PD-L1 restrains PD-1+Nrp1lo Treg cells to suppress inflammation-driven colorectal tumorigenesis

Cell Rep. 2024 Oct 22;43(10):114819. doi: 10.1016/j.celrep.2024.114819. Epub 2024 Oct 3.

Abstract

T cells function not only as an essential component of host cancer immunosurveillance but also as a regulator of colonic inflammation, a process that promotes colorectal cancer. Programmed death-ligand 1 (PD-L1) is a T cell-negative regulator, but its role in regulation of T cell functions in the context of colorectal cancer is unknown. We report that global deletion of Cd274 results in increased colonic inflammation, PD-1+ T cells, and inflammation-driven colorectal tumorigenesis in mice. Single-cell RNA sequencing (scRNA-seq) analysis revealed that PD-L1 suppresses subpopulations of programmed cell death protein 1 (PD-1)+Nrp1lo regulatory T (Treg) cells and interleukin (IL) 6+ neutrophils in colorectal tumor. Treg cells produce transforming growth factor (TGF) β to recruit IL6+ neutrophils. Neutrophils produce IL6 to inhibit activation of tumor-specific cytotoxic T lymphocytes (CTLs) and primary CTLs. Accordingly, IL6 blockade immunotherapy increases CTL activation and suppresses colon tumor growth in vivo. Our findings determine that PD-L1 restrains PD-1+Nrp1loTGFβ+ Treg cells to suppress IL6+ neutrophil tumor recruitment to sustain CTL activation to control inflammation-driven colorectal tumorigenesis.

Keywords: CP: Cancer; CP: Immunology.

MeSH terms

  • Animals
  • B7-H1 Antigen* / metabolism
  • Carcinogenesis* / immunology
  • Carcinogenesis* / pathology
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Humans
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Interleukin-6 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neuropilin-1 / metabolism
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Programmed Cell Death 1 Receptor* / metabolism
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism
  • T-Lymphocytes, Regulatory* / immunology
  • T-Lymphocytes, Regulatory* / metabolism

Substances

  • B7-H1 Antigen
  • Programmed Cell Death 1 Receptor
  • Cd274 protein, mouse
  • Neuropilin-1
  • Interleukin-6
  • Pdcd1 protein, mouse