Differential regulation of IL-17A and IL-17F via STAT5 contributes to psoriatic disease

J Allergy Clin Immunol. 2023 Sep;152(3):783-798. doi: 10.1016/j.jaci.2023.03.035. Epub 2023 May 25.

Abstract

Background: IL-17A plays a pivotal pathogenic role in several immune-mediated inflammatory diseases. Despite sharing 50% sequence homology with IL-17A, the role of IL-17F remains less clear. Clinical findings suggest that dual inhibition of IL-17A and IL-17F in psoriatic disease is more efficacious than IL-17A inhibition alone, positing a pathogenic role for IL-17F.

Objective: We characterized the regulation of IL-17A and IL-17F in psoriatic disease.

Methods: Using both in vitro systems and lesional skin tissue from patients, we interrogated the chromosomal, transcriptional, and protein expression landscape of IL-17A+ and IL-17F+ TH17 cells. Alongside established assays such as single-cell RNA sequencing, we developed a novel cytokine-capture technique that was combined with chromatin immunoprecipitation sequencing and RNA sequencing.

Results: We confirm a preferential elevation of IL-17F over IL-17A in psoriatic disease and show that expression of each isoform predominantly occurs in distinct cell populations. The expression of both IL-17A and IL-17F exhibited a high degree of plasticity, with the balance between the 2 isoforms influenced by proinflammatory signaling and by anti-inflammatory drugs such as methylprednisolone. This plasticity was reflected in a broad H3K4me3 region at the IL17A-F locus, while opposing effects of STAT5/IL-2 signaling were observed for each of the 2 genes. Functionally, higher IL17F expression was linked to greater cell proliferation.

Conclusion: There are key differences in the regulation of IL-17A and IL-17F in psoriatic disease, leading to distinct inflammatory cell populations. As such, we propose that both IL-17A and IL-17F neutralization may be required to maximally inhibit IL-17-driven pathology.

Keywords: IL-17A; IL-17F; STAT5; autoimmunity; bimekizumab; inflammation; psoriasis; psoriatic arthritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Humans
  • Interleukin-17* / metabolism
  • STAT5 Transcription Factor* / genetics
  • STAT5 Transcription Factor* / metabolism
  • Signal Transduction

Substances

  • Interleukin-17
  • STAT5 Transcription Factor