Polymerase ε (POLE) ultra-mutation in uterine tumors correlates with T lymphocyte infiltration and increased resistance to platinum-based chemotherapy in vitro

Gynecol Oncol. 2017 Jan;144(1):146-152. doi: 10.1016/j.ygyno.2016.11.023. Epub 2016 Nov 26.

Abstract

Objective: Up to 12% of all endometrial-carcinomas (EC) harbor DNA-polymerase-ε-(POLE) mutations. It is currently unknown whether the favorable prognosis of POLE-mutated EC is derived from their low metastatic capability, extraordinary number of somatic mutations thus imparting immunogenicity, or a high sensitivity to chemotherapy.

Methods: Polymerase-chain-reaction-amplification and Sanger-sequencing were used to test for POLE exonuclease-domain-mutations (exons 9-14) 131 EC. Infiltration of CD4+ and CD8+ T-lymphocytes (TIL) and PD-1-expression in POLE-mutated vs POLE wild-type EC was studied by immunohistochemistry (IHC) and the correlations between survival and molecular features were investigated. Finally, primary POLE-mutated and POLE-wild-type EC cell lines were established and compared in-vitro for their sensitivity to chemotherapy.

Results: Eleven POLE-mutated EC (8.5%) were identified. POLE-mutated tumors were associated with improved progression-free-survival (P<0.05) and displayed increased numbers of CD4+ (44.5 vs 21.8; P=0.001) and CD8+ (32.8 vs 13.5; P<0.001) TILs when compared to wild-type POLE EC. PD-1 receptor was overexpressed in TILs from POLE-mutated vs wild-type-tumors (81% vs 28%; P<0.001). Primary POLE tumor cell lines were significantly more resistant to platinum-chemotherapy in-vitro when compared to POLE-wild-type tumors (P<0.004).

Conclusions: POLE ultra-mutated EC are heavily infiltrated with CD4+/CD8+ TIL, overexpress PD-1 immune-check-point (i.e., features consistent with chronic antigen-exposure), and have a better prognosis when compared to other molecular subtypes of EC patients. POLE-mutated tumor-cell lines are resistant to platinum-chemotherapy in-vitro suggesting that the better prognosis of POLE-patients is not secondary to a higher sensitivity to chemotherapy but likely linked to enhanced immunogenicity.

Keywords: Cisplatin; Endometrial carcinoma; Polymerase ε; Uterine serous papillary cancer; Whole exome sequencing.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Antineoplastic Agents / pharmacology
  • CD4 Lymphocyte Count
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Carboplatin / pharmacology
  • Carcinoma / chemistry
  • Carcinoma / genetics*
  • Carcinoma / immunology*
  • Cell Survival / drug effects
  • DNA Polymerase II / analysis
  • DNA Polymerase II / genetics*
  • Disease-Free Survival
  • Drug Resistance, Neoplasm / genetics*
  • Endometrial Neoplasms / chemistry
  • Endometrial Neoplasms / genetics*
  • Endometrial Neoplasms / immunology*
  • Female
  • Humans
  • Microsatellite Instability
  • Middle Aged
  • Mutation
  • Poly-ADP-Ribose Binding Proteins
  • Tumor Cells, Cultured

Substances

  • Antineoplastic Agents
  • Poly-ADP-Ribose Binding Proteins
  • Carboplatin
  • DNA Polymerase II
  • POLE protein, human