Interleukin-23 drives expansion of Thelper 17 cells through epigenetic regulation by signal transducer and activators of transcription 3 in lupus patients.


Journal

Rheumatology (Oxford, England)
ISSN: 1462-0332
Titre abrégé: Rheumatology (Oxford)
Pays: England
ID NLM: 100883501

Informations de publication

Date de publication:
01 10 2020
Historique:
received: 24 08 2019
revised: 15 03 2020
pubmed: 7 5 2020
medline: 23 1 2021
entrez: 7 5 2020
Statut: ppublish

Résumé

To elucidate the molecular mechanisms underlying pathogenic Th17 cells, we investigated the modulation of epigenetic modifications and its association with SLE. Naive CD4+ T cells were cultured in Th17 polarizing conditions for 5 days and then treated with various cytokines, including IL-23. Expression of Th17 cell-related markers and phosphorylation of signal transducers and activators of transcription (pSTATs) were analysed using flow cytometry and quantitative PCR. Histone modifications were assessed using chromatin immunoprecipitation PCR. T cell phenotypes and pSTATs were analysed in blood samples of patients with SLE (n = 28). Finally, the effects of baricitinib on memory Th17 cells were investigated in SLE patients (n = 12). Stimulation of resting Th17 cells with IL-23 promoted maturation of these cells (P < 0.0001). IL-23 induced pSTAT3, but not pSTAT4, during Th17 cell maturation (P < 0.05). IL-23-induced STAT3 directly bound the RORγT gene locus. This was accompanied by induction of the H3H4me3 permissive mark and reduction of the H3K27me3 repressive mark, leading to enhanced RORγT gene expression. IL-23-induced expansion of Th17 cells and pSTAT3 were suppressed by the addition of baricitinib in a concentration-dependent manner (P < 0.05). In memory Th17 cells from SLE patients, pSTAT3 was hypersensitized by IL-23 stimulation and inhibited by baricitinib (P < 0.05). The results of this study indicate that IL-23/STAT3 signalling plays a fundamental role in Th17 cell maturation through transcriptional and epigenetic modifications in patients with SLE. This mechanism may underlie pathogenic Th17 cell expansion and may lead to identification of novel therapeutic targets for SLE.

Identifiants

pubmed: 32375179
pii: 5831398
doi: 10.1093/rheumatology/keaa176
doi:

Substances chimiques

Azetidines 0
Interleukin-23 0
Interleukins 0
Nuclear Receptor Subfamily 1, Group F, Member 3 0
Purines 0
Pyrazoles 0
RORC protein, human 0
STAT3 Transcription Factor 0
STAT3 protein, human 0
STAT4 Transcription Factor 0
STAT4 protein, human 0
Sulfonamides 0
Interleukin-12 187348-17-0
Jumonji Domain-Containing Histone Demethylases EC 1.14.11.-
baricitinib ISP4442I3Y
interleukin-21 MKM3CA6LT1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3058-3069

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Auteurs

Seunghyun Lee (S)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

Shingo Nakayamada (S)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

Satoshi Kubo (S)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

Kaoru Yamagata (K)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

Hiroko Yoshinari (H)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

Yoshiya Tanaka (Y)

The First Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu Japan.

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Classifications MeSH