Obesity impairs apoptotic cell clearance in asthma

J Allergy Clin Immunol. 2013 Apr;131(4):1041-7, 1047.e1-3. doi: 10.1016/j.jaci.2012.09.028. Epub 2012 Nov 13.

Abstract

Background: Asthma in obese adults is typically more severe and less responsive to glucocorticoids than asthma in nonobese adults.

Objective: We sought to determine whether the clearance of apoptotic inflammatory cells (efferocytosis) by airway macrophages was associated with altered inflammation and reduced glucocorticoid sensitivity in obese asthmatic patients.

Methods: We investigated the relationship of efferocytosis by airway (induced sputum) macrophages and blood monocytes to markers of monocyte programming, in vitro glucocorticoid response, and systemic oxidative stress in a cohort of adults with persistent asthma.

Results: Efferocytosis by airway macrophages was assessed in obese (n=14) and nonobese (n=19) asthmatic patients. Efferocytosis by macrophages was 40% lower in obese than nonobese subjects, with a mean efferocytic index of 1.77 (SD, 1.07) versus 3.00 (SD, 1.25; P<.01). A similar reduction of efferocytic function was observed in blood monocytes of obese participants. In these monocytes there was also a relative decrease in expression of markers of alternative (M2) programming associated with efferocytosis, including peroxisome proliferator-activated receptor δ and CX3 chemokine receptor 1. Macrophage efferocytic index was significantly correlated with dexamethasone-induced mitogen-activated protein kinase phosphatase 1 expression (ρ=0.46, P<.02) and baseline glucocorticoid receptor α expression (ρ=0.44, P<.02) in PBMCs. Plasma 4-hydroxynonenal levels were increased in obese asthmatic patients at 0.33 ng/mL (SD, 0.15 ng/mL) versus 0.16 ng/mL (SD, 0.08 ng/mL) in nonobese patients (P=.006) and was inversely correlated with macrophage efferocytic index (ρ=-0.67, P=.02).

Conclusions: Asthma in obese adults is associated with impaired macrophage/monocyte efferocytosis. Impairment of this anti-inflammatory process is associated with altered monocyte/macrophage programming, reduced glucocorticoid responsiveness, and systemic oxidative stress.

Publication types

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

MeSH terms

  • Adult
  • Aldehydes / blood
  • Apoptosis
  • Asthma / complications
  • Asthma / drug therapy
  • Asthma / immunology
  • Asthma / pathology*
  • Biomarkers / metabolism
  • Cohort Studies
  • Dexamethasone / pharmacology
  • Dexamethasone / therapeutic use
  • Dual Specificity Phosphatase 1 / genetics
  • Dual Specificity Phosphatase 1 / immunology
  • Female
  • Gene Expression
  • Glucocorticoids / pharmacology
  • Glucocorticoids / therapeutic use
  • Humans
  • Inflammation / immunology
  • Inflammation / pathology
  • Macrophages / immunology
  • Macrophages / pathology*
  • Male
  • Middle Aged
  • Monocytes / immunology
  • Monocytes / pathology*
  • Obesity / complications
  • Obesity / drug therapy
  • Obesity / immunology
  • Obesity / pathology*
  • Oxidative Stress
  • PPAR delta / genetics
  • PPAR delta / immunology
  • Phagocytosis / drug effects
  • Phagocytosis / immunology
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / immunology
  • Receptors, Glucocorticoid / genetics
  • Receptors, Glucocorticoid / immunology
  • Sputum / cytology

Substances

  • Aldehydes
  • Biomarkers
  • Glucocorticoids
  • PPAR delta
  • Receptors, Chemokine
  • Receptors, Glucocorticoid
  • glucocorticoid receptor alpha
  • Dexamethasone
  • Dual Specificity Phosphatase 1
  • 4-hydroxy-2-nonenal