Epithelium-derived kallistatin promotes CD4+ T-cell chemotaxis to TH2-type inflammation in chronic rhinosinusitis

J Allergy Clin Immunol. 2024 Jul;154(1):120-130. doi: 10.1016/j.jaci.2024.02.013. Epub 2024 Feb 24.

Abstract

Background: The function of kallistatin in airway inflammation, particularly chronic rhinosinusitis with nasal polyps (CRSwNP), has not been elucidated.

Objective: We sought to investigate the role of kallistatin in airway inflammation.

Methods: Kallistatin and proinflammatory cytokine expression levels were detected in nasal polyps. For the in vivo studies, we constructed the kallistatin-overexpressing transgenic mice to elucidate the role of kallistatin in airway inflammation. Furthermore, the levels of plasma IgE and proinflammatory cytokines in the airways were evaluated in the kallistatin-/- rat in vivo model under a type 2 inflammatory background. Finally, the Notch signaling pathway was explored to understand the role of kallistatin in CRSwNP.

Results: We showed that the expression of kallistatin was significantly higher in nasal polyps than in the normal nasal mucosa and correlated with IL-4 expression. We also discovered that the nasal mucosa of kallistatin-overexpressing transgenic mice expressed higher levels of IL-4 expression, associating to TH2-type inflammation. Interestingly, we observed lower IL-4 levels in the nasal mucosa and lower total plasma IgE of the kallistatin-/- group treated with house dust mite allergen compared with the wild-type house dust mite group. Finally, we observed a significant increase in the expression of Jagged2 in the nasal epithelium cells transduced with adenovirus-kallistatin. This heightened expression correlated with increased secretion of IL-4, attributed to the augmented population of CD4+CD45+Notch1+ T cells. These findings collectively may contribute to the induction of TH2-type inflammation.

Conclusions: Kallistatin was demonstrated to be involved in the CRSwNP pathogenesis by enhancing the TH2 inflammation, which was found to be associated with more expression of IL-4, potentially facilitated through Jagged2-Notch1 signaling in CD4+ T cells.

Keywords: Kallistatin; Notch; T(H)2-type inflammation; chronic rhinosinusitis with nasal polyps (CRSwNP).

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes* / immunology
  • Chemotaxis, Leukocyte / immunology
  • Chronic Disease
  • Cytokines / metabolism
  • Female
  • Humans
  • Immunoglobulin E / blood
  • Immunoglobulin E / immunology
  • Inflammation / immunology
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • Nasal Mucosa* / immunology
  • Nasal Mucosa* / metabolism
  • Nasal Polyps / immunology
  • Rats
  • Rhinosinusitis* / immunology
  • Serpins* / genetics
  • Serpins* / immunology
  • Serpins* / metabolism
  • Signal Transduction
  • Th2 Cells* / immunology

Substances

  • Cytokines
  • Immunoglobulin E
  • Interleukin-4
  • kallistatin
  • Serpins