Mitochondrial H2O2 in Lung Antigen-Presenting Cells Blocks NF-κB Activation to Prevent Unwarranted Immune Activation

Cell Rep. 2016 May 24;15(8):1700-14. doi: 10.1016/j.celrep.2016.04.060. Epub 2016 May 12.

Abstract

Inhalation of environmental antigens such as allergens does not always induce inflammation in the respiratory tract. While antigen-presenting cells (APCs), including dendritic cells and macrophages, take up inhaled antigens, the cell-intrinsic molecular mechanisms that prevent an inflammatory response during this process, such as activation of the transcription factor NF-κB, are not well understood. Here, we show that the nuclear receptor PPARγ plays a critical role in blocking NF-κB activation in response to inhaled antigens to preserve immune tolerance. Tolerance induction promoted mitochondrial respiration, generation of H2O2, and suppression of NF-κB activation in WT, but not PPARγ-deficient, APCs. Forced restoration of H2O2 in PPARγ-deficient cells suppressed IκBα degradation and NF-κB activation. Conversely, scavenging reactive oxygen species from mitochondria promoted IκBα degradation with loss of regulatory and promotion of inflammatory T cell responses in vivo. Thus, communication between PPARγ and the mitochondria maintains immune quiescence in the airways.

MeSH terms

  • Animals
  • Antigen-Presenting Cells / immunology*
  • CD11c Antigen / metabolism
  • Cell Proliferation
  • Cytokines / genetics
  • Dendritic Cells / metabolism
  • Fatty Acids / metabolism
  • Gene Expression Regulation
  • Hydrogen Peroxide / metabolism*
  • Immune Tolerance
  • Inflammation Mediators / metabolism
  • Lung / cytology*
  • Mice, Inbred C57BL
  • Mitochondria / metabolism*
  • NF-kappa B / metabolism*
  • PPAR gamma / deficiency
  • PPAR gamma / metabolism
  • Promoter Regions, Genetic / genetics
  • Reactive Oxygen Species / metabolism
  • T-Lymphocytes / cytology

Substances

  • CD11c Antigen
  • Cytokines
  • Fatty Acids
  • Inflammation Mediators
  • NF-kappa B
  • PPAR gamma
  • Reactive Oxygen Species
  • Hydrogen Peroxide