Neutrophils Driving Unconventional T Cells Mediate Resistance against Murine Sarcomas and Selected Human Tumors

Cell. 2019 Jul 11;178(2):346-360.e24. doi: 10.1016/j.cell.2019.05.047. Epub 2019 Jun 27.

Abstract

Neutrophils are a component of the tumor microenvironment and have been predominantly associated with cancer progression. Using a genetic approach complemented by adoptive transfer, we found that neutrophils are essential for resistance against primary 3-methylcholantrene-induced carcinogenesis. Neutrophils were essential for the activation of an interferon-γ-dependent pathway of immune resistance, associated with polarization of a subset of CD4- CD8- unconventional αβ T cells (UTCαβ). Bulk and single-cell RNA sequencing (scRNA-seq) analyses unveiled the innate-like features and diversity of UTCαβ associated with neutrophil-dependent anti-sarcoma immunity. In selected human tumors, including undifferentiated pleomorphic sarcoma, CSF3R expression, a neutrophil signature and neutrophil infiltration were associated with a type 1 immune response and better clinical outcome. Thus, neutrophils driving UTCαβ polarization and type 1 immunity are essential for resistance against murine sarcomas and selected human tumors.

Keywords: carcinogenesis; innate immunity; interleukin-12; macrophages; neutrophils; soft tissue sarcomas; tumor immunology; unconventional T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromones / toxicity
  • Disease Resistance* / immunology
  • Humans
  • Immunity, Innate
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism
  • Interleukin-12 / genetics
  • Interleukin-12 / metabolism
  • Kaplan-Meier Estimate
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms / immunology
  • Neoplasms / mortality
  • Neoplasms / pathology*
  • Neutrophil Infiltration
  • Neutrophils / cytology
  • Neutrophils / immunology*
  • Neutrophils / metabolism
  • Receptors, Colony-Stimulating Factor / metabolism
  • Sarcoma / chemically induced
  • Sarcoma / immunology
  • Sarcoma / pathology*
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • Tumor Microenvironment

Substances

  • Chromones
  • Receptors, Colony-Stimulating Factor
  • Interleukin-12
  • Interferon-gamma
  • 3-methylchromone