A neomorphic mutation in the interferon activation domain of IRF4 causes a dominant primary immunodeficiency.


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:
05 06 2023
Historique:
received: 28 07 2022
revised: 10 01 2023
accepted: 10 02 2023
entrez: 14 3 2023
pubmed: 15 3 2023
medline: 17 3 2023
Statut: ppublish

Résumé

Here, we report on a heterozygous interferon regulatory factor 4 (IRF4) missense variant identified in three patients from a multigeneration family with hypogammaglobulinemia. Patients' low blood plasmablast/plasma cell and naïve CD4 and CD8 T cell counts contrasted with high terminal effector CD4 and CD8 T cell counts. Expression of the mutant IRF4 protein in control lymphoblastoid B cell lines reduced the expression of BLIMP-1 and XBP1 (key transcription factors in plasma cell differentiation). In B cell lines, the mutant IRF4 protein as wildtype was found to bind to known IRF4 binding motifs. The mutant IRF4 failed to efficiently regulate the transcriptional activity of interferon-stimulated response elements (ISREs). Rapid immunoprecipitation mass spectrometry of endogenous proteins indicated that the mutant and wildtype IRF4 proteins differed with regard to their respective sets of binding partners. Our findings highlight a novel mechanism for autosomal-dominant primary immunodeficiency through altered protein binding by mutant IRF4 at ISRE, leading to defective plasma cell differentiation.

Identifiants

pubmed: 36917008
pii: 213935
doi: 10.1084/jem.20221292
pmc: PMC10037104
pii:
doi:

Substances chimiques

Interferon Regulatory Factors 0
interferon regulatory factor-4 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 Thouenon et al.

Références

Proc Natl Acad Sci U S A. 2005 Nov 1;102(44):15989-94
pubmed: 16236719
J Exp Med. 2013 Dec 16;210(13):2887-902
pubmed: 24323359
Nat Commun. 2017 Dec 12;8(1):2085
pubmed: 29233972
Life Sci Alliance. 2020 Aug 25;3(10):
pubmed: 32843533
Immunity. 2017 Dec 19;47(6):1129-1141.e5
pubmed: 29246443
J Allergy Clin Immunol. 2018 May;141(5):1924-1927.e18
pubmed: 29408330
J Clin Invest. 2019 Mar 1;129(3):1047-1060
pubmed: 30521495
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nat Protoc. 2016 Feb;11(2):316-26
pubmed: 26797456
J Clin Immunol. 2020 Jan;40(1):66-81
pubmed: 32048120
Nat Immunol. 2021 Jul;22(7):893-903
pubmed: 34155405
Immunity. 2017 Sep 19;47(3):481-497.e7
pubmed: 28930660
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Proc Natl Acad Sci U S A. 2019 Aug 6;116(32):16046-16055
pubmed: 31341086
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Nat Rev Immunol. 2013 Jul;13(7):519-33
pubmed: 23765059
Nat Commun. 2016 Mar 01;7:10815
pubmed: 26926045
Blood Adv. 2018 Apr 24;2(8):883-894
pubmed: 29669755
J Clin Immunol. 2020 Jan;40(1):24-64
pubmed: 31953710
Cell. 2013 Nov 21;155(5):1022-33
pubmed: 24267888
Nucleic Acids Res. 2021 Feb 26;49(4):2255-2265
pubmed: 33533913
Genome Biol. 2014;15(12):550
pubmed: 25516281
J Biol Chem. 2015 Nov 13;290(46):27779-90
pubmed: 26405037
J Immunol. 1999 Dec 15;163(12):6468-78
pubmed: 10586038
Mol Cell Biol. 2002 Nov;22(21):7439-48
pubmed: 12370291
Nat Biotechnol. 2019 Aug;37(8):907-915
pubmed: 31375807
EMBO J. 1999 Feb 15;18(4):977-91
pubmed: 10022840
Trends Genet. 2020 Dec;36(12):936-950
pubmed: 32873422
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Nat Immunol. 2013 Nov;14(11):1155-65
pubmed: 24056747
Cytometry B Clin Cytom. 2020 Mar;98(2):146-160
pubmed: 31758746
Science. 1997 Jan 24;275(5299):540-3
pubmed: 8999800
J Allergy Clin Immunol. 2021 Feb;147(2):734-737
pubmed: 32531373
Cell Rep. 2013 Feb 21;3(2):342-9
pubmed: 23403292
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Genome Biol. 2014 Feb 03;15(2):R29
pubmed: 24485249
Immunol Rev. 2012 May;247(1):73-92
pubmed: 22500833
Immunity. 2013 May 23;38(5):918-29
pubmed: 23684984
Nature. 2012 Oct 25;490(7421):543-6
pubmed: 22992523
J Immunol. 2007 Dec 1;179(11):7614-23
pubmed: 18025207
Genes Dev. 1996 Sep 15;10(18):2335-47
pubmed: 8824592
Trends Immunol. 2020 Jul;41(7):614-628
pubmed: 32467029
Immunity. 2006 Aug;25(2):225-36
pubmed: 16919487
Arch Pharm Res. 2016 Nov;39(11):1548-1555
pubmed: 27826752
Annu Rev Immunol. 2005;23:367-86
pubmed: 15771575
Cell Rep. 2020 Dec 22;33(12):108517
pubmed: 33357426
Nat Immunol. 2006 Jul;7(7):773-82
pubmed: 16767092
Elife. 2018 Mar 14;7:
pubmed: 29537367
Eur J Immunol. 2014 Jul;44(7):1886-95
pubmed: 24782159
PLoS Genet. 2008 May 16;4(5):e1000074
pubmed: 18483556

Auteurs

Romane Thouenon (R)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Loïc Chentout (L)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Nidia Moreno-Corona (N)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Lucie Poggi (L)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Emilia Puig Lombardi (EP)

Université de Paris, Bioinformatics Core Facility, Imagine Institute, INSERM UMR 1163 , Paris, France.

Benedicte Hoareau (B)

Sorbonne Université , UMS037, PASS, Plateforme de Cytométrie de la Pitié-Salpêtrière , Paris, France.

Yohann Schmitt (Y)

Plateforme de génomique, Institut Imagine-Structure Fédérative de Recherche Necker, INSERM U1163 et INSERM US24/CNRS UMS3633, Université de Paris , Paris, France.

Chantal Lagresle-Peyrou (C)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.
Biotherapy Clinical Investigation Center, Groupe Hospitalier Universitaire Ouest, Assistance Publique-Hôpitaux de Paris, INSERM , Paris, France.

Jacinta Bustamante (J)

St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University , New York, NY, USA.
Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children , Paris, France.
Paris Hospital, Study Center for Primary Immunodeficiencies, Assistance Publique-Hôpitaux de Paris , Paris, France.

Isabelle André (I)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Marina Cavazzana (M)

Université Paris Cité , Paris, France.
Biotherapy Clinical Investigation Center, Groupe Hospitalier Universitaire Ouest, Assistance Publique-Hôpitaux de Paris, INSERM , Paris, France.
Departement de Biotherapie Hôpital Universitaire Necker-Enfants malades, Groupe Hospitalier Paris Centre Assistance Publique-Hôpitaux de Paris , Paris, France.
Imagine Institute, INSERM UMR 1163 , Paris, France.

Anne Durandy (A)

Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

Jean-Laurent Casanova (JL)

St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University , New York, NY, USA.
Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children , Paris, France.
Necker Hospital, Pediatric Hematology-Immunology and Rheumatology Unit, Assistance Publique-Hôpitaux de Paris , Paris, France.
Howard Hughes Medical Institute , New York, NY, USA.

Lionel Galicier (L)

Clinical Immunology Department, Hôpital Saint Louis, Université de Paris , Paris, France.
National Reference Center for Castleman disease, Hôpital Saint Louis, Université de Paris , Paris, France.

Jehane Fadlallah (J)

Clinical Immunology Department, Hôpital Saint Louis, Université de Paris , Paris, France.
National Reference Center for Castleman disease, Hôpital Saint Louis, Université de Paris , Paris, France.

Alain Fischer (A)

Imagine Institute, INSERM UMR 1163 , Paris, France.
Necker Hospital, Pediatric Hematology-Immunology and Rheumatology Unit, Assistance Publique-Hôpitaux de Paris , Paris, France.
Collège de France , Paris, France.

Sven Kracker (S)

Université Paris Cité , Paris, France.
Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163 , Paris, France.

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Classifications MeSH