Inherited TNFSF9 deficiency causes broad Epstein-Barr virus infection with EBV+ smooth muscle tumors.


Journal

The Journal of experimental medicine
ISSN: 1540-9538
Titre abrégé: J Exp Med
Pays: United States
ID NLM: 2985109R

Informations de publication

Date de publication:
04 07 2022
Historique:
received: 06 08 2021
revised: 16 03 2022
accepted: 25 04 2022
entrez: 3 6 2022
pubmed: 4 6 2022
medline: 9 6 2022
Statut: ppublish

Résumé

Epstein-Barr virus (EBV) can infect smooth muscle cells causing smooth muscle tumors (SMTs) or leiomyoma. Here, we report a patient with a heterozygous 22q11.2 deletion/DiGeorge syndrome who developed a unique, broad, and lethal susceptibility to EBV characterized by EBV-infected T and B cells and disseminated EBV+SMT. The patient also harbored a homozygous missense mutation (p.V140G) in TNFSF9 coding for CD137L/4-1BBL, the ligand of the T cell co-stimulatory molecule CD137/4-1BB, whose deficiency predisposes to EBV infection. We show that wild-type CD137L was up-regulated on activated monocytes and dendritic cells, EBV-infected B cells, and SMT. The CD137LV140G mutant was weakly expressed on patient cells or when ectopically expressed in HEK and P815 cells. Importantly, patient EBV-infected B cells failed to trigger the expansion of EBV-specific T cells, resulting in decreased T cell effector responses. T cell expansion was recovered when CD137L expression was restored on B cells. Therefore, these results highlight the critical role of the CD137-CD137L pathway in anti-EBV immunity, in particular in the control of EBV+SMT.

Identifiants

pubmed: 35657354
pii: 213262
doi: 10.1084/jem.20211682
pmc: PMC9170382
pii:
doi:

Substances chimiques

4-1BB Ligand 0
TNFSF9 protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Centre National de la Recherche Scientifique
Organisme : Fondation pour la Recherche Médicale
ID : FDM20170638301
Organisme : Ligue Contre le Cancer
Organisme : Institut National de la Santé et de la Recherche Médicale
Organisme : Agence Nationale de Recherche
ID : ANR-18-CE15-0025-01
Organisme : Institut National du Cancer
ID : PLBIO-2020
Organisme : Société Française de Lutte contre les Cancers et Leucémies de l'Enfant et de l'Adolescent
Organisme : Fédération Enfants et Santé
Organisme : Rare Diseases Foundation

Informations de copyright

© 2022 Fournier et al.

Références

FASEB J. 2007 Feb;21(2):456-63
pubmed: 17167064
Cell Rep. 2018 Oct 23;25(4):909-920.e4
pubmed: 30355497
Am J Med Genet A. 2017 Sep;173(9):2366-2372
pubmed: 28627729
J Allergy Clin Immunol. 2018 Mar;141(3):1028-1035
pubmed: 28606585
N Engl J Med. 1995 Jan 5;332(1):12-8
pubmed: 7990860
J Allergy Clin Immunol. 2019 Aug;144(2):574-583.e5
pubmed: 30872117
Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1291-6
pubmed: 14745033
Blood. 2019 Oct 31;134(18):1510-1516
pubmed: 31501153
J Biol Chem. 2019 Feb 8;294(6):1831-1845
pubmed: 30545939
J Biol Chem. 2018 Jun 22;293(25):9880-9891
pubmed: 29720399
Curr Pediatr Rev. 2019;15(4):245-250
pubmed: 31530267
Am J Clin Pathol. 2001 Apr;115(4):543-9
pubmed: 11293902
Croat Med J. 2008 Apr;49(2):192-200
pubmed: 18461674
Immunol Lett. 2003 Dec 15;90(2-3):215-21
pubmed: 14687728
Circulation. 2008 Mar 11;117(10):1292-301
pubmed: 18285570
J Immunol. 2007 Apr 15;178(8):5227-36
pubmed: 17404306
J Exp Med. 2020 Nov 2;217(11):
pubmed: 32812031
Eur J Immunol. 2010 Jul;40(7):1938-49
pubmed: 20432236
Blood. 2009 Oct 15;114(16):3431-8
pubmed: 19641184
J Immunol. 2002 May 15;168(10):4897-906
pubmed: 11994439
Immunol Rev. 2019 Jan;287(1):186-201
pubmed: 30565249
Cancer Res. 2011 Feb 1;71(3):801-11
pubmed: 21266358
Blood. 2020 Feb 27;135(9):644-655
pubmed: 31942615
Immunol Rev. 2019 Sep;291(1):174-189
pubmed: 31402499
Am J Med Genet A. 2018 Oct;176(10):2058-2069
pubmed: 30380191
J Exp Med. 2017 Jan;214(1):73-89
pubmed: 28011863
Hum Pathol. 2011 Dec;42(12):2037-41
pubmed: 21683977
Blood Adv. 2019 Apr 9;3(7):1129-1144
pubmed: 30952679
Nature. 2014 Jun 12;510(7504):288-92
pubmed: 24870241
Blood. 2018 Jan 4;131(1):49-57
pubmed: 29118009
Clin Case Rep. 2017 Mar 02;5(4):486-490
pubmed: 28396774
Blood. 2009 Sep 10;114(11):2280-9
pubmed: 19608748
J Pediatr. 2014 Jun;164(6):1475-80.e2
pubmed: 24657119
Int Immunol. 2002 Oct;14(10):1155-67
pubmed: 12356681
N Engl J Med. 1995 Jan 5;332(1):19-25
pubmed: 7990861
Front Pediatr. 2019 Feb 04;7:15
pubmed: 30778380
J Exp Med. 2019 Dec 2;216(12):2800-2818
pubmed: 31537641
Cell Immunol. 2003 Nov;226(1):37-44
pubmed: 14746806
J Biol Chem. 2010 Mar 19;285(12):9202-10
pubmed: 20032458
Blood. 2020 Dec 3;136(23):2638-2655
pubmed: 32603431
Am J Med Genet A. 2018 Oct;176(10):2121-2127
pubmed: 28940864
Proc Natl Acad Sci U S A. 2018 Jan 23;115(4):E686-E695
pubmed: 29311309
Annu Rev Pathol. 2019 Jan 24;14:29-53
pubmed: 30125149
Am J Hum Genet. 1999 Apr;64(4):1076-86
pubmed: 10090893
J Vasc Res. 2004 Jan-Feb;41(1):84-90
pubmed: 14752253

Auteurs

Benjamin Fournier (B)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.
Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Akihiro Hoshino (A)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.

Julie Bruneau (J)

Department of Pathology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Camille Bachelet (C)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.

Mathieu Fusaro (M)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.
Study Center for Primary Immunodeficiencies, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Roman Klifa (R)

Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Romain Lévy (R)

Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Christelle Lenoir (C)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.

Claire Soudais (C)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.

Capucine Picard (C)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.
Study Center for Primary Immunodeficiencies, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Stéphane Blanche (S)

Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Martin Castelle (M)

Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Despina Moshous (D)

Paris Cité University, Imagine Institute, Paris, France.
Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Thierry Molina (T)

Department of Pathology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Anne-Sophie Defachelles (AS)

Department of Pediatric Oncology, Oscar Lambret Cancer Center, Lille, France.

Bénédicte Neven (B)

Paris Cité University, Imagine Institute, Paris, France.
Department of Pediatric Immunology, Hematology and Rheumatology, Necker-Enfants Malades Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Sylvain Latour (S)

Laboratory of Lymphocyte Activation and Susceptibility to EBV infection, Institut national de la santé et de la recherche médicale UMR 1163, Paris, France.
Paris Cité University, Imagine Institute, Paris, France.

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