Deficiency of gp91phox inhibits allergic airway inflammation

Am J Respir Cell Mol Biol. 2013 Sep;49(3):396-402. doi: 10.1165/rcmb.2012-0442OC.

Abstract

Nicotinamide adenine dinucleotide phosphate (NADPH) oxidase, a multienzyme complex, is the major source for production of reactive oxygen species (ROS). ROS are increased in allergic diseases, such as asthma, but the role of ROS in disease pathogenesis remains uncertain. We hypothesized that mice unable to generate ROS via the NADPH oxidase pathway would have decreased allergic airway inflammation. To test this hypothesis, we studied gp91phox(-/-) mice in a model of allergic airway inflammation after sensitization and challenge with ovalbumin. Serum, bronchoalveolar lavage fluid, and lungs were then examined for evidence of allergic inflammation. We found that mice lacking a functional NADPH oxidase complex had significantly decreased ROS production and allergic airway inflammation, compared with wild-type (WT) control animals. To determine the mechanism by which allergic inflammation was inhibited by gp91phox deficiency, we cultured bone marrow-derived dendritic cells from WT and gp91phox(-/-) mice and activated them with LPS. IL-12 expression was significantly increased in the gp91phox(-/-) bone marrow-derived dendritic cells, suggesting that the cytokine profile produced in the absence of gp91phox enhanced the conditions leading to T helper (Th) type 1 differentiation, while inhibiting Th2 polarization. Splenocytes from sensitized gp91phox(-/-) animals produced significantly less IL-13 in response to ovalbumin challenge in vitro compared with splenocytes from sensitized WT mice, suggesting that NADPH oxidase promotes allergic sensitization. In contrast, inflammatory cytokines produced by T cells cultured from WT and gp91phox(-/-) mice under Th0, Th1, Th2, and Th17 conditions were not significantly different. This study demonstrates the importance of NADPH oxidase activity and ROS production in a murine model of asthma.

Publication types

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

MeSH terms

  • Animals
  • Asthma / chemically induced
  • Asthma / genetics
  • Asthma / immunology*
  • Asthma / pathology
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cells, Cultured
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / pathology
  • Female
  • Gene Deletion
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / immunology*
  • Interleukin-13 / biosynthesis
  • Interleukin-13 / immunology*
  • Lipopolysaccharides / pharmacology
  • Lung / immunology*
  • Lung / metabolism
  • Lung / pathology
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology*
  • Mice
  • Mice, Knockout
  • NADPH Oxidase 2
  • NADPH Oxidases / deficiency
  • NADPH Oxidases / genetics
  • NADPH Oxidases / immunology*
  • Ovalbumin / immunology
  • Ovalbumin / pharmacology
  • Reactive Oxygen Species / immunology*
  • Reactive Oxygen Species / metabolism
  • Th1 Cells / immunology
  • Th1 Cells / pathology
  • Th1-Th2 Balance
  • Th17 Cells / immunology
  • Th17 Cells / pathology
  • Th2 Cells / immunology
  • Th2 Cells / pathology

Substances

  • Interleukin-13
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Reactive Oxygen Species
  • Interleukin-12
  • Ovalbumin
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases