T lymphocyte recruitment to melanoma brain tumors depends on distinct venous vessels

Immunity. 2024 Nov 12;57(11):2688-2703.e11. doi: 10.1016/j.immuni.2024.09.003. Epub 2024 Oct 4.

Abstract

To improve immunotherapy for brain tumors, it is important to determine the principal intracranial site of T cell recruitment from the bloodstream and their intracranial route to brain tumors. Using intravital microscopy in mouse models of intracranial melanoma, we discovered that circulating T cells preferably adhered and extravasated at a distinct type of venous blood vessel in the tumor vicinity, peritumoral venous vessels (PVVs). Other vascular structures were excluded as alternative T cell routes to intracranial melanomas. Anti-PD-1/CTLA-4 immune checkpoint inhibitors increased intracranial T cell motility, facilitating migration from PVVs to the tumor and subsequently inhibiting intracranial tumor growth. The endothelial adhesion molecule ICAM-1 was particularly expressed on PVVs, and, in samples of human brain metastases, ICAM-1 positivity of PVV-like vessels correlated with intratumoral T cell infiltration. These findings uncover a distinct mechanism by which the immune system can access and control brain tumors and potentially influence other brain pathologies.

Keywords: brain cancer; brain metastases; brain metastasis; cancer; immunotherapy; intravital imaging; lymphocyte recruitment; melanoma; tumor immunology.

MeSH terms

  • Animals
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Cell Line, Tumor
  • Cell Movement / immunology
  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Intercellular Adhesion Molecule-1 / metabolism
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • Melanoma* / immunology
  • Mice
  • Mice, Inbred C57BL
  • T-Lymphocytes* / immunology
  • Veins / immunology

Substances

  • Intercellular Adhesion Molecule-1
  • Immune Checkpoint Inhibitors