Immunoglobulin genes and severity of COVID-19.

FCGR2A ADCC COVID-19 GM allotypes Humoral immunity SARS-CoV-2

Journal

Immunogenetics
ISSN: 1432-1211
Titre abrégé: Immunogenetics
Pays: United States
ID NLM: 0420404

Informations de publication

Date de publication:
11 Apr 2024
Historique:
received: 08 02 2024
accepted: 02 04 2024
medline: 11 4 2024
pubmed: 11 4 2024
entrez: 11 4 2024
Statut: aheadofprint

Résumé

There is tremendous interindividual and interracial variability in the outcome of SARS-CoV-2 infection, suggesting the involvement of host genetic factors. Here, we investigated whether IgG allotypes GM (γ marker) 3 and GM 17, genetic markers of IgG1, contributed to the severity of COVID-19. IgG1 plays a pivotal role in response against SARS-CoV-2 infection. We also investigated whether these GM alleles synergistically/epistatically with IGHG3 and FCGR2A alleles-which have been previously implicated in COVID-19-modulated the extent of COVID-19 severity. The study population consisted of 316 COVID-19 patients who needed treatment in the intensive care unit of Hospital Universitario Central de Asturias. All individuals were genotyped for GM 3/17, IGHG3 hinge length, and FCGR2A rs1801274 A/G polymorphisms. Among the 316 critical patients, there were 86 deaths. The risk of death among critical patients was significantly higher in subjects with GM 17 (IgG1) and short hinge length (IgG3). GM 17-carriers were at almost three-fold higher risk of death than non-carriers (p < 0.001; OR = 2.86, CI 1.58-5.16). Subjects with short hinge length of IgG3 had a two-fold higher risk of death than those with medium hinge length (p = 0.01; OR = 2.16, CI 1.19-3.90). GM 3/3 and IGHG3 (MM) genotypes were less frequent among death vs. survivors (9% vs 36%, p < 0.001) and associated with protective effect (OR = 0.18, 95% CI = 0.08-0.39). This is the first report implicating IgG1 allotypes in COVID-19-spurred death. It needs to be replicated in an independent study population.

Identifiants

pubmed: 38602517
doi: 10.1007/s00251-024-01341-z
pii: 10.1007/s00251-024-01341-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : U.S. Department of Defense
ID : W81XWH2210072
Organisme : Instituto de Salud Carlos III
ID : ISCIII PI-21/00971

Informations de copyright

© 2024. The Author(s).

Références

Armour KL, Smith CS, Clark MR (2010) Expression of human FcgammaRIIIa as a GPI-linked molecule on CHO cells to enable measurement of human IgG binding. J Immunol Methods 354:20–33
doi: 10.1016/j.jim.2010.01.011 pubmed: 20138184
Bruhns P, Iannascoli B, England P et al (2009) Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113:3716–3725
doi: 10.1182/blood-2008-09-179754 pubmed: 19018092
Di Bona D, Accardi G, Aiello A et al (2018) Association between γ marker, human leucocyte antigens and killer immunoglobulin-like receptors and the natural course of human cytomegalovirus infection: a pilot study performed in a Sicilian population. Immunology 153:523–531
doi: 10.1111/imm.12855 pubmed: 29067686
Gaunt TR, Rodríguez S, Day IN (2007) Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool ‘CubeX.’ BMC Bioinformatics 8:428
doi: 10.1186/1471-2105-8-428 pubmed: 17980034 pmcid: 2180187
Grubb R (1995) Advances in human immunoglobulin allotypes. Exp Clin Immunogenet 12:191–197
pubmed: 8534505
Kallolimath S, Sun L, Palt R et al (2021) Highly active engineered IgG3 antibodies against SARS-CoV-2. Proc Natl Acad Sci U S A 118(42):e2107249118
doi: 10.1073/pnas.2107249118 pubmed: 34599091 pmcid: 8545452
Ligotti ME, Calabrò A, Accardi G et al (2022) GM allotypes and COVID-19. A pilot study performed on Sicilian patients. Transl Med UniSa 24:26–29
pubmed: 37476201 pmcid: 10354864
López-Martínez R, Albaiceta GM, Amado-Rodríguez L et al (2022a) IGHG3 hinge length variation was associated with the risk of critical disease and death in a Spanish COVID-19 cohort. Genes Immun 23:205–208
doi: 10.1038/s41435-022-00179-3 pubmed: 36088493 pmcid: 9463670
López-Martínez R, Albaiceta GM, Amado-Rodríguez L et al (2022b) The FCGR2A rs1801274 polymorphism was associated with the risk of death among COVID-19 patients. Clin Immunol 236:108954
doi: 10.1016/j.clim.2022.108954 pubmed: 35149195 pmcid: 8824710
Moraru M, Black LE, Muntasell A et al (2015) NK cells and immunoglobulins interplay in defense against herpes simplex virus type 1: epistatic interaction of CD16A and IgG1 allotypes of variable affinity modulates antibody-dependent cellular cytotoxicity and susceptibility to clinical reactivation. J Immunol 195:1676–1684
doi: 10.4049/jimmunol.1500872 pubmed: 26179905
Nagelkerke SQ, Schmidt DE, de Haas M, Kuijpers TW (2019) Genetic variation in low-to-medium-affinity Fcγ receptors: functional consequences, disease associations, and opportunities for personalized medicine. Front Immunol 10:1–24
doi: 10.3389/fimmu.2019.02237
Oxelius VA, Pandey JP (2013) Human immunoglobulin constant heavy G chain (IGHG) (Fcγ) (GM) genes, defining innate variants of IgG molecules and B cells, have impact on disease and therapy. Clin Immunol 149:475–486
doi: 10.1016/j.clim.2013.10.003 pubmed: 24239836
Pandey JP (2022) IgG3 constant-region GM (γ marker) allotypes could influence the neutralizing potency of anti-SARS-CoV-2 monoclonal antibodies. Proc Natl Acad Sci USA 119(6):e2119380119
doi: 10.1073/pnas.2119380119 pubmed: 35105812 pmcid: 8833157
Pandey JP, Kothera RT, Liu S et al (2019) Immunoglobulin genes and immunity to HSV1 in Alzheimer’s disease. J Alzheimer’s Dis 70:917–924
doi: 10.3233/JAD-190265
Typiak M, Rękawiecki B, Rębała K, Dubaniewicz A (2023) Comparative analysis of FCGR gene polymorphism in pulmonary sarcoidosis and tuberculosis. Cells 12:1221
doi: 10.3390/cells12091221 pubmed: 37174624 pmcid: 10177102
Vejbaesya S, Tanwandee T, Pandey JP (2004) Immunoglobulin GM and KM genotypes in hepatitis C virus infection. J Med Virol 73:384–386
doi: 10.1002/jmv.20102 pubmed: 15170632

Auteurs

Daniel Vázquez-Coto (D)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain.
Genética Molecular, Hospital Universitario Central Asturias, Oviedo, Spain.

Christine Kimball (C)

Department of Microbiology and Immunology, Medical University of South Carolina, Charleston, SC, 29425, USA.

Guillermo M Albaiceta (GM)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain.
Unidad de Cuidados Intensivos Cardiológicos, Hospital Universitario Central Asturias, Oviedo, Spain.
Universidad de Oviedo, Oviedo, Spain.
CIBER-Enfermedades Respiratorias, Instituto de Salud Carlos III, Madrid, Spain.
Instituto Universitario de Oncología del Principado de Asturias, Oviedo, Spain.

Laura Amado-Rodríguez (L)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain.
Unidad de Cuidados Intensivos Cardiológicos, Hospital Universitario Central Asturias, Oviedo, Spain.
Universidad de Oviedo, Oviedo, Spain.
CIBER-Enfermedades Respiratorias, Instituto de Salud Carlos III, Madrid, Spain.
Instituto Universitario de Oncología del Principado de Asturias, Oviedo, Spain.

Marta García-Clemente (M)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain.
Universidad de Oviedo, Oviedo, Spain.
Neumología, Hospital Universitario Central Asturias, Oviedo, Spain.

Juan Gómez (J)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain.
Genética Molecular, Hospital Universitario Central Asturias, Oviedo, Spain.

Eliecer Coto (E)

Instituto de Investigación Sanitaria del Principado de Asturias, ISPA, Oviedo, Spain. eliecer.coto@sespa.es.
Genética Molecular, Hospital Universitario Central Asturias, Oviedo, Spain. eliecer.coto@sespa.es.
Universidad de Oviedo, Oviedo, Spain. eliecer.coto@sespa.es.

Janardan P Pandey (JP)

Department of Microbiology and Immunology, Medical University of South Carolina, Charleston, SC, 29425, USA. pandeyj@musc.edu.

Classifications MeSH