Integrative molecular profiling of autoreactive CD4 T cells in autoimmune hepatitis.


Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
12 2020
Historique:
received: 20 12 2019
revised: 25 05 2020
accepted: 27 05 2020
pubmed: 11 7 2020
medline: 12 11 2021
entrez: 11 7 2020
Statut: ppublish

Résumé

In most autoimmune disorders, crosstalk of B cells and CD4 T cells results in the accumulation of autoantibodies. In autoimmune hepatitis (AIH), the presence of anti-soluble liver antigen (SLA) autoantibodies is associated with reduced overall survival, but the associated autoreactive CD4 T cells have not yet been characterised. Herein, we isolated and deeply characterised SLA-specific CD4 T cells in patients with AIH. We used brief ex vivo restimulation with overlapping SLA peptides to isolate and phenotype circulating SLA-specific CD4 T cells, and integrative single-cell RNA-seq (scRNA-seq) to characterise their transcriptome and T-cell receptor (TCR) repertoire. Autoreactive TCRs were cloned and used to identify dominant SLA-derived epitopes. SLA-specific CD4 T cells were tracked in peripheral blood through TCR sequencing to identify their phenotypic niche. We further characterised disease-associated peripheral blood T cells by high-content flow cytometry in 42 patients with AIH and 17 controls with non-alcoholic steatohepatitis. Autoreactive SLA-specific CD4 T cells were only detected in patients with anti-SLA autoantibodies and had a memory PD-1 We provide a deep characterisation of rare circulating autoreactive CD4 T cells and identify their peripheral reservoir in AIH. We also propose a specific phenotype of autoreactive T cells related to AIH disease activity, which will be essential to track, delineate, and potentially target these pathogenic cells. One principal characteristic of autoimmune hepatitis (AIH), like for many other autoimmune diseases, is the accumulation of autoantibodies produced by B lymphocytes following their interaction with autoreactive CD4 T lymphocytes. In this study, we identified and characterised with high resolution these CD4 T cells. This will be essential to track, delineate, and potentially target them during AIH.

Sections du résumé

BACKGROUND & AIMS
In most autoimmune disorders, crosstalk of B cells and CD4 T cells results in the accumulation of autoantibodies. In autoimmune hepatitis (AIH), the presence of anti-soluble liver antigen (SLA) autoantibodies is associated with reduced overall survival, but the associated autoreactive CD4 T cells have not yet been characterised. Herein, we isolated and deeply characterised SLA-specific CD4 T cells in patients with AIH.
METHODS
We used brief ex vivo restimulation with overlapping SLA peptides to isolate and phenotype circulating SLA-specific CD4 T cells, and integrative single-cell RNA-seq (scRNA-seq) to characterise their transcriptome and T-cell receptor (TCR) repertoire. Autoreactive TCRs were cloned and used to identify dominant SLA-derived epitopes. SLA-specific CD4 T cells were tracked in peripheral blood through TCR sequencing to identify their phenotypic niche. We further characterised disease-associated peripheral blood T cells by high-content flow cytometry in 42 patients with AIH and 17 controls with non-alcoholic steatohepatitis.
RESULTS
Autoreactive SLA-specific CD4 T cells were only detected in patients with anti-SLA autoantibodies and had a memory PD-1
CONCLUSIONS
We provide a deep characterisation of rare circulating autoreactive CD4 T cells and identify their peripheral reservoir in AIH. We also propose a specific phenotype of autoreactive T cells related to AIH disease activity, which will be essential to track, delineate, and potentially target these pathogenic cells.
LAY SUMMARY
One principal characteristic of autoimmune hepatitis (AIH), like for many other autoimmune diseases, is the accumulation of autoantibodies produced by B lymphocytes following their interaction with autoreactive CD4 T lymphocytes. In this study, we identified and characterised with high resolution these CD4 T cells. This will be essential to track, delineate, and potentially target them during AIH.

Identifiants

pubmed: 32649971
pii: S0168-8278(20)30453-0
doi: 10.1016/j.jhep.2020.05.053
pii:
doi:

Substances chimiques

Autoantibodies 0
Autoantigens 0
CXCR5 protein, human 0
Epitopes, T-Lymphocyte 0
PDCD1 protein, human 0
Programmed Cell Death 1 Receptor 0
Receptors, Antigen, T-Cell 0
Receptors, CXCR5 0
Tumor Necrosis Factor Receptor Superfamily, Member 7 0
liver antigen LA-1 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1379-1390

Informations de copyright

Copyright © 2020 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflicts of interest The authors declare no conflicts of interest that pertain to this work. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Amédée Renand (A)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Iñaki Cervera-Marzal (I)

Aix Marseille Université, CNRS, Inserm, Centre d'Immunologie de Marseille-Luminy, CIML, Marseille, France.

Laurine Gil (L)

Aix Marseille Université, CNRS, Inserm, Centre d'Immunologie de Marseille-Luminy, CIML, Marseille, France.

Chuang Dong (C)

Aix Marseille Université, CNRS, Inserm, Centre d'Immunologie de Marseille-Luminy, CIML, Marseille, France.

Alexandra Garcia (A)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Erwan Kervagoret (E)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Hélène Aublé (H)

Centre d'Investigation Clinique gastro-nutrition, CHU Nantes, Nantes, France.

Sarah Habes (S)

Service Hepato-gastro-entérologie et Assistance Nutritionnelle, CHU Nantes, Nantes, France.

Caroline Chevalier (C)

Centre d'Investigation Clinique gastro-nutrition, CHU Nantes, Nantes, France.

Fabienne Vavasseur (F)

Centre d'Investigation Clinique gastro-nutrition, CHU Nantes, Nantes, France.

Béatrice Clémenceau (B)

Université de Nantes, CHU Nantes, Inserm, CRCINA, Nantes, France.

Anaïs Cardon (A)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Jean-Paul Judor (JP)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Jean-François Mosnier (JF)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France; Service Anatomie et Cytologie Pathologiques, CHU Nantes, Nantes, France.

Florence Tanné (F)

Service d'hépato gastroentérologie, CHU Cavale Blanche, Brest, France.

David-Axel Laplaud (DA)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France; Service de Neurologie et CIC 1413, CHU Nantes, Nantes, France.

Sophie Brouard (S)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France.

Jérôme Gournay (J)

Service Hepato-gastro-entérologie et Assistance Nutritionnelle, CHU Nantes, Nantes, France; Institut des Maladies de l'Appareil Digestif, IMAD, CHU Nantes, Nantes, France.

Pierre Milpied (P)

Aix Marseille Université, CNRS, Inserm, Centre d'Immunologie de Marseille-Luminy, CIML, Marseille, France.

Sophie Conchon (S)

Université de Nantes, CHU Nantes, Inserm, Centre de Recherche en Transplantation et Immunologie, UMR 1064, ITUN, Nantes, France. Electronic address: sophie.conchon@univ-nantes.fr.

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