ICOS+ Foxp3+ TILs in gastric cancer are prognostic markers and effector regulatory T cells associated with Helicobacter pylori

Int J Cancer. 2017 Feb 1;140(3):686-695. doi: 10.1002/ijc.30475. Epub 2016 Oct 27.

Abstract

Regulatory T cells (Tregs) have an immunosuppressive role in the tumor microenvironment. Since effector Tregs (eTregs), which have highly suppressive functions, are located in a subpopulation of Foxp3+ CD4+ Tregs, the TCR-inducible costimulatory receptor (ICOS) was applied as a marker of eTregs that infiltrated gastric cancer tissue and the induction pathway of ICOS+ Foxp3+ cells was analyzed by flow cytometry and immunohistochemistry. In tumor-infiltrating lymphocytes (TILs), ICOS+ Foxp3+ CD4+ T cells were abundantly observed in the late stages of gastric cancer. ICOS+ CD4+ TILs exhibited the ability to produce IL-10, but not IFN-γ, TNF, or IL-17 and also to suppress the proliferation of CFSE-labeled responder CD8+ T cells. With the agonistic ICOS-L protein (rICOS-L Ig), ICOS+ Foxp3+ cells were efficiently induced from naive CD4+ T cells under a stimulation with TGF-β and CD3/CD28 mAbs. Furthermore, when A*0201 PBMCs were cultured with the CMV or Melan-A antigenic peptide and rICOS-L Ig, the induction of CMV or Melan-A tetramer-binding CD8+ T cells, respectively, was inhibited. The expression of ICOS in Foxp3+ cells was closely related to plasmacytoid dendritic cells (pDCs) and their expression of ICOS-L and TLR9 as well as Helicobacter pylori infection. Collectively, our results demonstrate the potential of ICOS as a promising target for direct Treg-targeting therapeutic agents for gastric cancer, and that of eradicating therapy for H. pylori as an indirect immune therapy for gastric cancer.

Keywords: Foxp3; ICOS ligand; TIL; TLR9; pDC.

MeSH terms

  • Biomarkers, Tumor / immunology*
  • CD28 Antigens / immunology
  • CD28 Antigens / metabolism
  • CD3 Complex / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Dendritic Cells / pathology
  • Forkhead Transcription Factors / metabolism*
  • Helicobacter Infections / immunology
  • Helicobacter Infections / metabolism
  • Helicobacter Infections / pathology
  • Helicobacter pylori / immunology*
  • Humans
  • Inducible T-Cell Co-Stimulator Protein / metabolism*
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Interleukin-17 / metabolism
  • Lymphocyte Activation / immunology
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Lymphocytes, Tumor-Infiltrating / pathology
  • Prognosis
  • Stomach Neoplasms / immunology*
  • Stomach Neoplasms / pathology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Transforming Growth Factor beta / metabolism

Substances

  • Biomarkers, Tumor
  • CD28 Antigens
  • CD3 Complex
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • ICOS protein, human
  • Inducible T-Cell Co-Stimulator Protein
  • Interleukin-17
  • Transforming Growth Factor beta
  • Interleukin-10
  • Interferon-gamma