Oxygen Sensing by T Cells Establishes an Immunologically Tolerant Metastatic Niche

Cell. 2016 Aug 25;166(5):1117-1131.e14. doi: 10.1016/j.cell.2016.07.032.

Abstract

Cancer cells must evade immune responses at distant sites to establish metastases. The lung is a frequent site for metastasis. We hypothesized that lung-specific immunoregulatory mechanisms create an immunologically permissive environment for tumor colonization. We found that T-cell-intrinsic expression of the oxygen-sensing prolyl-hydroxylase (PHD) proteins is required to maintain local tolerance against innocuous antigens in the lung but powerfully licenses colonization by circulating tumor cells. PHD proteins limit pulmonary type helper (Th)-1 responses, promote CD4(+)-regulatory T (Treg) cell induction, and restrain CD8(+) T cell effector function. Tumor colonization is accompanied by PHD-protein-dependent induction of pulmonary Treg cells and suppression of IFN-γ-dependent tumor clearance. T-cell-intrinsic deletion or pharmacological inhibition of PHD proteins limits tumor colonization of the lung and improves the efficacy of adoptive cell transfer immunotherapy. Collectively, PHD proteins function in T cells to coordinate distinct immunoregulatory programs within the lung that are permissive to cancer metastasis. PAPERCLIP.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • CD8-Positive T-Lymphocytes / enzymology
  • CD8-Positive T-Lymphocytes / immunology*
  • Glycolysis / immunology
  • Interferon-gamma / immunology
  • Lung / immunology*
  • Lung / pathology
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / secondary*
  • Lung Neoplasms / therapy
  • Lymphocyte Activation
  • Mice
  • Mice, Knockout
  • Neoplasm Metastasis
  • Neuropilin-1 / metabolism
  • Oxygen / metabolism*
  • Prolyl Hydroxylases / genetics
  • Prolyl Hydroxylases / metabolism*
  • T-Lymphocytes, Regulatory / enzymology
  • T-Lymphocytes, Regulatory / immunology*
  • Th1 Cells / enzymology
  • Th1 Cells / immunology

Substances

  • Neuropilin-1
  • Interferon-gamma
  • Prolyl Hydroxylases
  • Oxygen