AI-resistant cells identified steroid-independent ER target genes. Matched patient tumor samples, collected before and after AI treatment, were used to assess ER activity.

Results: Maintained ER activity was observed in patient tumors following neoadjuvant AI therapy. Genome-wide ER-DNA-binding analysis in AI-resistant cell lines identified a subset of classic ligand-dependent ER target genes that develop steroid independence. The Kaplan-Meier analysis revealed a significant association between tumors, which fail to decrease this steroid-independent ER target gene set in response to neoadjuvant AI therapy, and poor disease-free survival and overall survival (n = 72 matched patient tumor samples, P = 0.00339 and 0.00155, respectively). The adaptive ER response to AI treatment was highlighted by the ER/AIB1 target gene, early growth response 3 (EGR3). Elevated levels of EGR3 were detected in endocrine-resistant local disease recurrent patient tumors in comparison with matched primary tissue. However, evidence from distant metastatic tumors demonstrates that the ER signaling network may undergo further adaptations with disease progression as estrogen-independent ER target gene expression is routinely lost in established metastatic tumors.

Conclusions: Overall, these data provide evidence of a dynamic ER response to endocrine treatment that may provide vital clues for overcoming the clinical issue of therapy resistance. Clin Cancer Res; 22(11); 2765-77. ©2016 AACR.

MeSH terms

  • Adaptor Proteins, Vesicular Transport
  • Antineoplastic Agents, Hormonal / pharmacology*
  • Antineoplastic Agents, Hormonal / therapeutic use
  • Aromatase Inhibitors / pharmacology*
  • Aromatase Inhibitors / therapeutic use
  • Brain Neoplasms / metabolism*
  • Brain Neoplasms / mortality
  • Brain Neoplasms / prevention & control
  • Brain Neoplasms / secondary
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / mortality
  • Breast Neoplasms / pathology
  • Carrier Proteins / metabolism
  • Drug Resistance, Neoplasm
  • Early Growth Response Protein 3 / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Kaplan-Meier Estimate
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / mortality
  • Liver Neoplasms / prevention & control
  • Liver Neoplasms / secondary
  • MCF-7 Cells
  • Nuclear Receptor Coactivator 3 / metabolism
  • Protein Binding
  • Receptors, Estrogen / metabolism*
  • Signal Transduction
  • Transcriptome

Substances

  • Adaptor Proteins, Vesicular Transport
  • Antineoplastic Agents, Hormonal
  • Aromatase Inhibitors
  • Carrier Proteins
  • EGR3 protein, human
  • MREG protein, human
  • Receptors, Estrogen
  • Early Growth Response Protein 3
  • NCOA3 protein, human
  • Nuclear Receptor Coactivator 3