IL-27 and type 2 immunity in asthmatic patients: association with severity, CXCL9, and signal transducer and activator of transcription signaling

J Allergy Clin Immunol. 2015 Feb;135(2):386-94. doi: 10.1016/j.jaci.2014.08.023. Epub 2014 Oct 11.

Abstract

Background: Severe asthma (SA) can involve both innate and type 2 cytokine-associated adaptive immunity. Although IL-27 has been reported to potentiate TH1 responses (including the chemokine CXCL9) and suppress TH2 responses, its function in asthmatic patients is unknown.

Objective: We sought to evaluate IL-27 expression in human asthma alone and in combination with type 2 immunity to determine the relationship to disease severity and CXCL9 expression. We also sought to model these interactions in vitro in human bronchial epithelial cells.

Methods: Bronchoalveolar lavage cells from 87 participants were evaluated for IL-27 mRNA and protein alone and in association with epithelial CCL26 (a marker of type 2 activation) in relation to asthma severity and CXCL9 mRNA. Human bronchial epithelial cells cultured at the air-liquid interface and stimulated with IL-27 (1-100 ng/mL) with or without IL-13 (1 ng/mL) were evaluated for CXCL9 expression by using quantitative real-time PCR and ELISA. Phosphorylated and total signal transducer and activator of transcription (STAT) 1/3 were detected by means of Western blotting. Small interfering RNA knockdown of STAT1 or STAT3 was performed.

Results: Bronchoalveolar lavage cell IL-27 mRNA and protein levels were increased in asthmatic patients. Patients with evidence for type 2 pathway activation had higher IL-27 expression (P = .02). Combined IL-27 and CCL26 expression associated with more SA and higher CXCL9 expression (P = .004 and P = .007 respectively), whereas IL-27 alone was associated with milder disease. In vitro IL-13 augmented IL-27-induced CXCL9 expression, which appeared to be due to augmented STAT1 activation and reduced STAT3 activation.

Conclusions: IL-27, in combination with a type 2/CCL26 signature, identifies a more SA phenotype, perhaps through combined effects of IL-27 and IL-13 on STAT signaling. Understanding these interactions could lead to new targets for asthma therapy.

Keywords: Asthma; CXCL9; IL-13; IL-27; epithelial cells; signal transducer and activator of transcription 1; signal transducer and activator of transcription 3.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Asthma / diagnosis
  • Asthma / genetics
  • Asthma / immunology*
  • Asthma / metabolism*
  • Biomarkers / metabolism
  • Bronchoalveolar Lavage Fluid / cytology
  • Bronchoalveolar Lavage Fluid / immunology
  • Chemokine CCL26
  • Chemokine CXCL9 / metabolism
  • Chemokines, CC / genetics
  • Chemokines, CC / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Female
  • Forced Expiratory Volume
  • Gene Expression
  • Humans
  • Immunity*
  • Immunoglobulin E / blood
  • Immunoglobulin E / immunology
  • Interleukin-27 / genetics
  • Interleukin-27 / metabolism*
  • Male
  • Middle Aged
  • Nitric Oxide
  • Respiratory Mucosa / immunology
  • Respiratory Mucosa / metabolism
  • STAT Transcription Factors / metabolism
  • Severity of Illness Index
  • Signal Transduction
  • Young Adult

Substances

  • Biomarkers
  • CCL26 protein, human
  • Chemokine CCL26
  • Chemokine CXCL9
  • Chemokines, CC
  • Cytokines
  • Interleukin-27
  • STAT Transcription Factors
  • Nitric Oxide
  • Immunoglobulin E