Lung adenocarcinoma-related TNF-α-dependent inflammation upregulates MHC-II on alveolar type II cells through CXCR-2 to contribute to Treg expansion

FASEB J. 2020 Sep;34(9):12197-12213. doi: 10.1096/fj.202000166RR. Epub 2020 Jul 27.

Abstract

MHC-II on alveolar type-II (AT-II) cells is associated with immune tolerance in an inflammatory microenvironment. Recently, we found TNF-α upregulated MHC-II in AT-II in vitro. In this study, we explored whether TNF-α-mediated inflammation upregulates MHC-II on AT-II cells to trigger Treg expansion in inflammation-driven lung adenocarcinoma (IDLA). Using urethane-induced mice IDLA model, we found that IDLA cells mainly arise from AT-II cells, which are the major source of MHC-II. Blocking urethane-induced inflammation by TNF-α neutralization inhibited tumorigenesis and reversed MHC-II upregulation on tumor cells of AT-II cellular origin in IDLA. MHC-II-dependent AT-II cells were isolated from IDLA-induced Treg expansion. In human LA samples, we found high expression of MHC-II in tumor cells of AT-II cellular origin, which was correlated with increased Foxp3+ T cells infiltration as well as CXCR-2 expression. CXCR-2 and MHC-II colocalization was observed in inflamed lung tissue and IDLA cells of AT-II cellular origin. Furthermore, at the pro-IDLA inflammatory stage, TNF-α-neutralization or CXCR-2 deficiency inhibited the upregulation of MHC-II on AT-II cells in inflamed lung tissue. Thus, tumor cells of AT-II cellular origin contribute to Treg expansion in an MHC-II-dependent manner in TNF-α-mediated IDLA. At the pro-tumor inflammatory stage, TNF-α-dependent lung inflammation plays an important role in MHC-II upregulation on AT-II cells.

Keywords: MHC‐II; Treg; alveolar type‐II (AT‐II) cells; lung adenocarcinoma; lung inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma of Lung / immunology*
  • Alveolar Epithelial Cells / immunology*
  • Animals
  • Female
  • HLA-DR Antigens / analysis
  • Histocompatibility Antigens Class II / analysis*
  • Histocompatibility Antigens Class II / physiology
  • Humans
  • Inflammation / immunology*
  • Lung Neoplasms / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Receptors, Interleukin-8B / physiology*
  • T-Lymphocytes, Regulatory / physiology*
  • Tumor Necrosis Factor-alpha / physiology*
  • Up-Regulation

Substances

  • HLA-DR Antigens
  • Histocompatibility Antigens Class II
  • Receptors, Interleukin-8B
  • Tumor Necrosis Factor-alpha