Anti-PD-1 antibody-mediated activation of type 17 T-cells undermines checkpoint blockade therapy

Cancer Immunol Immunother. 2021 Jun;70(6):1789-1796. doi: 10.1007/s00262-020-02795-2. Epub 2020 Nov 27.

Abstract

Tumors that develop in the genetic LSL-K-rasG12D murine lung cancer model are resistant to anti-PD-1 antibody treatment. Analysis of tumor-bearing lungs from anti-PD-1-treated mice revealed an up to 2.5-fold increase in IL-17-producing T-cells, with minimal change in CD8+ T-cell activity. Neutralization of IL-17 concurrent with anti-PD-1 treatment on the other hand, resulted in robust CD8+ T-cell activation and a threefold reduction in tumor burden. Loss-of-function studies demonstrated that anti-PD-1 driven activation of CD4+ and γδTCR+ T-cells contributed to IL-17-mediated de-sensitization of CD8+ cytotoxic T-cells (CTL) to therapy; and that CTL activation was critical to tumor eradication. Importantly, post-therapy lung Th17 cell prevalence and activity prognosticated treatment efficacy. Consistent with the murine data, analysis of tumor biopsy samples from non-small cell lung cancer (NSCLC) patients revealed that pre-therapy intratumoral CD8+/RORc+ cell ratio correlated with response to immune checkpoint blockade (ICB). These findings provide the initial evidence for a new mechanism of ICB resistance in lung cancer.

Keywords: Anti-PD-1; CD4 T-cell; Checkpoint blockade resistance; IL-17; NSCLC; Th17 cell.

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology*
  • Carcinoma, Non-Small-Cell Lung / drug therapy*
  • Carcinoma, Non-Small-Cell Lung / immunology
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Drug Resistance, Neoplasm*
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / immunology
  • Lung Neoplasms / pathology
  • Lymphocyte Activation / immunology*
  • Mice
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes, Cytotoxic / immunology
  • Th17 Cells / immunology*
  • Tumor Cells, Cultured

Substances

  • Antibodies, Monoclonal
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor