Severe Autoinflammatory Manifestations and Antibody Deficiency Due to Novel Hypermorphic PLCG2 Mutations


Por: Martín-Nalda A, Fortuny-Guasch C, Rey L, Bunney TD, Alsina L, Esteve-Solé A, Bull D, Anton MC, Basagaña M, Casals F, Deyá A, García-Prat M, Gimeno R, Juan-Otero M, Martinez-Banaclocha H, Martinez-Garcia JJ, Mensa-Vilaró A, Rabionet-Janssen R, Martin-Begue N, Rudilla F, Yagüe-Ribes J, Estivill X, García-Patos V, Pujol RM, Soler-Palacín P, Katan M, Pelegrín P, Colobran R, Vicente-Villa MA and Arostegui-Gorospe JI

Publicada: 1 oct 2020 Ahead of Print: 1 jul 2020
Resumen:
Autoinflammatory diseases (AIDs) were first described as clinical disorders characterized by recurrent episodes of seemingly unprovoked sterile inflammation. In the past few years, the identification of novel AIDs expanded their phenotypes toward more complex clinical pictures associating vasculopathy, autoimmunity, or immunodeficiency. Herein, we describe two unrelated patients suffering since the neonatal period from a complex disease mainly characterized by severe sterile inflammation, recurrent bacterial infections, and marked humoral immunodeficiency. Whole-exome sequencing detected a novel, de novo heterozygous PLCG2 variant in each patient (p.Ala708Pro and p.Leu845_Leu848del). A clear enhanced PLC gamma 2 activity for both variants was demonstrated by both ex vivo calcium responses of the patient's B cells to IgM stimulation and in vitro assessment of PLC activity. These data supported the autoinflammation and PLC gamma 2-associated antibody deficiency and immune dysregulation (APLAID) diagnosis in both patients. Immunological evaluation revealed a severe decrease of immunoglobulins and B cells, especially class-switched memory B cells, with normal T and NK cell counts. Analysis of bone marrow of one patient revealed a reduced immature B cell fraction compared with controls. Additional investigations showed that both PLCG2 variants activate the NLRP3-inflammasome through the alternative pathway instead of the canonical pathway. Collectively, the evidences here shown expand APLAID diversity toward more severe phenotypes than previously reported including dominantly inherited agammaglobulinemia, add novel data about its genetic basis, and implicate the alternative NLRP3-inflammasome activation pathway in the basis of sterile inflammation.

Filiaciones:
Martín-Nalda A:
 Pediatric Infectious Diseases and Immunodeficiencies Unit, Vall d'Hebron Institut de Recerca, Hospital Universitari Vall d'Hebron, Barcelona, Spain

 Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain

Fortuny-Guasch C:
 Pediatric Infectious Diseases and Immunodeficiencies Unit, Vall d'Hebron Institut de Recerca, Hospital Universitari Vall d'Hebron, Barcelona, Spain

 Department of Pediatrics, Hospital Sant Joan de Deu, Esplugues, Spain

 Institut de Recerca Hospital Sant Joan de Déu, Universitat de Barcelona, Esplugues, Spain

Rey L:
 Department of Pediatrics, Hospital Alvaro Cunqueiro, Vigo, Spain

Bunney TD:
 Institute of Structural and Molecular Biology, University College London, London, UK

Alsina L:
 Institut de Recerca Hospital Sant Joan de Déu, Universitat de Barcelona, Esplugues, Spain

 Department of Allergy and Clinical Immunology Clinical Immunology and Primary, Immunodeficiencies Unit, Hospital Sant Joan de Déu, Esplugues, Spain

 Clinical Immunology Unit, Hospital Sant Joan de Déu-Hospital Clínic, Barcelona, Spain

Esteve-Solé A:
 Institut de Recerca Hospital Sant Joan de Déu, Universitat de Barcelona, Esplugues, Spain

 Department of Allergy and Clinical Immunology Clinical Immunology and Primary, Immunodeficiencies Unit, Hospital Sant Joan de Déu, Esplugues, Spain

 Clinical Immunology Unit, Hospital Sant Joan de Déu-Hospital Clínic, Barcelona, Spain

Bull D:
 ARUK Drug Discovery Institute, University College London, London, UK

Anton MC:
 Department of Immunology-CDB (esc 4-pl 0), Hospital Clínic, Villarroel, 170, 08036, Barcelona, Spain

Basagaña M:
 Allergy Section, Hospital Universitari Germans Trias i Pujol, Autonomous University of Barcelona, Badalona, Spain

Casals F:
 Genomics Core Facility, Experimental and Health Sciences Department, Universitat Pompeu Fabra, Barcelona, Spain

Deyá A:
 Institut de Recerca Hospital Sant Joan de Déu, Universitat de Barcelona, Esplugues, Spain

 Department of Allergy and Clinical Immunology Clinical Immunology and Primary, Immunodeficiencies Unit, Hospital Sant Joan de Déu, Esplugues, Spain

 Clinical Immunology Unit, Hospital Sant Joan de Déu-Hospital Clínic, Barcelona, Spain

García-Prat M:
 Pediatric Infectious Diseases and Immunodeficiencies Unit, Vall d'Hebron Institut de Recerca, Hospital Universitari Vall d'Hebron, Barcelona, Spain

 Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain

Gimeno R:
 Department of Immunology, Hospital del Mar, Institut Mar d'Investigacions Mèdiques, Barcelona, Spain

Juan-Otero M:
 Department of Immunology-CDB (esc 4-pl 0), Hospital Clínic, Villarroel, 170, 08036, Barcelona, Spain

 Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain

 School of Medicine, Universitat de Barcelona, Barcelona, Spain

Martinez-Banaclocha H:
 Instituto Murciano de Investigación Biosanitaria IMIB-Arrixaca, Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain

Martinez-Garcia JJ:
 Instituto Murciano de Investigación Biosanitaria IMIB-Arrixaca, Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain

Mensa-Vilaró A:
 Department of Immunology-CDB (esc 4-pl 0), Hospital Clínic, Villarroel, 170, 08036, Barcelona, Spain

Rabionet-Janssen R:
 Institut de Recerca Hospital Sant Joan de Déu, Universitat de Barcelona, Esplugues, Spain

 Department of Genetics, Microbiology and Statistics, Faculty of Biology, University of Barcelona, IBUB, IRJSD, CIBERER, Barcelona, Spain

Martin-Begue N:
 Department of Pediatric Ophthalmology, Hospital Universitari Vall d'Hebron, Vall d'Hebron Institut de Recerca, Barcelona, Spain

Rudilla F:
 Histocompatibility and Immunogenetics Laboratory, Blood and Tissue Bank, Barcelona, Spain

 Transfusional Medicine Group, Vall d'Hebron Research Institute, Autonomous University of Barcelona, Barcelona, Spain

Yagüe-Ribes J:
 Department of Immunology-CDB (esc 4-pl 0), Hospital Clínic, Villarroel, 170, 08036, Barcelona, Spain

 Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain

 School of Medicine, Universitat de Barcelona, Barcelona, Spain

Estivill X:
 Quantitative Genomic Medicine Laboratories (qGenomics), Esplugues del Llobregat, Barcelona, Catalonia, Spain

García-Patos V:
 Department of Pediatric Dermatology, Hospital Universitari Vall d'Hebron, Vall d'Hebron Institut de Recerca, Barcelona, Spain

Pujol RM:
 Department of Dermatology, Hospital del Mar, Institut Mar d'Investigacions Mèdiques, Universitat Autonoma de Barcelona, Barcelona, Spain

Soler-Palacín P:
 Pediatric Infectious Diseases and Immunodeficiencies Unit, Vall d'Hebron Institut de Recerca, Hospital Universitari Vall d'Hebron, Barcelona, Spain

 Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain

 Universitat Autònoma de Barcelona, Barcelona, Spain

Katan M:
 Institute of Structural and Molecular Biology, University College London, London, UK

Pelegrín P:
 Instituto Murciano de Investigación Biosanitaria IMIB-Arrixaca, Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain

Colobran R:
 Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain

 Immunology Division, Department of Clinical and Molecular Genetics, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute, Barcelona, Spain

 Department of Cell Biology, Physiology and Immunology, Autonomous University of Barcelona, Barcelona, Spain

Vicente-Villa MA:
 Department of Pediatric Dermatology, Hospital Sant Joan de Deu, Esplugues, Spain

Arostegui-Gorospe JI:
 Department of Immunology-CDB (esc 4-pl 0), Hospital Clínic, Villarroel, 170, 08036, Barcelona, Spain.

 Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain.

 School of Medicine, Universitat de Barcelona, Barcelona, Spain.
ISSN: 02719142





JOURNAL OF CLINICAL IMMUNOLOGY
Editorial
SPRINGER/PLENUM PUBLISHERS, 233 SPRING ST, NEW YORK, NY 10013, Estados Unidos America
Tipo de documento: Article
Volumen: 40 Número: 7
Páginas: 987-1000
WOS Id: 000548758900001
ID de PubMed: 32671674
imagen Green Submitted, Green Published, hybrid

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