Epigenetic priming sensitizes gastric cancer cells to irinotecan and cisplatin by restoring multiple pathways

Gastric Cancer. 2020 Jan;23(1):105-115. doi: 10.1007/s10120-019-01010-1. Epub 2019 Sep 25.

Abstract

Background: Gastric cancer is heavily influenced by aberrant DNA methylation that alters multiple cancer-related pathways, and may respond to DNA demethylating agents, such as 5-aza-2'-deoxycytidine (5-aza-dC). Here, we aimed to analyze whether 5-aza-dC can sensitize gastric cancer cells to clinically used cytotoxic drugs.

Methods: Ten gastric cancer cell lines were treated with 5-aza-dC for 72 h and their growth was analyzed by conducting WST assay. In vivo effect of the drugs was analyzed using xenografts of OCUM-2 M/SN38 cells. Genome-wide expression and DNA methylation analyses were conducted using microarrays, and biological functions were identified through ingenuity pathway analysis.

Results: The cell lines most resistant to SN38 (an active metabolite of irinotecan), CDDP, PTX, and 5-FU, were identified. 5-Aza-dC pre-treatment of the resistant cell lines decreased the IC50 values for SN38 (TMK1, 226.4 nM to 32.91 nM; 44As3, 128.2 nM to 19.32 nM; OCUM2 M/SN38, 74.43 nM to 16.47 nM) and CDDP (TMK1, 5.05 µM to 2.26 µM; OCUM2 M, 10.79 µM to 2.77 µM), but not PTX and 5-FU. The reactivation of apoptosis-related genes, such as RUNX3, PYCARD, TNF, FAS, and FASLG, was induced by pre-treatment with 5-aza-dC, and the DNA demethylation of promoter CpG islands of RUNX3 and PYCARD was confirmed. In a xenograft model with OCUM2 M/SN38, treatment with 5-aza-dC before irinotecan showed markedly enhanced tumor suppression.

Conclusion: Epigenetic priming with 5-aza-dC can improve the sensitivity of gastric cancer cells to SN38 and CDDP.

Keywords: Cisplatin; DNA methylation; Decitabine; Irinotecan; Resistance.

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Cell Line, Tumor
  • Cisplatin / administration & dosage
  • DNA Methylation / drug effects
  • Decitabine / administration & dosage
  • Drug Resistance, Neoplasm / drug effects*
  • Drug Resistance, Neoplasm / genetics
  • Epigenesis, Genetic / drug effects*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Irinotecan / administration & dosage
  • Mice, Nude
  • Stomach Neoplasms / drug therapy*
  • Stomach Neoplasms / genetics*
  • Xenograft Model Antitumor Assays

Substances

  • Irinotecan
  • Decitabine
  • Cisplatin