Multi-HLA class II tetramer analyses of citrulline-reactive T cells and early treatment response in rheumatoid arthritis.


Journal

BMC immunology
ISSN: 1471-2172
Titre abrégé: BMC Immunol
Pays: England
ID NLM: 100966980

Informations de publication

Date de publication:
18 05 2020
Historique:
received: 16 08 2019
accepted: 04 05 2020
entrez: 20 5 2020
pubmed: 20 5 2020
medline: 5 6 2021
Statut: epublish

Résumé

HLA class II tetramers can be used for ex vivo enumeration and phenotypic characterisation of antigen-specific CD4+ T cells. They are increasingly applied in settings like allergy, vaccination and autoimmune diseases. Rheumatoid arthritis (RA) is a chronic autoimmune disorder for which many autoantigens have been described. Using multi-parameter flow cytometry, we developed a multi-HLA class II tetramer approach to simultaneously study several antigen specificities in RA patient samples. We focused on previously described citrullinated HLA-DRB1*04:01-restricted T cell epitopes from α-enolase, fibrinogen-β, vimentin as well as cartilage intermediate layer protein (CILP). First, we examined inter-assay variability and the sensitivity of the assay in peripheral blood from healthy donors (n = 7). Next, we confirmed the robustness and sensitivity in a cohort of RA patients with repeat blood draws (n = 14). We then applied our method in two different settings. We assessed lymphoid tissue from seropositive arthralgia (n = 5) and early RA patients (n = 5) and could demonstrate autoreactive T cells in individuals at risk of developing RA. Lastly, we studied peripheral blood from early RA patients (n = 10) and found that the group of patients achieving minimum disease activity (DAS28 < 2.6) at 6 months follow-up displayed a decrease in the frequency of citrulline-specific T cells. Our study demonstrates the development of a sensitive tetramer panel allowing simultaneous characterisation of antigen-specific T cells in ex vivo patient samples including RA 'at risk' subjects. This multi-tetramer approach can be useful for longitudinal immune-monitoring in any disease with known HLA-restriction element and several candidate antigens.

Sections du résumé

BACKGROUND
HLA class II tetramers can be used for ex vivo enumeration and phenotypic characterisation of antigen-specific CD4+ T cells. They are increasingly applied in settings like allergy, vaccination and autoimmune diseases. Rheumatoid arthritis (RA) is a chronic autoimmune disorder for which many autoantigens have been described.
RESULTS
Using multi-parameter flow cytometry, we developed a multi-HLA class II tetramer approach to simultaneously study several antigen specificities in RA patient samples. We focused on previously described citrullinated HLA-DRB1*04:01-restricted T cell epitopes from α-enolase, fibrinogen-β, vimentin as well as cartilage intermediate layer protein (CILP). First, we examined inter-assay variability and the sensitivity of the assay in peripheral blood from healthy donors (n = 7). Next, we confirmed the robustness and sensitivity in a cohort of RA patients with repeat blood draws (n = 14). We then applied our method in two different settings. We assessed lymphoid tissue from seropositive arthralgia (n = 5) and early RA patients (n = 5) and could demonstrate autoreactive T cells in individuals at risk of developing RA. Lastly, we studied peripheral blood from early RA patients (n = 10) and found that the group of patients achieving minimum disease activity (DAS28 < 2.6) at 6 months follow-up displayed a decrease in the frequency of citrulline-specific T cells.
CONCLUSIONS
Our study demonstrates the development of a sensitive tetramer panel allowing simultaneous characterisation of antigen-specific T cells in ex vivo patient samples including RA 'at risk' subjects. This multi-tetramer approach can be useful for longitudinal immune-monitoring in any disease with known HLA-restriction element and several candidate antigens.

Identifiants

pubmed: 32423478
doi: 10.1186/s12865-020-00357-w
pii: 10.1186/s12865-020-00357-w
pmc: PMC7236297
doi:

Substances chimiques

Epitopes, T-Lymphocyte 0
Extracellular Matrix Proteins 0
Histocompatibility Antigens Class II 0
Vimentin 0
Citrulline 29VT07BGDA
Fibrinogen 9001-32-5
Pyrophosphatases EC 3.6.1.-

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

27

Subventions

Organisme : Reumatikerförbundet
ID : R-481771
Pays : International
Organisme : Stiftelsen Konung Gustaf V:s 80-årsfond
ID : FAI-2016-0312
Pays : International
Organisme : Stiftelsen Konung Gustaf V:s 80-årsfond
ID : FAI-2016-0312
Pays : International
Organisme : Vetenskapsrådet
ID : 2015-02900
Pays : International
Organisme : Innovative Medicines Initiative
ID : BTCure 115142
Pays : International
Organisme : Innovative Medicines Initiative
ID : RTCure 777357
Pays : International
Organisme : Innovative Medicines Initiative
ID : BTCure 115142
Pays : International
Organisme : FP7 Health
ID : FP7-HEALTH-F2-2012-305549
Pays : International
Organisme : ReumaNederland
ID : 11-1-308
Pays : International
Organisme : ReumaNederland
ID : 14-2-403
Pays : International
Organisme : Margareta af Ugglas Foundation
ID : not applicable
Pays : International

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Auteurs

Christina Gerstner (C)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Sara Turcinov (S)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Aase H Hensvold (AH)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Karine Chemin (K)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Hannes Uchtenhagen (H)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.
Translational Research Program, BRI at Virginia Mason, Seattle, (WA), USA.

Tamara H Ramwadhdoebe (TH)

Department of Clinical Immunology and Rheumatology and Department of Experimental Immunology, Amsterdam UMC, University of Amsterdam, Amsterdam Infection & Immunity Institute, Amsterdam, Netherlands.
Amsterdam Rheumatology & Immunology Center (ARC), Academic Medical Center, Amsterdam, Netherlands.

Anatoly Dubnovitsky (A)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Genadiy Kozhukh (G)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Lars Rönnblom (L)

Department of Medical Sciences, Rheumatology, Science for Life Laboratory, Uppsala, Sweden.

William W Kwok (WW)

Translational Research Program, BRI at Virginia Mason, Seattle, (WA), USA.

Adnane Achour (A)

Science for Life Laboratory, Department of Medicine Solna, Karolinska Institutet & Division of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.

Anca I Catrina (AI)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.

Lisa G M van Baarsen (LGM)

Department of Clinical Immunology and Rheumatology and Department of Experimental Immunology, Amsterdam UMC, University of Amsterdam, Amsterdam Infection & Immunity Institute, Amsterdam, Netherlands.
Amsterdam Rheumatology & Immunology Center (ARC), Academic Medical Center, Amsterdam, Netherlands.

Vivianne Malmström (V)

Division of Rheumatology, Department of Medicine Solna, Center for Molecular Medicine, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden. vivianne.malmstrom@ki.se.

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