Hypoxia augments MHC class I antigen presentation via facilitation of ERO1-α-mediated oxidative folding in murine tumor cells

Eur J Immunol. 2016 Dec;46(12):2842-2851. doi: 10.1002/eji.201646525. Epub 2016 Oct 18.

Abstract

To establish an effective cancer immunotherapy, it is crucial that cancer cells present a cancer-specific antigen in a hypoxic area, a hallmark of the tumor microenvironment. Here, we show the impact of hypoxia on MHC class I antigen presentation in vitro and in vivo in murine tumors. Activation of antigen-specific CTLs by tumor cells that had been pre-incubated under a condition of hypoxia was enhanced compared with that by tumor cells pre-incubated under a condition of normoxia. Cell surface expression of MHC class I-peptide complex on the tumor cells was increased under a condition of hypoxia, thereby leading to higher susceptibility to specific CTLs. We show that the hypoxia-inducible ER-resident oxidase ERO1-α plays an important role in the hypoxia-induced augmentation of MHC class I-peptide complex expression. ERO1-α facilitated oxidative folding of MHC class I heavy chains, thereby resulting in the augmentation of cell surface expression of MHC class I-peptide complex under hypoxic conditions. These results suggest that since the expression of MHC class I-peptide complex is augmented in a hypoxic tumor microenvironment, strategies for inhibiting the function of regulatory T cells and myeloid-derived suppressor cells and/or immunotherapy with immune checkpoint inhibitors are promising for improving cancer immunotherapy.

Keywords: Cancer immunity; Disulfide bond; Hypoxia; MHC class I molecule; Oxidoreductase.

MeSH terms

  • Animals
  • Antigen Presentation
  • Disease Models, Animal
  • Female
  • Glycoproteins / metabolism*
  • H-2 Antigens / metabolism
  • Humans
  • Hypoxia / immunology*
  • Hypoxia / therapy
  • Immunotherapy / methods*
  • Melanoma / immunology*
  • Melanoma / therapy
  • Melanoma, Experimental
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Oxidation-Reduction
  • Oxidoreductases
  • Protein Folding
  • T-Lymphocytes, Cytotoxic / immunology*
  • T-Lymphocytes, Cytotoxic / transplantation
  • Tumor Microenvironment

Substances

  • Glycoproteins
  • H-2 Antigens
  • H-2Kb protein, mouse
  • Ero1l protein, mouse
  • Oxidoreductases