A novel role of IL-17A in contributing to the impaired suppressive function of Tregs in psoriasis

J Dermatol Sci. 2021 Feb;101(2):84-92. doi: 10.1016/j.jdermsci.2020.09.002. Epub 2020 Sep 28.

Abstract

Background: Regulatory T cells (Tregs) are crucial in maintaining T cell homeostasis and preventing autoimmune responses. Deficiencies in the suppressive function of Tregs contribute to the pathogenesis of various autoimmune diseases, such as psoriasis. However, whether IL-17A upregulation in psoriatic patients contributes to Treg dysfunction is unknown.

Objective: To explore the effect and underlying mechanism of IL-17A on the suppressive function of Tregs and to evaluate the restoration of the suppressive function of Tregs in psoriasis during anti-IL-17A (secukinumab) treatment.

Methods: In vitro suppression assays were performed with or without the addition of IL-17A to the coculture system. The release of inhibitory cytokines, including IL-10 and TGF-β, was assessed by qRT-PCR and flow cytometry. RNA-sequencing was conducted to characterize the cellular responses of Tregs. IL-17A signaling activation was analyzed by flow cytometry and immunofluorescence. Blood samples were collected from three psoriasis patients before and after secukinumab treatment.

Results: IL-17A blocked the suppressive function of Tregs, possibly by inhibiting the release of TGF-β and promoting the production of IFN-γ. Moreover, IL-17A activated the NF-κB signaling pathway in Tregs. Inhibition of the NF-κB pathway blocked IL-17A-induced upregulation of IFN-γ without affecting the secretion of TGF-β by Tregs. Clinical treatment in psoriasis with secukinumab restored the suppressive function and increased production of TGF-β in Tregs of psoriasis.

Conclusion: Our study implies a crucial role of IL-17A in mediating the dysfunction of the Treg suppressive function in psoriasis. Secukinumab, which neutralizes IL-17A signaling, restored the suppressive function of Tregs to exert its antipsoriatic effect.

Keywords: IFN-γ; IL-17A; Psoriasis; Secukinumab; TGF-β; Tregs.

Publication types

  • Observational Study

MeSH terms

  • Adult
  • Antibodies, Monoclonal, Humanized / pharmacology
  • Antibodies, Monoclonal, Humanized / therapeutic use*
  • Coculture Techniques
  • Dermatologic Agents / pharmacology
  • Dermatologic Agents / therapeutic use*
  • Female
  • Healthy Volunteers
  • Humans
  • Injections, Subcutaneous
  • Interferon-gamma / metabolism
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / metabolism*
  • Male
  • Middle Aged
  • Nitriles / pharmacology
  • Phosphorylation / drug effects
  • Psoriasis / drug therapy
  • Psoriasis / immunology*
  • RNA-Seq
  • Recombinant Proteins / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • Sulfones / pharmacology
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Transforming Growth Factor beta / antagonists & inhibitors
  • Transforming Growth Factor beta / metabolism
  • Treatment Outcome

Substances

  • 3-(4-methylphenylsulfonyl)-2-propenenitrile
  • Antibodies, Monoclonal, Humanized
  • Dermatologic Agents
  • IFNG protein, human
  • IL17A protein, human
  • Interleukin-17
  • Nitriles
  • Recombinant Proteins
  • Sulfones
  • Transforming Growth Factor beta
  • Interferon-gamma
  • secukinumab