NBEAL2 deficiency in humans leads to low CTLA-4 expression in activated conventional T cells.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
22 06 2023
Historique:
received: 08 09 2022
accepted: 06 06 2023
medline: 26 6 2023
pubmed: 23 6 2023
entrez: 22 6 2023
Statut: epublish

Résumé

Loss of NBEAL2 function leads to grey platelet syndrome (GPS), a bleeding disorder characterized by macro-thrombocytopenia and α-granule-deficient platelets. A proportion of patients with GPS develop autoimmunity through an unknown mechanism, which might be related to the proteins NBEAL2 interacts with, specifically in immune cells. Here we show a comprehensive interactome of NBEAL2 in primary T cells, based on mass spectrometry identification of altogether 74 protein association partners. These include LRBA, a member of the same BEACH domain family as NBEAL2, recessive mutations of which cause autoimmunity and lymphocytic infiltration through defective CTLA-4 trafficking. Investigating the potential association between NBEAL2 and CTLA-4 signalling suggested by the mass spectrometry results, we confirm by co-immunoprecipitation that CTLA-4 and NBEAL2 interact with each other. Interestingly, NBEAL2 deficiency leads to low CTLA-4 expression in patient-derived effector T cells, while their regulatory T cells appear unaffected. Knocking-down NBEAL2 in healthy primary T cells recapitulates the low CTLA-4 expression observed in the T cells of GPS patients. Our results thus show that NBEAL2 is involved in the regulation of CTLA-4 expression in conventional T cells and provide a rationale for considering CTLA-4-immunoglobulin therapy in patients with GPS and autoimmune disease.

Identifiants

pubmed: 37349339
doi: 10.1038/s41467-023-39295-7
pii: 10.1038/s41467-023-39295-7
pmc: PMC10287742
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Blood Proteins 0
CTLA-4 Antigen 0
LRBA protein, human EC 2.7.10.-
NBEAL2 protein, human 0
CTLA4 protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3728

Informations de copyright

© 2023. The Author(s).

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Auteurs

Laure Delage (L)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.
Checkpoint Immunology, Immunology and Inflammation Therapeutic Area, Sanofi, F-94400, Vitry-sur-Seine, France.

Francesco Carbone (F)

Université Paris Cité, Institut Imagine, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM UMR 1163, F-75015, Paris, France.
Labtech Single-Cell@Imagine, Imagine Institute, INSERM UMR 1163, F-75015, Paris, France.

Quentin Riller (Q)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.

Jean-Luc Zachayus (JL)

Immunology and Inflammation Therapeutic Area, Sanofi, F-94400, Vitry-sur-Seine, France.

Erwan Kerbellec (E)

Checkpoint Immunology, Immunology and Inflammation Therapeutic Area, Sanofi, F-94400, Vitry-sur-Seine, France.

Armelle Buzy (A)

BioStructure and Biophysics, Integrated Drug Discovery, Sanofi, F- 94400, Vitry-sur-Seine, France.

Marie-Claude Stolzenberg (MC)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.

Marine Luka (M)

Université Paris Cité, Institut Imagine, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM UMR 1163, F-75015, Paris, France.
Labtech Single-Cell@Imagine, Imagine Institute, INSERM UMR 1163, F-75015, Paris, France.

Camille de Cevins (C)

Université Paris Cité, Institut Imagine, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM UMR 1163, F-75015, Paris, France.
Artificial Intelligence & Deep Analytics (AIDA) Group, Data & Data Science (DDS), Sanofi R&D, F- 91380, Chilly-Mazarin, France.

Georges Kalouche (G)

Cellomics, Translational Sciences, Sanofi, F- 91380, Chilly-Mazarin, France.

Rémi Favier (R)

Assistance Publique-Hôpitaux de Paris, French national reference center for platelet disorders, Armand Trousseau Children Hospital, F-75012, Paris, France.
INSERM Unité Mixte de Recherche 1287, Gustave Roussy Cancer Campus, Paris-Saclay University, F-94805, Villejuif, France.

Alizée Michel (A)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.

Sonia Meynier (S)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.

Aurélien Corneau (A)

Sorbonne Université, UMS037, PASS, Plateforme de cytométrie de la Pitié-Salpêtrière CyPS, F-75013, Paris, France.

Caroline Evrard (C)

Immunology and Inflammation Therapeutic Area, Sanofi, F-94400, Vitry-sur-Seine, France.

Nathalie Neveux (N)

Laboratory of Biological Nutrition, EA 4466, Faculty of Pharmacy, Paris University, F-75014, Paris, France.
Clinical Chemistry Department, Hôpital Cochin, Assistance Publique - Hôpitaux de Paris (AP-HP), 4 Avenue de l'Observatoire, F-75014, Paris, France.

Sébastien Roudières (S)

BioStructure and Biophysics, Integrated Drug Discovery, Sanofi, F- 94400, Vitry-sur-Seine, France.

Brieuc P Pérot (BP)

Université Paris Cité, Institut Imagine, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM UMR 1163, F-75015, Paris, France.

Mathieu Fusaro (M)

Université Paris Cité, Institut Imagine, Laboratory of Lymphocyte Activation and Susceptibility to EBV Infection, INSERM UMR 1163, F-75015, Paris, France.

Christelle Lenoir (C)

Université Paris Cité, Institut Imagine, Laboratory of Lymphocyte Activation and Susceptibility to EBV Infection, INSERM UMR 1163, F-75015, Paris, France.

Olivier Pellé (O)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.
Flow Cytometry Core Facility, Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS3633, F-75015, Paris, France.

Mélanie Parisot (M)

Genomics Core Facility, Institut Imagine-Structure Fédérative de Recherche Necker, INSERM U1163 et INSERM US24/CNRS UAR3633, Université Paris Cité, F-75015, Paris, France.

Marc Bras (M)

Bioinformatics Platform, Structure Fédérative de Recherche Necker, INSERM UMR1163, Université Paris Cité, Imagine Institute, F-75015, Paris, France.

Sébastien Héritier (S)

Sorbonne Université, INSERM UMRS_938, CRSA, AP-HP, Pediatric Oncology Hematology Unit, Hôpital Armand Trousseau, F-75012, Paris, France.

Guy Leverger (G)

Sorbonne Université, INSERM UMRS_938, CRSA, AP-HP, Pediatric Oncology Hematology Unit, Hôpital Armand Trousseau, F-75012, Paris, France.

Anne-Sophie Korganow (AS)

Department of Clinical Immunology and Internal Medicine, National Reference Center for Systemic Autoimmune Diseases (CNR RESO), Tertiary Center for Primary Immunodeficiency, Strasbourg University Hospital, F-67091, Strasbourg, France.

Capucine Picard (C)

French National Reference Center for Primary Immune Deficiencies (CEREDIH), Necker-Enfants Malades University Hospital, AP-HP, F-75015, Paris, France.
Study Center for Primary Immunodeficiencies (CEDI), Necker-Enfants Malades University Hospital, AP-HP, F-75015, Paris, France.
Imagine Institute, INSERM UMR1163, Université Paris Cité, F-75015, Paris, France.

Sylvain Latour (S)

Université Paris Cité, Institut Imagine, Laboratory of Lymphocyte Activation and Susceptibility to EBV Infection, INSERM UMR 1163, F-75015, Paris, France.

Bénédicte Collet (B)

Pediatric Unit, Centre Hospitalier de Roubaix, F-59100, Roubaix, France.

Alain Fischer (A)

Imagine Institute, INSERM UMR1163, Université Paris Cité, F-75015, Paris, France.
Department of Paediatric Immuno-Haematology and Rheumatology, Reference Center for Rheumatic, AutoImmune and Systemic Diseases in Children (RAISE), Hôpital Necker-Enfants Malades, Assistance Publique - Hôpitaux de Paris (AP-HP), F-75015, Paris, France.
Collège de France, F-75231, Paris, France.

Bénédicte Neven (B)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.
Pediatric Immunohematology and Rheumatology Department, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris (AP-HP), F-75015, Paris, France.

Aude Magérus (A)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France.

Mickaël Ménager (M)

Université Paris Cité, Institut Imagine, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM UMR 1163, F-75015, Paris, France.
Labtech Single-Cell@Imagine, Imagine Institute, INSERM UMR 1163, F-75015, Paris, France.

Benoit Pasquier (B)

Checkpoint Immunology, Immunology and Inflammation Therapeutic Area, Sanofi, F-94400, Vitry-sur-Seine, France.

Frédéric Rieux-Laucat (F)

Université Paris Cité, Institut Imagine, Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163, F-75015, Paris, France. frederic.rieux-laucat@inserm.fr.

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Classifications MeSH