Dual TGF-β and PD-1 blockade synergistically enhances MAGE-A3-specific CD8+ T cell response in esophageal squamous cell carcinoma

Int J Cancer. 2018 Nov 15;143(10):2561-2574. doi: 10.1002/ijc.31730. Epub 2018 Sep 21.

Abstract

PD-1 is highly expressed on tumor-infiltrated antigen-specific T cells and limit the antitumor function. Blocking of PD-1/PD-L1 signaling has shown unprecedented curative efficacies in patients with advanced cancer. However, only a limited population of patients benefited from such therapies. Our study aimed to explore biological properties, functional regulation and reversal of MAGE-A3-specific CD8+ T cells in patients with esophageal squamous cell carcinoma (ESCC). The underlying principle of deficiency and restoring MAGE-A3-specific CD8+ T cells function in tumor microenvironment (TME) was evaluated. MAGE-A3-specific CD8+ T cells could lyse HLA-A2+ /MAGE-A3+ tumor cells. Tetramer+ T cell frequency was higher in elder patients, but lower in patients with lymph node metastasis and late tumor stage (p < 0.05). CD107ahigh expression on functional T cells was an independent prognostic factor in Cox regression analysis. PD-1 was highly expressed on dysfunctional antigen-specific CD8+ T cells and tumor infiltrating T lymphocytes (p < 0.05). Myeloid-derived suppressor cells (MDSCs) derived-TGF-β mediated PD-1high expression on CD8+ T cells, which led to be resistance to PD-1/PD-L1 blockade in TME. Dual PD-1/PD-L1 and TGF-β signaling pathway blockades synergistically restored the function and antitumor ability of antigen-specific CD8+ T cells in vitro/vivo assay. The presence of functional MAGE-A3-specific CD8+ T cells had an independent prognostic impact on survival of patients with ESCC. Furthermore, MDSCs-derived TGF-β increased PD-1 expression on T cells and decreased the sensitivity to PD-1/PD-L1 blockade. Combining T cell-based therapy with dual PD-1/PD-L1 and TGF-β signaling pathway blockade could be considered a promising strategy for cancer treatment.

Keywords: MAGE-A3; TGF-β; esophageal squamous cell carcinoma; myeloid-derived suppressor cells; programmed death receptor 1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Neoplasm / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • Epitopes, T-Lymphocyte
  • Esophageal Neoplasms / blood
  • Esophageal Neoplasms / immunology
  • Esophageal Neoplasms / therapy*
  • Esophageal Squamous Cell Carcinoma / blood
  • Esophageal Squamous Cell Carcinoma / immunology
  • Esophageal Squamous Cell Carcinoma / therapy*
  • HLA-A2 Antigen / immunology
  • Humans
  • Mice
  • Neoplasm Proteins / immunology*
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • Programmed Cell Death 1 Receptor / immunology
  • Receptors, Transforming Growth Factor beta / antagonists & inhibitors
  • Transforming Growth Factor beta / antagonists & inhibitors*
  • Transforming Growth Factor beta / immunology
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, Neoplasm
  • Epitopes, T-Lymphocyte
  • HLA-A2 Antigen
  • MAGEA3 protein, human
  • Neoplasm Proteins
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Receptors, Transforming Growth Factor beta
  • Transforming Growth Factor beta