NLRP4 negatively regulates type I interferon response and influences the outcome in anti-programmed cell death protein (PD)-1/PD-ligand 1 therapy

Cancer Sci. 2022 Mar;113(3):838-851. doi: 10.1111/cas.15243. Epub 2022 Jan 19.

Abstract

The challenge to improve the clinical efficacy and enlarge the population that benefits from immune checkpoint inhibitors (ICIs) for non-small-cell lung cancer (NSCLC) is significant. Based on whole-exosome sequencing analysis of biopsies from NSCLC patients before anti-programmed cell death protein-2 (PD-1) treatment, we identified NLRP4 mutations in the responders with a longer progression-free survival (PFS). Knockdown of NLRP4 in mouse Lewis lung cancer cell line enhanced interferon (IFN)-α/β production through the cGAS-STING-IRF3/IRF7 axis and promoted the accumulation of intratumoral CD8+ T cells, leading to tumor growth retardation in vivo and a synergistic effect with anti-PD-ligand 1 therapy. This was consistent with clinical observations that more tumor-infiltrating CD8+ T cells and elevated peripheral IFN-α before receiving nivolumab treatment were associated with a longer PFS in NSCLC patients. Our study highlights the roles of tumor-intrinsic NLRP4 in remodeling the immune contextures in the tumor microenvironment, making regional type I IFN beneficial for ICI treatment.

Keywords: NLRP4; immune checkpoint inhibitor therapy; lung cancer; tumor microenvironment; type I interferon.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • B7-H1 Antigen / antagonists & inhibitors*
  • CD8-Positive T-Lymphocytes / drug effects
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Non-Small-Cell Lung / immunology
  • Cell Line, Tumor
  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use*
  • Interferon Type I / metabolism*
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / genetics
  • Lung Neoplasms / immunology
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Macrophages / drug effects
  • Male
  • Mice
  • Middle Aged
  • Mutation
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • Progression-Free Survival
  • Signal Transduction / drug effects
  • Treatment Outcome
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Adaptor Proteins, Signal Transducing
  • B7-H1 Antigen
  • Immune Checkpoint Inhibitors
  • Interferon Type I
  • NLRP4 protein, human
  • Programmed Cell Death 1 Receptor