Tumor endothelial cell autophagy is a key vascular-immune checkpoint in melanoma

EMBO Mol Med. 2023 Dec 7;15(12):e18028. doi: 10.15252/emmm.202318028. Epub 2023 Nov 27.

Abstract

Tumor endothelial cells (TECs) actively repress inflammatory responses and maintain an immune-excluded tumor phenotype. However, the molecular mechanisms that sustain TEC-mediated immunosuppression remain largely elusive. Here, we show that autophagy ablation in TECs boosts antitumor immunity by supporting infiltration and effector function of T-cells, thereby restricting melanoma growth. In melanoma-bearing mice, loss of TEC autophagy leads to the transcriptional expression of an immunostimulatory/inflammatory TEC phenotype driven by heightened NF-kB and STING signaling. In line, single-cell transcriptomic datasets from melanoma patients disclose an enriched InflammatoryHigh /AutophagyLow TEC phenotype in correlation with clinical responses to immunotherapy, and responders exhibit an increased presence of inflamed vessels interfacing with infiltrating CD8+ T-cells. Mechanistically, STING-dependent immunity in TECs is not critical for the immunomodulatory effects of autophagy ablation, since NF-kB-driven inflammation remains functional in STING/ATG5 double knockout TECs. Hence, our study identifies autophagy as a principal tumor vascular anti-inflammatory mechanism dampening melanoma antitumor immunity.

Keywords: autophagy; cancer; immunotherapy; inflammation; tumor endothelial cells.

MeSH terms

  • Animals
  • Autophagy
  • CD8-Positive T-Lymphocytes
  • Endothelial Cells / metabolism
  • Humans
  • Immunotherapy
  • Melanoma* / pathology
  • Mice
  • NF-kappa B / metabolism
  • Tumor Microenvironment

Substances

  • NF-kappa B