Oxidative stress-induced mitochondrial dysfunction drives inflammation and airway smooth muscle remodeling in patients with chronic obstructive pulmonary disease

J Allergy Clin Immunol. 2015 Sep;136(3):769-80. doi: 10.1016/j.jaci.2015.01.046. Epub 2015 Mar 29.

Abstract

Background: Inflammation and oxidative stress play critical roles in patients with chronic obstructive pulmonary disease (COPD). Mitochondrial oxidative stress might be involved in driving the oxidative stress-induced pathology.

Objective: We sought to determine the effects of oxidative stress on mitochondrial function in the pathophysiology of airway inflammation in ozone-exposed mice and human airway smooth muscle (ASM) cells.

Methods: Mice were exposed to ozone, and lung inflammation, airway hyperresponsiveness (AHR), and mitochondrial function were determined. Human ASM cells were isolated from bronchial biopsy specimens from healthy subjects, smokers, and patients with COPD. Inflammation and mitochondrial function in mice and human ASM cells were measured with and without the presence of the mitochondria-targeted antioxidant MitoQ.

Results: Mice exposed to ozone, a source of oxidative stress, had lung inflammation and AHR associated with mitochondrial dysfunction and reflected by decreased mitochondrial membrane potential (ΔΨm), increased mitochondrial oxidative stress, and reduced mitochondrial complex I, III, and V expression. Reversal of mitochondrial dysfunction by the mitochondria-targeted antioxidant MitoQ reduced inflammation and AHR. ASM cells from patients with COPD have reduced ΔΨm, adenosine triphosphate content, complex expression, basal and maximum respiration levels, and respiratory reserve capacity compared with those from healthy control subjects, whereas mitochondrial reactive oxygen species (ROS) levels were increased. Healthy smokers were intermediate between healthy nonsmokers and patients with COPD. Hydrogen peroxide induced mitochondrial dysfunction in ASM cells from healthy subjects. MitoQ and Tiron inhibited TGF-β-induced ASM cell proliferation and CXCL8 release.

Conclusions: Mitochondrial dysfunction in patients with COPD is associated with excessive mitochondrial ROS levels, which contribute to enhanced inflammation and cell hyperproliferation. Targeting mitochondrial ROS represents a promising therapeutic approach in patients with COPD.

Keywords: MitoQ; Ozone; airway hyperresponsiveness; airway smooth muscle; antioxidant; chronic obstructive pulmonary disease; inflammation; mitochondria; oxidative stress; proliferation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Airway Remodeling / genetics
  • Animals
  • Antioxidants / pharmacology*
  • Bronchial Hyperreactivity / chemically induced
  • Bronchial Hyperreactivity / drug therapy
  • Bronchial Hyperreactivity / genetics
  • Bronchial Hyperreactivity / pathology
  • Electron Transport Chain Complex Proteins / genetics
  • Electron Transport Chain Complex Proteins / metabolism
  • Female
  • Gene Expression Regulation
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Middle Aged
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Muscle, Smooth / drug effects
  • Muscle, Smooth / metabolism*
  • Muscle, Smooth / pathology
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Organophosphorus Compounds / pharmacology*
  • Oxidative Stress / drug effects
  • Ozone
  • Pneumonia / chemically induced
  • Pneumonia / drug therapy
  • Pneumonia / genetics
  • Pneumonia / pathology
  • Pulmonary Disease, Chronic Obstructive / chemically induced
  • Pulmonary Disease, Chronic Obstructive / genetics
  • Pulmonary Disease, Chronic Obstructive / metabolism*
  • Pulmonary Disease, Chronic Obstructive / pathology
  • Reactive Oxygen Species / antagonists & inhibitors
  • Reactive Oxygen Species / metabolism
  • Respiratory System / drug effects
  • Respiratory System / metabolism*
  • Respiratory System / pathology
  • Signal Transduction
  • Smoking / metabolism
  • Smoking / physiopathology
  • Ubiquinone / analogs & derivatives*
  • Ubiquinone / pharmacology

Substances

  • Antioxidants
  • Electron Transport Chain Complex Proteins
  • Organophosphorus Compounds
  • Reactive Oxygen Species
  • Ubiquinone
  • mitoquinone
  • Ozone
  • Hydrogen Peroxide