Dual role for CXCR3 and CCR5 in asthmatic type 1 inflammation

J Allergy Clin Immunol. 2022 Jan;149(1):113-124.e7. doi: 10.1016/j.jaci.2021.05.044. Epub 2021 Jun 16.

Abstract

Background: Many patients with severe asthma (SA) fail to respond to type 2 inflammation-targeted therapies. We previously identified a cohort of subjects with SA expressing type 1 inflammation manifesting with IFN-γ expression and variable type 2 responses.

Objective: We investigated the role of the chemotactic receptors C-X-C chemokine receptor 3 (CXCR3) and C-C chemokine receptor 5 (CCR5) in establishing type 1 inflammation in SA.

Methods: Bronchoalveolar lavage microarray data from the Severe Asthma Research Program I/II were analyzed for pathway expression and paired with clinical parameters. Wild-type, Cxcr3-/-, and Ccr5-/- mice were exposed to a type 1-high SA model with analysis of whole lung gene expression and histology. Wild-type and Cxcr3-/- mice were treated with a US Food and Drug Administration-approved CCR5 inhibitor (maraviroc) with assessment of airway resistance, inflammatory cell recruitment by flow cytometry, whole lung gene expression, and histology.

Results: A cohort of subjects with increased IFN-γ expression showed higher asthma severity. IFN-γ expression was correlated with CXCR3 and CCR5 expression, but in Cxcr3-/- and Ccr5-/- mice type 1 inflammation was preserved in a murine SA model, most likely owing to compensation by the other pathway. Incorporation of maraviroc into the experimental model blunted airway hyperreactivity despite only mild effects on lung inflammation.

Conclusions: IFNG expression in asthmatic airways was strongly correlated with expression of both the chemokine receptors CXCR3 and CCR5. Although these pathways provide redundancy for establishing type 1 lung inflammation, inhibition of the CCL5/CCR5 pathway with maraviroc provided unique benefits in reducing airway hyperreactivity. Targeting this pathway may be a novel approach for improving lung function in individuals with type 1-high asthma.

Keywords: CCL5; CCR5; CXCL10; CXCL9; CXCR3; IFN-γ; maraviroc; severe asthma.

Publication types

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

MeSH terms

  • Adult
  • Airway Resistance
  • Animals
  • Asthma / drug therapy
  • Asthma / immunology*
  • Asthma / physiopathology
  • Bronchi / immunology
  • Bronchoalveolar Lavage Fluid / immunology
  • CCR5 Receptor Antagonists / therapeutic use
  • Female
  • Humans
  • Inflammation / immunology
  • Inflammation / physiopathology
  • Interferon-gamma / immunology
  • Male
  • Maraviroc / therapeutic use
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Receptors, CCR5 / genetics
  • Receptors, CCR5 / immunology*
  • Receptors, CXCR3 / genetics
  • Receptors, CXCR3 / immunology*
  • Respiratory Mucosa / immunology
  • Severity of Illness Index
  • Young Adult

Substances

  • CCR5 Receptor Antagonists
  • Receptors, CCR5
  • Receptors, CXCR3
  • Interferon-gamma
  • Maraviroc