Cyclin E2 overexpression is associated with endocrine resistance but not insensitivity to CDK2 inhibition in human breast cancer cells

Mol Cancer Ther. 2012 Jul;11(7):1488-99. doi: 10.1158/1535-7163.MCT-11-0963. Epub 2012 May 7.

Abstract

Cyclin E2, but not cyclin E1, is included in several gene signatures that predict disease progression in either tamoxifen-resistant or metastatic breast cancer. We therefore examined the role of cyclin E2 in antiestrogen resistance in vitro and its potential for therapeutic targeting through cyclin-dependent kinase (CDK) inhibition. High expression of CCNE2, but not CCNE1, was characteristic of the luminal B and HER2 subtypes of breast cancer and was strongly predictive of shorter distant metastasis-free survival following endocrine therapy. After antiestrogen treatment of MCF-7 breast cancer cells, cyclin E2 mRNA and protein were downregulated and cyclin E2-CDK2 activity decreased. However, this regulation was lost in tamoxifen-resistant (MCF-7 TAMR) cells, which overexpressed cyclin E2. Expression of either cyclin E1 or E2 in T-47D breast cancer cells conferred acute antiestrogen resistance, suggesting that cyclin E overexpression contributes to the antiestrogen resistance of tamoxifen-resistant cells. Ectopic expression of cyclin E1 or E2 also reduced sensitivity to CDK4, but not CDK2, inhibition. Proliferation of tamoxifen-resistant cells was inhibited by RNAi-mediated knockdown of cyclin E1, cyclin E2, or CDK2. Furthermore, CDK2 inhibition of E-cyclin overexpressing cells and tamoxifen-resistant cells restored sensitivity to tamoxifen or CDK4 inhibition. Cyclin E2 overexpression is therefore a potential mechanism of resistance to both endocrine therapy and CDK4 inhibition. CDK2 inhibitors hold promise as a component of combination therapies in endocrine-resistant disease as they effectively inhibit cyclin E1 and E2 overexpressing cells and enhance the efficacy of other therapeutics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / mortality
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cyclin E / genetics
  • Cyclin-Dependent Kinase 2 / antagonists & inhibitors*
  • Cyclins / genetics*
  • Drug Resistance, Neoplasm / genetics*
  • Estrogen Receptor Modulators / pharmacology
  • Female
  • Gene Expression Profiling
  • Gene Expression*
  • Humans
  • Neoplasm Staging
  • Oncogene Proteins / genetics
  • Protein Kinase Inhibitors / pharmacology
  • Signal Transduction / drug effects

Substances

  • CCNE1 protein, human
  • CCNE2 protein, human
  • Cyclin E
  • Cyclins
  • Estrogen Receptor Modulators
  • Oncogene Proteins
  • Protein Kinase Inhibitors
  • Cyclin-Dependent Kinase 2