Differentiation of IL-26+ TH17 intermediates into IL-17A producers via epithelial crosstalk in psoriasis

Anissa Fries, Fanny Saidoune, François Kuonen, Isabelle Dupanloup, Nadine Fournier, Ana Cristina Guerra de Souza, Muzlifah Haniffa, Feiyang Ma, Johann E. Gudjonsson, Lennart Roesner, Yang Li, Thomas Werfel, Curdin Conrad, Raphael Gottardo, Robert L. Modlin, Jeremy Di Domizio () and Michel Gilliet ()
Additional contact information
Anissa Fries: CHUV University Hospital and University of Lausanne (UNIL)
Fanny Saidoune: CHUV University Hospital and University of Lausanne (UNIL)
François Kuonen: CHUV University Hospital and University of Lausanne (UNIL)
Isabelle Dupanloup: Agora Cancer Research Center, Swiss Institute of Bioinformatics
Nadine Fournier: Agora Cancer Research Center, Swiss Institute of Bioinformatics
Ana Cristina Guerra de Souza: Agora Cancer Research Center, Swiss Institute of Bioinformatics
Muzlifah Haniffa: Newcastle Hospitals NHS Foundation Trust
Feiyang Ma: University of Michigan
Johann E. Gudjonsson: University of Michigan
Lennart Roesner: Hannover Medical School
Yang Li: Hannover Medical School (MHH)
Thomas Werfel: Hannover Medical School
Curdin Conrad: CHUV University Hospital and University of Lausanne (UNIL)
Raphael Gottardo: Biomedical Data Sciences Center, CHUV, UNIL, and SIB
Robert L. Modlin: University of California
Jeremy Di Domizio: CHUV University Hospital and University of Lausanne (UNIL)
Michel Gilliet: CHUV University Hospital and University of Lausanne (UNIL)

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract Interleukin (IL)-26 is a TH17 cytokine with known antimicrobial and pro-inflammatory functions. However, the precise role of IL-26 in the context of pathogenic TH17 responses is unknown. Here we identify a population of blood TH17 intermediates that produce high levels of IL-26 and differentiate into IL-17A-producing TH17 cells upon TGF-β1 exposure. By combining single cell RNA sequencing, TCR sequencing and spatial transcriptomics we show that this process occurs in psoriatic skin. In fact, IL-26+ TH17 intermediates infiltrating psoriatic skin induce TGF-β1 expression in basal keratinocytes and thereby promote their own differentiation into IL-17A-producing cells. Thus, our study identifies IL-26-producing cells as an early differentiation stage of TH17 cells that infiltrates psoriatic skin and controls its own maturation into IL17A-producing TH17 cells, via epithelial crosstalk involving paracrine production of TGF-β1.

Date: 2023
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DOI: 10.1038/s41467-023-39484-4

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