Rhinovirus infection causes steroid resistance in airway epithelium through nuclear factor κB and c-Jun N-terminal kinase activation

J Allergy Clin Immunol. 2013 Nov;132(5):1075-1085.e6. doi: 10.1016/j.jaci.2013.05.028. Epub 2013 Jul 18.

Abstract

Background: Although inhaled glucocorticoids are the mainstays of asthma treatment, they are poorly effective at treating and preventing virus-induced asthma exacerbations. The major viruses precipitating asthma exacerbations are rhinoviruses.

Objective: We sought to evaluate whether rhinovirus infection interferes with the mechanisms of action of glucocorticoids.

Methods: Cultured primary human bronchial or transformed (A549) respiratory epithelial cells were infected with rhinovirus 16 (RV-16) before dexamethasone exposure. Glucocorticoid receptor (GR) α nuclear translocation, glucocorticoid response element (GRE) binding, and transactivation/transrepression functional readouts were evaluated by using immunocytochemistry, Western blotting, DNA binding assays, real-time quantitative PCR, coimmunoprecipitation, and ELISA techniques. Specific inhibitors of c-Jun N-terminal kinase (JNK) and of IκB kinase (IKK) were used to investigate the involvement of intracellular signaling pathways.

Results: RV-16 infection impaired dexamethasone-dependent (1) inhibition of IL-1β-induced CXCL8 release, (2) induction of mitogen-activated protein kinase phosphatase 1 gene expression, and (3) binding of GR to GREs in airway epithelial cells. This was associated with impaired GRα nuclear translocation, as assessed by means of both immunochemistry (54.0% ± 6.8% vs 24.7% ± 3.8% GR-positive nuclei after 10 nmol/L dexamethasone treatment in sham- or RV-16-infected cells, respectively; P < .01) and Western blotting. RV-16 infection induced nuclear factor κB activation and GRα phosphorylation, which were prevented by inhibitors of IKK2 and JNK, respectively. In rhinovirus-infected cells the combination of JNK and IKK2 inhibitors totally restored dexamethasone suppression of CXCL8 release, induction of mitogen-activated protein kinase phosphatase 1 gene expression, and GRα nuclear translocation.

Conclusion: RV-16 infection of human airway epithelium induces glucocorticoid resistance. Inhibition of RV-16-induced JNK and nuclear factor κB activation fully reversed rhinovirus impairment of both GRα nuclear translocation and the transactivation/transrepression activities of glucocorticoids.

Keywords: Asthma; EC(50); Emax; GAPDH; GR; GRE; Glucocorticoid receptor; Glucocorticoid response element; Glyceraldehyde-3-phosphate dehydrogenase; HBEC; Human bronchial epithelial cell; ICAM-1; ICS; IKK; Inhaled corticosteroid; Intercellular adhesion molecule 1; IκB kinase; JNK; MKP-1; MOI; Maximal effective concentration; Median effective concentration; Mitogen-activated protein kinase phosphatase; Multiplicity of infection; NF-κB; Nuclear factor κB; RV-16; RV-1B; Rhinovirus 16; Rhinovirus type 1B; Small interfering RNA; c-Jun N-terminal kinase; glucocorticoids; kinases; siRNA; transcription factors; viral respiratory tract infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Asthma / complications
  • Asthma / drug therapy
  • Asthma / metabolism
  • Cell Line
  • Cell Nucleus
  • Dexamethasone / pharmacology
  • Dexamethasone / therapeutic use
  • Drug Resistance*
  • Enzyme Activation
  • Glucocorticoids / pharmacology
  • Glucocorticoids / therapeutic use
  • Humans
  • I-kappa B Kinase / antagonists & inhibitors
  • I-kappa B Kinase / metabolism
  • Interleukin-1beta / pharmacology
  • Interleukin-8 / biosynthesis
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • NF-kappa B / metabolism*
  • Picornaviridae Infections / complications
  • Picornaviridae Infections / metabolism*
  • Protein Transport / drug effects
  • Receptors, Glucocorticoid / metabolism
  • Respiratory Mucosa / metabolism*
  • Respiratory Mucosa / virology*
  • Rhinovirus*

Substances

  • Glucocorticoids
  • Interleukin-1beta
  • Interleukin-8
  • NF-kappa B
  • Receptors, Glucocorticoid
  • Dexamethasone
  • I-kappa B Kinase
  • JNK Mitogen-Activated Protein Kinases