IL-27 maintains cytotoxic Ly6C+ γδ T cells that arise from immature precursors

EMBO J. 2024 Jul;43(14):2878-2907. doi: 10.1038/s44318-024-00133-1. Epub 2024 May 30.

Abstract

In mice, γδ-T lymphocytes that express the co-stimulatory molecule, CD27, are committed to the IFNγ-producing lineage during thymic development. In the periphery, these cells play a critical role in host defense and anti-tumor immunity. Unlike αβ-T cells that rely on MHC-presented peptides to drive their terminal differentiation, it is unclear whether MHC-unrestricted γδ-T cells undergo further functional maturation after exiting the thymus. Here, we provide evidence of phenotypic and functional diversity within peripheral IFNγ-producing γδ T cells. We found that CD27+ Ly6C- cells convert into CD27+Ly6C+ cells, and these CD27+Ly6C+ cells control cancer progression in mice, while the CD27+Ly6C- cells cannot. The gene signatures of these two subsets were highly analogous to human immature and mature γδ-T cells, indicative of conservation across species. We show that IL-27 supports the cytotoxic phenotype and function of mouse CD27+Ly6C+ cells and human Vδ2+ cells, while IL-27 is dispensable for mouse CD27+Ly6C- cell and human Vδ1+ cell functions. These data reveal increased complexity within IFNγ-producing γδ-T cells, comprising immature and terminally differentiated subsets, that offer new insights into unconventional T-cell biology.

Keywords: Cancer; Differentiation; IL-27; Innate; γδ T Cells.

MeSH terms

  • Animals
  • Antigens, Ly* / genetics
  • Antigens, Ly* / metabolism
  • Cell Differentiation / immunology
  • Humans
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Interleukin-27 / genetics
  • Interleukin-27 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Antigen, T-Cell, gamma-delta* / genetics
  • Receptors, Antigen, T-Cell, gamma-delta* / immunology
  • Receptors, Antigen, T-Cell, gamma-delta* / metabolism
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism
  • Tumor Necrosis Factor Receptor Superfamily, Member 7* / genetics
  • Tumor Necrosis Factor Receptor Superfamily, Member 7* / immunology
  • Tumor Necrosis Factor Receptor Superfamily, Member 7* / metabolism

Substances

  • Antigens, Ly
  • Tumor Necrosis Factor Receptor Superfamily, Member 7
  • Receptors, Antigen, T-Cell, gamma-delta
  • Ly-6C antigen, mouse
  • Interferon-gamma
  • Interleukin-27