EMT-like circulating tumor cells in ovarian cancer patients are enriched by platinum-based chemotherapy

Oncotarget. 2017 Jul 25;8(30):48820-48831. doi: 10.18632/oncotarget.16179.

Abstract

Background: Assuming that tumor cell dissemination requires a shift to a mesenchymal phenotype, we analyzed the incidence of epithelial-to-mesenchymal-transition (EMT)-like circulating tumor cells (CTCs) in ovarian cancer patients and inquired, how their molecular phenotypes respond to platinum-based chemotherapy and influence outcome.

Results: Before surgery, overall detection rate for epithelial CTCs was 18%. EMT-like CTCs were more frequently observed (30%) and were mutually exclusive to epithelial CTCs in the majority of patients (82%). After chemotherapy, EMT-like CTCs increased up to 52%, accompanied by the "de novo" emergence of PI3Kα+/Twist+ EMT-like CTCs. Before surgery, PI3K+ EMT-like CTCs in combination with epithelial CTCs indicated decreased OS (p = 0.02) and FIGO I-III patients with residual tumor burden after surgery were more likely to be positive for EMT-like CTCs after chemotherapy (p = 0.02). In the latter group, epithelial CTCs alone significantly correlated with decreased PFS and OS (p = 0.02, p = 0.002), supported by an additional inclusion of PI3K+ CTCs (OS, p = 0.001).

Materials and methods: Blood samples of 91 ovarian cancer patients before surgery and 31 matched samples after adjuvant chemotherapy were evaluated for CTCs with the AdnaTest ovarian cancer and EMT-1, analyzing the epithelial-associated transcripts EpCAM, Muc-1 and CA125 and the EMT-associated transcripts PI3Kα, Akt-2 and Twist.

Conclusions: Platinum-based chemotherapy seems to select for EMT-like CTCs in ovarian cancer patients and provokes a shift towards PI3Kα and Twist expressing CTCs, which may reflect clonal tumor evolution towards therapy resistance. It has to be determined, whether this CTC subgroup may serve as a biomarker to identify patients at high risk.

Keywords: Akt-2; PI3Kα; circulating tumor cells; epithelial-to-mesenchymal-transition; ovarian cancer.

MeSH terms

  • Antineoplastic Combined Chemotherapy Protocols / adverse effects
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Biomarkers, Tumor
  • Cell Count
  • Chemotherapy, Adjuvant
  • Class Ia Phosphatidylinositol 3-Kinase / metabolism
  • Epithelial-Mesenchymal Transition*
  • Female
  • Humans
  • Immunophenotyping
  • Kaplan-Meier Estimate
  • Neoplastic Cells, Circulating / pathology*
  • Ovarian Neoplasms / drug therapy
  • Ovarian Neoplasms / mortality
  • Ovarian Neoplasms / pathology*
  • Phenotype
  • Platinum / administration & dosage
  • Prognosis
  • Twist-Related Protein 1 / metabolism

Substances

  • Biomarkers, Tumor
  • Twist-Related Protein 1
  • Platinum
  • Class Ia Phosphatidylinositol 3-Kinase