Increased type 1 inflammation in gynecologic cervicovaginal samples in patients with APS-1

J Allergy Clin Immunol. 2024 Jun;153(6):1736-1742. doi: 10.1016/j.jaci.2024.02.012. Epub 2024 Feb 21.

Abstract

Background: Inborn errors of immunity offer important insights into mucosal immunity. In autoimmune polyendocrine syndrome type-1 (APS-1), chronic mucocutaneous candidiasis has been ascribed to neutralizing IL-17 autoantibodies. Recent evidence implicates excessive T-cell IFN-γ secretion and ensuing epithelial barrier disruption in predisposition to candidiasis, but these results remain to be replicated. Whether IL-17 paucity, increased type I inflammation, or their combination underlies susceptibility to chronic mucocutaneus candidiasis in APS-1 is debated.

Objective: Our aim was to characterize the immunologic features in the cervicovaginal mucosa of females with APS-1.

Methods: Vaginal fluid was collected with a flocked swab from 17 females with APS-1 and 18 controls, and cytokine composition was analyzed using Luminex (Luminex Corporation, Austin, Tex). Cervical cell samples were obtained with a cervix brush from 6 patients and 6 healthy controls and subjected to transcriptome analysis.

Results: The vaginal fluid samples from patients with APS-1 had IFN-γ concentrations comparable to those of the controls (2.6 vs 2.4 pg/mL) but high concentrations of the TH1 chemokines CXCL9 and CXCL10 (1094 vs 110 pg/mL [P < .001] and 4033 vs 273 pg/mL [P = .001], respectively), whereas the IL-17 levels in the samples from the 2 groups were comparable (28 vs 8.8 pg/mL). RNA sequencing of the cervical cells revealed upregulation of pathways related to mucosal inflammation and cell death in the patients with APS-1.

Conclusion: Excessive TH1 cell response appears to underlie disruption of the mucosal immune responses in the genital tract of patients with APS-1 and may contribute to susceptibility to candidiasis in the genital tract as well.

Keywords: AIRE; APECED; CXCL10; CXCL9; IFN-γ; IL-17; autoantibody; candidiasis; female genital tract; mucosal immunology.

MeSH terms

  • Adult
  • Candidiasis, Chronic Mucocutaneous / genetics
  • Candidiasis, Chronic Mucocutaneous / immunology
  • Cervix Uteri* / immunology
  • Cervix Uteri* / pathology
  • Chemokine CXCL9 / immunology
  • Chemokine CXCL9 / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism
  • Female
  • Humans
  • Inflammation / immunology
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Middle Aged
  • Mucous Membrane / immunology
  • Polyendocrinopathies, Autoimmune* / immunology
  • Vagina* / immunology
  • Young Adult

Substances

  • Cytokines
  • Interleukin-17
  • Chemokine CXCL9
  • Interferon-gamma