Claudin-18 deficiency is associated with airway epithelial barrier dysfunction and asthma

J Allergy Clin Immunol. 2017 Jan;139(1):72-81.e1. doi: 10.1016/j.jaci.2016.02.035. Epub 2016 Apr 20.

Abstract

Background: Epithelial barrier dysfunction and increased permeability may contribute to antigen sensitization and disease progression in asthma. Claudin-18.1 is the only known lung-specific tight junction protein, but its contribution to airway barrier function or asthma is unclear.

Objectives: We sought to test the hypotheses that claudin-18 is a determinant of airway epithelial barrier function that is downregulated by IL-13 and that claudin-18 deficiency results in increased aeroantigen sensitization and airway hyperresponsiveness.

Methods: Claudin-18.1 mRNA levels were measured in airway epithelial brushings from healthy controls and patients with asthma. In patients with asthma, claudin-18 levels were compared with a three-gene-mean marker of TH2 inflammation. Airway epithelial permeability changes due to claudin-18 deficiency were measured in 16HBE cells and claudin-18 null mice. The effect of IL-13 on claudin expression was determined in primary human airway epithelial cells and in mice. Airway hyperresponsiveness and serum IgE levels were compared in claudin-18 null and wild-type mice following aspergillus sensitization.

Results: Epithelial brushings from patients with asthma (n = 67) had significantly lower claudin-18 mRNA levels than did those from healthy controls (n = 42). Claudin-18 levels were lowest among TH2-high patients with asthma. Loss of claudin-18 was sufficient to impair epithelial barrier function in 16HBE cells and in mouse airways. IL-13 decreased claudin-18 expression in primary human cells and in mice. Claudin-18 null mice had significantly higher serum IgE levels and increased airway responsiveness following intranasal aspergillus sensitization.

Conclusions: These data support the hypothesis that claudin-18 is an essential contributor to the airway epithelial barrier to aeroantigens. Furthermore, TH2 inflammation suppresses claudin-18 expression, potentially promoting sensitization and airway hyperresponsiveness.

Keywords: Asthma; airway hyperresponsiveness; antigen sensitization; epithelial barrier function; epithelium; tight junction.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Antigens, Fungal / immunology
  • Arylsulfonates / metabolism
  • Aspergillus / immunology
  • Asthma / blood
  • Asthma / metabolism*
  • Asthma / pathology
  • Asthma / physiopathology
  • Cell Line
  • Cells, Cultured
  • Claudins / deficiency
  • Claudins / genetics
  • Claudins / metabolism*
  • Humans
  • Immunoglobulin E / blood
  • Interleukin-13 / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Permeability
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • Respiratory Mucosa / metabolism*
  • Respiratory System / cytology
  • Respiratory System / metabolism*
  • Respiratory System / pathology
  • Respiratory System / physiopathology
  • Young Adult

Substances

  • Antigens, Fungal
  • Arylsulfonates
  • CLDN18 protein, human
  • Claudins
  • Cldn18 protein, mouse
  • Interleukin-13
  • RNA, Messenger
  • RNA, Small Interfering
  • Immunoglobulin E
  • pyranine