Cyclin E overexpression as a biomarker for combination treatment strategies in inflammatory breast cancer

Oncotarget. 2017 Feb 28;8(9):14897-14911. doi: 10.18632/oncotarget.14689.

Abstract

Inflammatory breast cancer (IBC) is a virulent form of breast cancer, and novel treatment strategies are urgently needed. Immunohistochemical analysis of tumors from women with a clinical diagnosis of IBC (n = 147) and those with non-IBC breast cancer (n = 2510) revealed that, whereas in non-IBC cases cytoplasmic cyclin E was highly correlated with poor prognosis (P < 0.001), in IBC cases both nuclear and cytoplasmic cyclin E were indicative of poor prognosis. These results underscored the utility of the cyclin E/CDK2 complex as a novel target for treatment. Because IBC cell lines were highly sensitive to the CDK2 inhibitors dinaciclib and meriolin 5, we developed a high-throughput survival assay (HTSA) to design novel sequential combination strategies based on the presence of cyclin E and CDK2. Using a 14-cell-line panel, we found that dinaciclib potentiated the activity of DNA-damaging chemotherapies treated in a sequence of dinaciclib followed by chemotherapy, whereas this was not true for paclitaxel. We also identified a signature of DNA repair-related genes that are downregulated by dinaciclib, suggesting that global DNA repair is inhibited and that prolonged DNA damage leads to apoptosis. Taken together, our findings argue that CDK2-targeted combinations may be viable strategies in IBC worthy of future clinical investigation.

Keywords: CDK2; cell cycle; cyclin E; inflammatory breast cancer; treatment.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Apoptosis
  • Biomarkers, Tumor / metabolism*
  • Bridged Bicyclo Compounds, Heterocyclic / therapeutic use
  • Cell Cycle
  • Cell Proliferation
  • Combined Modality Therapy
  • Cyclic N-Oxides
  • Cyclin E / metabolism*
  • Cyclin-Dependent Kinase 2 / antagonists & inhibitors
  • Cyclin-Dependent Kinase 2 / metabolism*
  • Female
  • Follow-Up Studies
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Indolizines
  • Inflammatory Breast Neoplasms / metabolism
  • Inflammatory Breast Neoplasms / pathology*
  • Inflammatory Breast Neoplasms / therapy
  • Middle Aged
  • Neoplasm Grading
  • Neoplasm Invasiveness
  • Neoplasm Staging
  • Oncogene Proteins / metabolism*
  • Prognosis
  • Pyridinium Compounds / therapeutic use
  • Survival Rate
  • Tumor Cells, Cultured
  • Young Adult

Substances

  • Biomarkers, Tumor
  • Bridged Bicyclo Compounds, Heterocyclic
  • CCNE1 protein, human
  • Cyclic N-Oxides
  • Cyclin E
  • Indolizines
  • Oncogene Proteins
  • Pyridinium Compounds
  • dinaciclib
  • CDK2 protein, human
  • Cyclin-Dependent Kinase 2