Batf3+ DCs and the 4-1BB/4-1BBL axis are required at the effector phase in the tumor microenvironment for PD-1/PD-L1 blockade efficacy

Cell Rep. 2024 May 28;43(5):114141. doi: 10.1016/j.celrep.2024.114141. Epub 2024 Apr 23.

Abstract

The cellular source of positive signals that reinvigorate T cells within the tumor microenvironment (TME) for the therapeutic efficacy of programmed death-1 (PD-1)/programmed death-ligand 1 (PD-L1) blockade has not been clearly defined. We now show that Batf3-lineage dendritic cells (DCs) are essential in this process. Flow cytometric analysis, gene-targeted mice, and blocking antibody studies revealed that 4-1BBL is a major positive co-stimulatory signal provided by these DCs within the TME that translates to CD8+ T cell functional reinvigoration and tumor regression. Immunofluorescence and spatial transcriptomics on human tumor samples revealed clustering of Batf3+ DCs and CD8+ T cells, which correlates with anti-PD-1 efficacy. In addition, proximity to Batf3+ DCs within the TME is associated with CD8+ T cell transcriptional states linked to anti-PD-1 response. Our results demonstrate that Batf3+ DCs within the TME are critical for PD-1/PD-L1 blockade efficacy and indicate a major role for the 4-1BB/4-1BB ligand (4-1BBL) axis during this process.

Keywords: 4-1BB; 4-1BBL; Batf3-lineage dendritic cells; CD8(+) T cells; CP: Cancer; CP: Immunology; DC1s; PD-1/PD-L1 blockade; immunotherapy; immunotherapy efficacy; spatial transcriptomics.

MeSH terms

  • 4-1BB Ligand / genetics
  • 4-1BB Ligand / metabolism
  • Animals
  • B7-H1 Antigen* / metabolism
  • Basic-Leucine Zipper Transcription Factors* / genetics
  • Basic-Leucine Zipper Transcription Factors* / metabolism
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Cell Line, Tumor
  • Dendritic Cells* / immunology
  • Dendritic Cells* / metabolism
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Repressor Proteins* / metabolism
  • Signal Transduction
  • Tumor Microenvironment*
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / metabolism

Substances

  • 4-1BB Ligand
  • B7-H1 Antigen
  • Basic-Leucine Zipper Transcription Factors
  • BATF3 protein, human
  • Immune Checkpoint Inhibitors
  • Programmed Cell Death 1 Receptor
  • Repressor Proteins
  • SNFT protein, mouse
  • Tumor Necrosis Factor Receptor Superfamily, Member 9