Carriers of the p.P522R variant in PLCγ2 have a slightly more responsive immune system.

Flow cytometry Functional studies Healthy aging Immunosenescence PLCG2 rs72824905 PLCγ2 p.P522R Phospholipase C gamma 2

Journal

Molecular neurodegeneration
ISSN: 1750-1326
Titre abrégé: Mol Neurodegener
Pays: England
ID NLM: 101266600

Informations de publication

Date de publication:
20 04 2023
Historique:
received: 08 08 2022
accepted: 14 02 2023
medline: 24 4 2023
pubmed: 21 4 2023
entrez: 20 04 2023
Statut: epublish

Résumé

The rs72824905 single-nucleotide polymorphism in the PLCG2 gene, encoding the p.P522R residue change in Phospholipase C gamma 2 (PLCγ2), associates with protection against several dementia subtypes and with increased likelihood of longevity. Cell lines and animal models indicated that p.P522R is a functional hypermorph. We aimed to confirm this in human circulating peripheral immune cells. We compared effects of p.P522R on immune system function between carriers and non-carriers (aged 59-103y), using in-depth immunophenotyping, functional B-cell and myeloid cell assays, and in vivo SARS-CoV-2 vaccination. In line with expectations, p.P522R impacts immune cell function only slightly, but it does so across a wide array of immune cell types. Upon B-cell stimulation, we observed increased PLCγ2 phosphorylation and calcium release, suggesting increased B-cell sensitivity upon antigen recognition. Further, p.P522R-carriers had higher numbers of CD20++CD21-CD24+ naive B cells and IgG1+ memory B cells. In myeloid cells, normalized ROS production was higher upon PLCγ2-dependent stimulation. On classical monocytes, CD33 levels were elevated. Furthermore, carriers expressed lower levels of allergy-related FcεRI on several immune cell subsets. Nevertheless, carriers and non-carriers had similar serological responses to SARS-CoV-2 vaccination. The immune system from p.P522R-carriers is slightly more responsive to stimulation than in non-carriers.

Sections du résumé

BACKGROUND
The rs72824905 single-nucleotide polymorphism in the PLCG2 gene, encoding the p.P522R residue change in Phospholipase C gamma 2 (PLCγ2), associates with protection against several dementia subtypes and with increased likelihood of longevity. Cell lines and animal models indicated that p.P522R is a functional hypermorph. We aimed to confirm this in human circulating peripheral immune cells.
METHODS
We compared effects of p.P522R on immune system function between carriers and non-carriers (aged 59-103y), using in-depth immunophenotyping, functional B-cell and myeloid cell assays, and in vivo SARS-CoV-2 vaccination.
RESULTS
In line with expectations, p.P522R impacts immune cell function only slightly, but it does so across a wide array of immune cell types. Upon B-cell stimulation, we observed increased PLCγ2 phosphorylation and calcium release, suggesting increased B-cell sensitivity upon antigen recognition. Further, p.P522R-carriers had higher numbers of CD20++CD21-CD24+ naive B cells and IgG1+ memory B cells. In myeloid cells, normalized ROS production was higher upon PLCγ2-dependent stimulation. On classical monocytes, CD33 levels were elevated. Furthermore, carriers expressed lower levels of allergy-related FcεRI on several immune cell subsets. Nevertheless, carriers and non-carriers had similar serological responses to SARS-CoV-2 vaccination.
CONCLUSION
The immune system from p.P522R-carriers is slightly more responsive to stimulation than in non-carriers.

Identifiants

pubmed: 37081539
doi: 10.1186/s13024-023-00604-9
pii: 10.1186/s13024-023-00604-9
pmc: PMC10116473
doi:

Substances chimiques

COVID-19 Vaccines 0
Phospholipase C gamma EC 3.1.4.3
PLCG2 protein, human EC 3.1.4.3

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

25

Informations de copyright

© 2023. The Author(s).

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Auteurs

Annieck M Diks (AM)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.
Department of Human Genetics, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, the Netherlands.

Cristina Teodosio (C)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.
Translational and Clinical Research Program, Cancer Research Center (IBMCC; University of Salamanca - CSIC), Salamanca, Spain.
Department of Medicine, University of Salamanca and Institute of Biomedical Research of Salamanca (IBSAL), Salamanca, Spain.

Bas de Mooij (B)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Rick J Groenland (RJ)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Brigitta A E Naber (BAE)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Inge F de Laat (IF)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Sandra A Vloemans (SA)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Susan Rohde (S)

Department of Human Genetics, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, the Netherlands.

Marien I de Jonge (MI)

Laboratory of Medical Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Centre, Nijmegen, The Netherlands.

Linda Lorenz (L)

Department of Human Genetics, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, the Netherlands.

Debbie Horsten (D)

Department of Human Genetics, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, the Netherlands.

Jacques J M van Dongen (JJM)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands. J.J.M.van_Dongen@lumc.nl.
Translational and Clinical Research Program, Cancer Research Center (IBMCC; University of Salamanca - CSIC), Salamanca, Spain. J.J.M.van_Dongen@lumc.nl.
Department of Medicine, University of Salamanca and Institute of Biomedical Research of Salamanca (IBSAL), Salamanca, Spain. J.J.M.van_Dongen@lumc.nl.

Magdalena A Berkowska (MA)

Department of Immunology, Leiden University Medical Center, Albinusdreef 2, Leiden, ZA, 2333, the Netherlands.

Henne Holstege (H)

Department of Human Genetics, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, the Netherlands. H.holstege@amsterdamumc.nl.

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