Targeting IRE1α reprograms the tumor microenvironment and enhances anti-tumor immunity in prostate cancer

Nat Commun. 2024 Oct 15;15(1):8895. doi: 10.1038/s41467-024-53039-1.

Abstract

Unfolded protein response (UPR) is a central stress response pathway that is hijacked by tumor cells for their survival. Here, we find that IRE1α signaling, one of the canonical UPR arms, is increased in prostate cancer (PCa) patient tumors. Genetic or small molecule inhibition of IRE1α in syngeneic mouse PCa models and an orthotopic model decreases tumor growth. IRE1α ablation in cancer cells potentiates interferon responses and activates immune system related pathways in the tumor microenvironment (TME). Single-cell RNA-sequencing analysis reveals that targeting IRE1α in cancer cells reduces tumor-associated macrophage abundance. Consistently, the small molecule IRE1α inhibitor MKC8866, currently in clinical trials, reprograms the TME and enhances anti-PD-1 therapy. Our findings show that IRE1α signaling not only promotes cancer cell growth and survival but also interferes with anti-tumor immunity in the TME. Thus, targeting IRE1α can be a promising approach for improving anti-PD-1 immunotherapy in PCa.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Endoribonucleases* / genetics
  • Endoribonucleases* / metabolism
  • Humans
  • Immunotherapy / methods
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / metabolism
  • Prostatic Neoplasms* / drug therapy
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / immunology
  • Prostatic Neoplasms* / pathology
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Signal Transduction
  • Tumor Microenvironment* / immunology
  • Tumor-Associated Macrophages / immunology
  • Tumor-Associated Macrophages / metabolism
  • Unfolded Protein Response* / drug effects
  • Unfolded Protein Response* / immunology

Substances

  • Protein Serine-Threonine Kinases
  • Endoribonucleases
  • ERN1 protein, human
  • Ern1 protein, mouse
  • Programmed Cell Death 1 Receptor