ACSL6-activated IL-18R1-NF-κB promotes IL-18-mediated tumor immune evasion and tumor progression

Sci Adv. 2024 Sep 20;10(38):eadp0719. doi: 10.1126/sciadv.adp0719. Epub 2024 Sep 18.

Abstract

Aberrant activation of IL-18 signaling regulates tumor immune evasion and progression. However, the underlying mechanism remains unclear. Here, we report that long-chain acyl-CoA synthase 6 (ACSL6) is highly expressed in liver cancer and correlated with poor prognosis. ACSL6 promotes tumor growth, metastasis, and immune evasion mediated by IL-18, independent of its metabolic enzyme activity. Mechanistically, upon IL-18 stimulation, ACSL6 is phosphorylated by ERK2 at S674 and recruits IL-18RAP to interact with IL-18R1, thereby reinforcing the IL-18R1-IL-18RAP heterodimer and triggering NF-κB-dependent gene expression to facilitate tumor development. Furthermore, the up-regulation of CXCL1 and CXCL5 by ACSL6 promotes tumor-associated neutrophil and tumor-associated macrophage recruitment, thereby inhibiting cytotoxic CD8+ T cell infiltration. Ablation or S674A mutation of ACSL6 potentiated anti-PD-1 therapeutic efficacy by increasing the effector activity of intertumoral CD8+ T cells. We revealed that ACSL6 is a potential adaptor that activates IL-18-NF-κB axis-mediated tumor immune evasion and provides valuable insights for developing effective immunotherapy strategies for cancer.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Line, Tumor
  • Coenzyme A Ligases* / genetics
  • Coenzyme A Ligases* / metabolism
  • Disease Progression
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Interleukin-18* / genetics
  • Interleukin-18* / metabolism
  • Liver Neoplasms / genetics
  • Liver Neoplasms / immunology
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Mice
  • NF-kappa B* / metabolism
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Phosphorylation
  • Receptors, Interleukin-18 / genetics
  • Receptors, Interleukin-18 / metabolism
  • Signal Transduction
  • Tumor Escape / genetics

Substances

  • Coenzyme A Ligases
  • Interleukin-18
  • long-chain-fatty-acid-CoA ligase
  • NF-kappa B
  • Receptors, Interleukin-18
  • IL18 protein, human
  • IL18R1 protein, human
  • ACSL6 protein, human