EBV-associated gastric cancer evades T-cell immunity by PD-1/PD-L1 interactions

Gastric Cancer. 2019 May;22(3):486-496. doi: 10.1007/s10120-018-0880-4. Epub 2018 Sep 28.

Abstract

Background: Epstein-Barr virus (EBV) is an oncogenic human herpesvirus involved in the development of around 10% of gastric cancers. The overexpression of PD-L1 is one of the features of EBV-associated gastric cancer (EBVaGC); however, the function of PD-L1 has not been studied in EBVaGC.

Methods: We used three EBVaGC cell lines, SNU719 cells, NCC24 cells, and YCCEL1 cells, to evaluate the PD-L1 expression and function in EBVaGC. Jurkat T-lymphocytes expressing PD-1 were co-cultured with NCC24 and YCCEL1 cells and the cell cycles were analyzed. To study the regulatory mechanism for PD-L1 expression, the 3'UTR of PD-L1 was sequenced, and the effect of inhibitors of the IFN-γ signaling pathway was evaluated.

Results: All of the EBVaGC cell lines expressed PD-L1, and its expression was further enhanced by stimulation with IFN-γ. In Jurkat T-cells co-cultured with IFN-γ-stimulated NCC24 and YCCEL1 cells, the number of cells in the G0/G1 phase was significantly increased. This G0/G1 arrest was partially released by administration of anti-PD-L1 antibody. We found SNPs in PD-L1 3'UTR nucleotide sequences that were located at seed regions for microRNAs. Treatment of EBVaGC cell lines with JAK2-inhibitor, PI3K-inhibitor, and mTOR inhibitor reduced the level of PD-L1 expression to the same level as cells without IFN-γ stimulation.

Conclusions: EBVaGC cells expressing high levels of PD-L1 suppress T-cell proliferation, and the IFN-γ signaling pathway is involved in the expression of PD-L1.

Keywords: Epstein–Barr virus (EBV); Gastric cancer; Immune checkpoint inhibitor; Lymphoid infiltration; Programmed death 1-ligand 1.

MeSH terms

  • Apoptosis
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism*
  • Cell Cycle
  • Cell Proliferation
  • Enzyme Inhibitors / pharmacology
  • Epstein-Barr Virus Infections / complications*
  • Epstein-Barr Virus Infections / virology
  • Gene Expression Regulation, Neoplastic*
  • Herpesvirus 4, Human / immunology*
  • Humans
  • Polymorphism, Single Nucleotide
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism*
  • Stomach Neoplasms / immunology*
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / pathology
  • Stomach Neoplasms / virology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Tumor Cells, Cultured

Substances

  • B7-H1 Antigen
  • CD274 protein, human
  • Enzyme Inhibitors
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor