Mechanism of glucocorticoid protection of airway smooth muscle from proasthmatic effects of long-acting beta2-adrenoceptor agonist exposure

J Allergy Clin Immunol. 2010 May;125(5):1020-7. doi: 10.1016/j.jaci.2010.02.007. Epub 2010 Apr 14.

Abstract

Background: Chronic use of long-acting beta2-adrenergic receptor agonists (LABAs), resulting in beta2-adrenergic receptor desensitization, has been associated with increased asthma morbidity. When LABAs are used in combination with inhaled glucocorticoids, however, asthma control is improved, raising the following question: Do glucocorticoids inhibit the proasthmatic mechanism that mediates altered contractility in LABA-exposed airway smooth muscle (ASM)?

Objective: This study aimed to identify the potential protective role and mechanism of action of glucocorticoids in mitigating the effects of prolonged LABA exposure on ASM constrictor and relaxation responsiveness.

Methods: Cultured human ASM cells and isolated rabbit ASM tissues were examined for induced changes in agonist-mediated cyclic adenosine monophosphate accumulation, constrictor and relaxation responsiveness, and expression of specific glucocorticoid-regulated molecules after 24-hour exposure to the LABA salmeterol in the absence and presence of dexamethasone.

Results: Salmeterol-exposed ASM exhibited impaired cyclic adenosine monophosphate and relaxation responses to isoproterenol and increased acetylcholine-induced contractility. These proasthmatic effects of prolonged LABA exposure were attributed to upregulated phosphodiesterase 4 (PDE4) activity and were ablated by pretreatment with dexamethasone. Further studies demonstrated that (1) dexamethasone suppressed activation of the mitogen-activated protein kinases extracellular signal-regulated kinases 1 and 2 (ERK1/2), which upregulate PDE4 expression in salmeterol-exposed ASM; and (2) the inhibitory actions of dexamethasone on salmeterol-induced ERK1/2 activation and resultant PDE4-mediated changes in ASM responsiveness were prevented by gene silencing or pharmacologic inhibition of dexamethasone-induced expression of mitogen-activated protein kinase phosphatase 1, an endogenous deactivator of ERK1/2 signaling.

Conclusion: Glucocorticoids prevent the adverse proasthmatic effects of prolonged LABA exposure on airway responsiveness as a result of glucocorticoid-induced upregulation of mitogen-activated protein kinase phosphatase 1, which inhibits proasthmatic ERK1/2 signaling in the LABA-exposed ASM.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adrenergic beta-Agonists / adverse effects*
  • Albuterol / adverse effects
  • Albuterol / analogs & derivatives*
  • Animals
  • Asthma / prevention & control*
  • Cells, Cultured
  • Dexamethasone / administration & dosage
  • Dexamethasone / pharmacology
  • Dexamethasone / therapeutic use*
  • Dual Specificity Phosphatase 1 / metabolism
  • Glucocorticoids / administration & dosage
  • Glucocorticoids / pharmacology
  • Glucocorticoids / therapeutic use*
  • Humans
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Muscle, Smooth / drug effects*
  • Rabbits
  • Respiratory System / drug effects*
  • Respiratory System / metabolism
  • Respiratory System / pathology
  • Salmeterol Xinafoate
  • Up-Regulation

Substances

  • Adrenergic beta-Agonists
  • Glucocorticoids
  • Salmeterol Xinafoate
  • Dexamethasone
  • Mitogen-Activated Protein Kinase 3
  • Dual Specificity Phosphatase 1
  • Albuterol