Impaired IL-6-induced JAK-STAT signaling in CD4+ T cells associates with longer treatment duration in giant cell arteritis

J Autoimmun. 2024 Jun:146:103215. doi: 10.1016/j.jaut.2024.103215. Epub 2024 Apr 22.

Abstract

Introduction: The IL-12-IFNγ-Th1 and the IL-6-IL-23-Th17 axes are considered the dominant pathogenic pathways in Giant Cell Arteritis (GCA). Both pathways signal via activation of the downstream JAK/STAT proteins. We hypothesized that phosphorylated STAT (pSTAT) signatures in circulating immune cells may aid to stratify GCA-patients for personalized treatment.

Methods: To investigate pSTAT expression, PBMCs from treatment-naive GCA-patients (n = 18), infection controls (INF, n = 11) and age-matched healthy controls (HC, n = 15) were stimulated in vitro with IL-6, IL-2, IL-10, IFN-γ, M-CSF or GM-CSF, and stained with CD3, CD4, CD19, CD45RO, pSTAT1, pSTAT3, pSTAT5 antibodies, and analyzed by flow cytometry. Serum IL-6, sIL-6-receptor and gp130 were measured by Luminex. The change in percentages of pSTAT3+CD4+T-cells was evaluated at diagnosis and at 3 months and 1-year of follow-up. Kaplan-Meier analyses was used to asses prognostic accuracy.

Results: Analysis of IL-6 stimulated immune cell subsets revealed a significant decrease in percentages of pSTAT3+CD4+T-cells of GCA-patients and INF-controls compared to HCs. Following patient stratification according to high (median>1.5 pg/mL) and low (median<1.5 pg/mL) IL-6 levels, we observed a reduction in the pSTAT3 response in GCA-patients with high serum IL-6. Percentages of pSTAT3+CD4+T-cells in patients with high serum IL-6 levels at diagnosis normalized after glucocorticoid (GC) treatment. Importantly, we found that patients with low percentages of pSTAT3+CD4+T-cells at baseline require longer GC-treatment.

Conclusion: Overall, in GCA, the percentages of in vitro IL-6-induced pSTAT3+CD4+T-cells likely reflect prior in vivo exposure to high IL-6 and may serve as a prognostic marker for GC-treatment duration and may assist improving personalized treatment options in the future.

Keywords: Biomarkers; Giant cell arteritis; JAK/STAT pathway; Tocilizumab.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Biomarkers
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Cytokine Receptor gp130 / metabolism
  • Female
  • Giant Cell Arteritis* / diagnosis
  • Giant Cell Arteritis* / drug therapy
  • Giant Cell Arteritis* / immunology
  • Giant Cell Arteritis* / metabolism
  • Humans
  • Interleukin-6* / blood
  • Interleukin-6* / metabolism
  • Janus Kinases / metabolism
  • Male
  • Middle Aged
  • Phosphorylation
  • Receptors, Interleukin-6 / metabolism
  • STAT Transcription Factors / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction*

Substances

  • Interleukin-6
  • Janus Kinases
  • STAT3 Transcription Factor
  • STAT Transcription Factors
  • IL6 protein, human
  • Receptors, Interleukin-6
  • Biomarkers
  • Cytokine Receptor gp130