The BTLA-HVEM axis restricts CAR T cell efficacy in cancer

Nat Immunol. 2024 Jun;25(6):1020-1032. doi: 10.1038/s41590-024-01847-4. Epub 2024 Jun 3.

Abstract

The efficacy of T cell-based immunotherapies is limited by immunosuppressive pressures in the tumor microenvironment. Here we show a predominant role for the interaction between BTLA on effector T cells and HVEM (TNFRSF14) on immunosuppressive tumor microenvironment cells, namely regulatory T cells. High BTLA expression in chimeric antigen receptor (CAR) T cells correlated with poor clinical response to treatment. Therefore, we deleted BTLA in CAR T cells and show improved tumor control and persistence in models of lymphoma and solid malignancies. Mechanistically, BTLA inhibits CAR T cells via recruitment of tyrosine phosphatases SHP-1 and SHP-2, upon trans engagement with HVEM. BTLA knockout thus promotes CAR signaling and subsequently enhances effector function. Overall, these data indicate that the BTLA-HVEM axis is a crucial immune checkpoint in CAR T cell immunotherapy and warrants the use of strategies to overcome this barrier.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Humans
  • Immunotherapy, Adoptive* / methods
  • Mice
  • Mice, Knockout
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Receptors, Chimeric Antigen* / genetics
  • Receptors, Chimeric Antigen* / immunology
  • Receptors, Chimeric Antigen* / metabolism
  • Receptors, Immunologic* / genetics
  • Receptors, Immunologic* / metabolism
  • Receptors, Tumor Necrosis Factor, Member 14* / genetics
  • Receptors, Tumor Necrosis Factor, Member 14* / immunology
  • Receptors, Tumor Necrosis Factor, Member 14* / metabolism
  • Signal Transduction
  • T-Lymphocytes, Regulatory / immunology
  • Tumor Microenvironment* / immunology

Substances

  • BTLA protein, human
  • Receptors, Chimeric Antigen
  • Receptors, Immunologic
  • Receptors, Tumor Necrosis Factor, Member 14
  • TNFRSF14 protein, human
  • BTLA protein, mouse
  • Tnfrsf14 protein, mouse