Neutrophil profiling illuminates anti-tumor antigen-presenting potency

Cell. 2024 Mar 14;187(6):1422-1439.e24. doi: 10.1016/j.cell.2024.02.005. Epub 2024 Mar 5.

Abstract

Neutrophils, the most abundant and efficient defenders against pathogens, exert opposing functions across cancer types. However, given their short half-life, it remains challenging to explore how neutrophils adopt specific fates in cancer. Here, we generated and integrated single-cell neutrophil transcriptomes from 17 cancer types (225 samples from 143 patients). Neutrophils exhibited extraordinary complexity, with 10 distinct states including inflammation, angiogenesis, and antigen presentation. Notably, the antigen-presenting program was associated with favorable survival in most cancers and could be evoked by leucine metabolism and subsequent histone H3K27ac modification. These neutrophils could further invoke both (neo)antigen-specific and antigen-independent T cell responses. Neutrophil delivery or a leucine diet fine-tuned the immune balance to enhance anti-PD-1 therapy in various murine cancer models. In summary, these data not only indicate the neutrophil divergence across cancers but also suggest therapeutic opportunities such as antigen-presenting neutrophil delivery.

Keywords: antigen-presenting; immunotherapy; neoantigen; pan-cancer analysis; single-cell RNA sequencing; tumor-associated neutrophils.

MeSH terms

  • Animals
  • Antigen Presentation*
  • Antigens, Neoplasm
  • Humans
  • Leucine / metabolism
  • Mice
  • Neoplasms* / immunology
  • Neoplasms* / pathology
  • Neutrophils* / metabolism
  • Single-Cell Gene Expression Analysis
  • T-Lymphocytes

Substances

  • Antigens, Neoplasm
  • Leucine