Aging-induced immune microenvironment remodeling fosters melanoma in male mice via γδ17-Neutrophil-CD8 axis

Nat Commun. 2024 Dec 30;15(1):10860. doi: 10.1038/s41467-024-55164-3.

Abstract

Aging is associated with increased tumor metastasis and poor prognosis. However, how an aging immune system contributes to the process is unclear. Here, single-cell RNA sequencing reveals that in male mice, aging shifts the lung immune microenvironment towards a premetastatic niche, characterized by an increased proportion of IL-17-expressing γδT (γδ17) and neutrophils. Mechanistically, age-dependent downregulation of the immune trafficking receptor S1pr1 drives the expansion of γδ17. Compared to young mice, expanded γδ17 recruit tumor-promoting neutrophils with lower expression levels of CD62L and higher levels of C-kit and CXCR4. These neutrophils suppress the stemness and tumor-killing functions of CD8+ T cells in aged male mice. Accordingly, antibody-mediated depletion of γδT or neutrophils reduces tumor metastatic foci in aged animals, and the administration of the senolytic agent procyanidin C1 reverses the observed immune-mediated, tumor-promoting effects of aging. Thus, we uncover a γδ17-Neutrophil-CD8 axis that promotes aging-driven tumor metastasis in male mice and provides potential insights for managing metastatic tumors.

MeSH terms

  • Aging* / immunology
  • Animals
  • CD8-Positive T-Lymphocytes* / immunology
  • Cell Line, Tumor
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Intraepithelial Lymphocytes / immunology
  • Intraepithelial Lymphocytes / metabolism
  • Male
  • Melanoma / genetics
  • Melanoma / immunology
  • Melanoma / pathology
  • Mice
  • Mice, Inbred C57BL
  • Neutrophils* / immunology
  • Neutrophils* / metabolism
  • Receptors, Antigen, T-Cell, gamma-delta / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Tumor Microenvironment* / immunology

Substances

  • Interleukin-17
  • Receptors, Antigen, T-Cell, gamma-delta