Variability of Primary Sjögren's Syndrome Is Driven by Interferon-α and Interferon-α Blood Levels Are Associated With the Class II HLA-DQ Locus.


Journal

Arthritis & rheumatology (Hoboken, N.J.)
ISSN: 2326-5205
Titre abrégé: Arthritis Rheumatol
Pays: United States
ID NLM: 101623795

Informations de publication

Date de publication:
12 2022
Historique:
revised: 03 05 2022
received: 25 08 2021
accepted: 10 06 2022
pubmed: 22 6 2022
medline: 17 12 2022
entrez: 21 6 2022
Statut: ppublish

Résumé

Primary Sjögren's syndrome (SS) is the second most frequent systemic autoimmune disease, affecting 0.1% of the general population. To characterize the molecular and clinical variabilities among patients with primary SS, we integrated transcriptomic, proteomic, cellular, and genetic data with clinical phenotypes in a cohort of 351 patients with primary SS. We analyzed blood transcriptomes and genotypes of 351 patients with primary SS who were participants in a multicenter prospective clinical cohort. We replicated the transcriptome analysis in 3 independent cohorts (n = 462 patients). We determined circulating interferon-α (IFNα) and IFNγ protein concentrations using digital single molecular arrays (Simoa). Transcriptome analysis of the prospective cohort showed a strong IFN gene signature in more than half of the patients; this finding was replicated in the 3 independent cohorts. Because gene expression analysis did not discriminate between type I IFN and type II IFN, we used Simoa to demonstrate that the IFN transcriptomic signature was driven by circulating IFNα and not by IFNγ protein levels. IFNα protein levels, detectable in 75% of patients, were significantly associated with clinical and immunologic features of primary SS disease activity at enrollment and with increased frequency of systemic complications over the 5-year follow-up. Genetic analysis revealed a significant association between IFNα protein levels, a major histocompatibility (MHC) class II haplotype, and anti-SSA antibody. Additional cellular analysis revealed that an MHC class II HLA-DQ locus acts through up-regulation of HLA class II molecules on conventional dendritic cells. We identified the predominance of IFNα as a driver of primary SS variability, with IFNα demonstrating an association with HLA gene polymorphisms.

Identifiants

pubmed: 35726083
doi: 10.1002/art.42265
pmc: PMC10092541
doi:

Substances chimiques

Interferon-alpha 0
HLA-DQ Antigens 0

Types de publication

Multicenter Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1991-2002

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR065953
Pays : United States

Investigateurs

Emmanuelle Dernis (E)
Valerie Devauchelle-Pensec (V)
Philippe Dieude (P)
Jean-Jacques Dubost (JJ)
Anne-Laure Fauchais (AL)
Vincent Goeb (V)
Eric Hachulla (E)
Pierre Yves Hatron (PY)
Claire Larroche (C)
Véronique Le Guern (V)
Jacques Morel (J)
Aleth Perdriger (A)
Carinne Salliot (C)
Stephanie Rist (S)
Alain Saraux (A)
Jean Sibilia (J)
Olivier Vittecoq (O)
Gaétane Nocturne (G)
Philippe Ravaud (P)
Raphaèle Seror (R)
Laurent Abel (L)
Andres Alcover (A)
Hugues Aschard (H)
Kalla Astrom (K)
Philippe Bousso (P)
Pierre Bruhns (P)
Ana Cumano (A)
Caroline Demangel (C)
Ludovic Deriano (L)
James Di Santo (J)
Françoise Dromer (F)
Gérard Eberl (G)
Jost Enninga (J)
Jacques Fellay (J)
Odile Gelpi (O)
Ivo GompertsBoneca (I)
Milena Hasan (M)
Serge Hercberg (S)
Olivier Lantz (O)
Claude Leclerc (C)
Hugo Mouquet (H)
Sandra Pellegrini (S)
Stanislas Pol (S)
Antonio Rausell (A)
Lars Rogge (L)
Anavaj Sakuntabhai (A)
Olivier Schwartz (O)
Benno Schwikowski (B)
Spencer Shorte (S)
Vassili Soumelis (V)
Frédéric Tangy (F)
Eric Tartour (E)
Antoine Toubert (A)
Mathilde Touvier (M)
Marie-Noëlle Ungeheuer (MN)
Matthew L Albert (ML)
Darragh Duffy (D)
Lluis Quintana-Murci (L)

Informations de copyright

© 2022 The Authors. Arthritis & Rheumatology published by Wiley Periodicals LLC on behalf of American College of Rheumatology.

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Auteurs

Diana Trutschel (D)

Computational Systems Biomedicine Lab, Institut Pasteur, Université Paris Cité, Paris, France.

Pierre Bost (P)

Computational Systems Biomedicine Lab, Institut Pasteur, Université Paris Cité, Paris, France, Department of Quantitative Biomedicine, University of Zurich, and ETH Zurich, Institute for Molecular Health Sciences, Zurich, Switzerland.

Xavier Mariette (X)

Department of Rheumatology, Hôpital Bicêtre, Assistance Publique-Hôpitaux de Paris, Université Paris-Saclay, INSERM UMR1184-Immunology of viral infections and autoimmune diseases, Le Kremlin Bicêtre, France.

Vincent Bondet (V)

Department of Immunology, Translational Immunology Unit, Institut Pasteur, Universite Cité Paris, Paris, France.

Alba Llibre (A)

Department of Immunology, Translational Immunology Unit, Institut Pasteur, Universite Cité Paris, Paris, France.

Celine Posseme (C)

Department of Immunology, Translational Immunology Unit, Institut Pasteur, Universite Cité Paris, Paris, France.

Bruno Charbit (B)

Cytometry and Biomarkers UTechS, CRT, Institut Pasteur, Université Cite Paris, Institut Pasteur, Paris, France.

Christian W Thorball (CW)

School of Life Sciences, École Polytechnique Fédérale de Lausanne, and Precision Medicine Unit, Biomedical Data Science Center, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland.

Roland Jonsson (R)

Department of Rheumatology, Haukeland University Hospital, and Broegelmann Research Laboratory, Department of Clinical Science, University of Bergen, Bergen, Norway.

Christopher J Lessard (CJ)

Genes and Human Disease Research Program, Oklahoma Medical Research Foundation, and Department of Pathology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Renaud Felten (R)

Department of Rheumatology, Strasbourg University Hospital, National Centre For Rare Systemic Autoimmune Diseases, and Immunology, Immunopathology and Therapeutic Chemistry, Institute of Molecular and Cellular Biology, Strasbourg University, Strasbourg, France.

Wan Fai Ng (WF)

Translational and Clinical Research Institute, Newcastle University, NIHR Newcastle Biomedical Centre, and NIHR Newcastle Clinical Research Facility, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

Lucienne Chatenoud (L)

Université Paris Descartes, Sorbonne Paris Cité, INEM, CNRS UMR8253, Hôpital Necker-Enfants Malades, Paris, France.

Hélène Dumortier (H)

Immunology, Immunopathology and Therapeutic Chemistry, Institute of Molecular and Cellular Biology, Strasbourg University, Strasbourg, France.

Jean Sibilia (J)

Department of Rheumatology, Strasbourg University Hospital, National Centre For Rare Systemic Autoimmune Diseases, CNRS UPR3572, Immunology, Immunopathology and Therapeutic Chemistry, Institute of Molecular and Cellular Biology, Strasbourg University, Strasbourg, France.

Jacques Fellay (J)

School of Life Sciences, École Polytechnique Fédérale de Lausanne, and Precision Medicine Unit, Biomedical Data Science Center, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland.

Karl A Brokstad (KA)

Broegelmann Research Laboratory, Department of Clinical Science, University of Bergen, Bergen, Norway.

Silke Appel (S)

Broegelmann Research Laboratory, Department of Clinical Science, University of Bergen, Bergen, Norway.

Jessica R Tarn (JR)

Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, UK.

Lluis Quintana-Murci (L)

Department of Genomes & Genetics, Human Evolutionary Genetics, Institut Pasteur, CNRS URA3012, Paris, France.

Michael Mingueneau (M)

Multiple Sclerosis and Neurorepair Research Unit, Biogen, Cambridge, Massachusetts.

Nicolas Meyer (N)

CHU de Strasbourg, Service de Santé Publique, GMRC, Strasbourg, France, and CNRS, iCUBE, UMR7357, Illkirch, France.

Darragh Duffy (D)

Department of Immunology, Translational Immunology Unit, Institut Pasteur, Universite Cité Paris, Paris, France.

Benno Schwikowski (B)

Computational Systems Biomedicine Lab, Institut Pasteur, Université Paris Cité, Paris, France.

Jacques Eric Gottenberg (JE)

Department of Rheumatology, Strasbourg University Hospital, National Centre For Rare Systemic Autoimmune Diseases, and Immunology, Immunopathology and Therapeutic Chemistry, Institute of Molecular and Cellular Biology, Strasbourg University, Strasbourg, France.

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