MiR-21 Participates in the PD-1/PD-L1 Pathway-Mediated Imbalance of Th17/Treg Cells in Patients After Gastric Cancer Resection

Ann Surg Oncol. 2019 Mar;26(3):884-893. doi: 10.1245/s10434-018-07117-6. Epub 2018 Dec 18.

Abstract

Background: The programmed cell death-1/programmed cell death-ligand 1 (PD-1/PD-L1) pathway has been shown to be involved in trauma-induced immunosuppression and to influence CD4+ T cell differentiation. MicroRNA (miR)-21 is a critical player in immune responses. However, it remains largely unknown whether miR-21 is regulated by PD-1 and influences CD4+ T-cell lineage choice after gastric cancer resection.

Methods: In the present study, we analyzed the percentages of T-helper (Th)-17/regulatory T (Treg) cells and PD-1/PD-L1 expression on peripheral blood mononuclear cells (PBMCs) during the perioperative period. We also detected the secretion of interleukin (IL)-17 and transforming growth factor (TGF)-β1 using enzyme-linked immunosorbent assays (ELISAs). Furthermore, PBMCs isolated from patients were transfected with or without adenovirus-short hairpin-PD-1 (Ad-sh-PD1), pre-miR-21 or adenovirus-green fluorescent protein (Ad-GFP), and the percentages of Th17/Treg cells and related transcription factors were measured.

Results: In patients who underwent gastric cancer resection, the number of Th17 cells decreased, whereas the number of Treg cells increased, accompanied by an increased expression of PD-1/PD-L1. In addition, the expression of RORγt and IL-17 decreased, whereas the expression of Foxp3 and TGF-β1 increased. In vitro, silencing PD-1 via Ad-sh-PD1 promoted the expression of miR-21 and increased the percentage of Th17 cells, but decreased the percentage of Treg cells. The overexpression of miR-21 increased the percentage of Th17 cells but decreased the percentage of Treg cells.

Conclusions: Our study demonstrated that gastric cancer resection altered the balance of Th17/Treg cells and increased PD-1/PD-L1 expression. In the in vitro experiments, the transfection of Ad-sh-PD1 ameliorated Th17/Treg cell imbalance partially by increasing the expression of miR-21.

MeSH terms

  • B7-H1 Antigen / metabolism*
  • Biomarkers, Tumor / metabolism
  • Female
  • Follow-Up Studies
  • Gastrectomy / mortality*
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Interleukin-17 / metabolism
  • Male
  • MicroRNAs / genetics*
  • Middle Aged
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • Prognosis
  • Programmed Cell Death 1 Receptor / metabolism*
  • Signal Transduction
  • Stomach Neoplasms / immunology*
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / pathology
  • Stomach Neoplasms / surgery
  • Survival Rate
  • T-Lymphocytes, Regulatory / immunology*
  • Th17 Cells / immunology*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • B7-H1 Antigen
  • Biomarkers, Tumor
  • CD274 protein, human
  • IL17A protein, human
  • Interleukin-17
  • MIRN21 microRNA, human
  • MicroRNAs
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • TGFB1 protein, human
  • Transforming Growth Factor beta1