Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections

Abstract Background Immunoglobulin G (IgG) antibodies are thought to play important roles in the protection against Plasmodium falciparum (P. falciparum) malaria. A longitudinal cohort study performed in the Southern part of Benin, identified a group of infants who were able to control asymptomatic...

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Main Authors: Abdou Khadre Dit Jadir Fall, Ikhlaq Hussain Kana, Célia Dechavanne, Asier Garcia-Senosiain, Evelyne Guitard, Jacqueline Milet, Achille Massougbodji, André Garcia, Jean-Michel Dugoujon, Florence Migot-Nabias, Michael Theisen, David Courtin
Format: Article
Language:English
Published: BMC 2022-11-01
Series:Malaria Journal
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Online Access:https://doi.org/10.1186/s12936-022-04361-w
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author Abdou Khadre Dit Jadir Fall
Ikhlaq Hussain Kana
Célia Dechavanne
Asier Garcia-Senosiain
Evelyne Guitard
Jacqueline Milet
Achille Massougbodji
André Garcia
Jean-Michel Dugoujon
Florence Migot-Nabias
Michael Theisen
David Courtin
author_facet Abdou Khadre Dit Jadir Fall
Ikhlaq Hussain Kana
Célia Dechavanne
Asier Garcia-Senosiain
Evelyne Guitard
Jacqueline Milet
Achille Massougbodji
André Garcia
Jean-Michel Dugoujon
Florence Migot-Nabias
Michael Theisen
David Courtin
author_sort Abdou Khadre Dit Jadir Fall
collection DOAJ
description Abstract Background Immunoglobulin G (IgG) antibodies are thought to play important roles in the protection against Plasmodium falciparum (P. falciparum) malaria. A longitudinal cohort study performed in the Southern part of Benin, identified a group of infants who were able to control asymptomatic malaria infections (CAIG). Methods IgG antibodies against distinct merozoite antigens were quantified in plasma from Beninese infants. Functionality of these antibodies was assessed by the merozoite-phagocytosis assay using THP-1 cells and primary neutrophils as effector cells. Gm allotypes were determined by a serological method of haemagglutination inhibition. Results Purified IgG from infants in CAIG promoted higher levels of merozoite-phagocytosis than did IgG from children who were unable to control asymptomatic infections (Ologit multivariate regression model, Coef. = 0.06, 95% CI 0.02;0.10, P = 0.002). High level of merozoite-phagocytosis activity was significantly associated with high levels of IgG against AMA1 (Coef. = 1.76, 95% CI 0.39;3.14, P = 0.012) and GLURP-R2 (Coef. = 12.24, 95% CI 1.35;23.12, P = 0.028). Moreover, infants of the G3m5,6,10,11,13,14,24 phenotype showed higher merozoite-phagocytosis activity (Generalized linear model multivariate regression, Coef. = 7.46, 95% CI 0.31;14.61, P = 0.041) than those presenting other G3m phenotypes. Conclusion The results of the present study confirm the importance of antibodies to merozoite surface antigens in the control of asymptomatic malaria infection in Beninese infants. The study also demonstrated that G3m phenotypes impact the functional activity of IgG. This last point could have a considerable impact in the research of candidate vaccines against malaria parasites or other pathogens.
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spelling doaj.art-d9dfe845b1164b9fa258f8b5d83b4ba72022-12-22T03:48:27ZengBMCMalaria Journal1475-28752022-11-0121111510.1186/s12936-022-04361-wNaturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infectionsAbdou Khadre Dit Jadir Fall0Ikhlaq Hussain Kana1Célia Dechavanne2Asier Garcia-Senosiain3Evelyne Guitard4Jacqueline Milet5Achille Massougbodji6André Garcia7Jean-Michel Dugoujon8Florence Migot-Nabias9Michael Theisen10David Courtin11Université Paris Cité, IRD, MERITDepartment for Congenital Disorders, Statens Serum InstitutUniversité Paris Cité, IRD, MERITDepartment for Congenital Disorders, Statens Serum InstitutLaboratoire d’Anthropologie Moléculaire et Imagerie de Synthèse, UMR 5288, Université Paul Sabatier Toulouse IIIUniversité Paris Cité, IRD, MERITCentre d’Etude et de Recherche sur les Pathologies Associées à la Grossesse et à l’EnfanceUniversité Paris Cité, IRD, MERITLaboratoire d’Anthropologie Moléculaire et Imagerie de Synthèse, UMR 5288, Université Paul Sabatier Toulouse IIIUniversité Paris Cité, IRD, MERITDepartment for Congenital Disorders, Statens Serum InstitutUniversité Paris Cité, IRD, MERITAbstract Background Immunoglobulin G (IgG) antibodies are thought to play important roles in the protection against Plasmodium falciparum (P. falciparum) malaria. A longitudinal cohort study performed in the Southern part of Benin, identified a group of infants who were able to control asymptomatic malaria infections (CAIG). Methods IgG antibodies against distinct merozoite antigens were quantified in plasma from Beninese infants. Functionality of these antibodies was assessed by the merozoite-phagocytosis assay using THP-1 cells and primary neutrophils as effector cells. Gm allotypes were determined by a serological method of haemagglutination inhibition. Results Purified IgG from infants in CAIG promoted higher levels of merozoite-phagocytosis than did IgG from children who were unable to control asymptomatic infections (Ologit multivariate regression model, Coef. = 0.06, 95% CI 0.02;0.10, P = 0.002). High level of merozoite-phagocytosis activity was significantly associated with high levels of IgG against AMA1 (Coef. = 1.76, 95% CI 0.39;3.14, P = 0.012) and GLURP-R2 (Coef. = 12.24, 95% CI 1.35;23.12, P = 0.028). Moreover, infants of the G3m5,6,10,11,13,14,24 phenotype showed higher merozoite-phagocytosis activity (Generalized linear model multivariate regression, Coef. = 7.46, 95% CI 0.31;14.61, P = 0.041) than those presenting other G3m phenotypes. Conclusion The results of the present study confirm the importance of antibodies to merozoite surface antigens in the control of asymptomatic malaria infection in Beninese infants. The study also demonstrated that G3m phenotypes impact the functional activity of IgG. This last point could have a considerable impact in the research of candidate vaccines against malaria parasites or other pathogens.https://doi.org/10.1186/s12936-022-04361-wIgGGm allotypesOpsonic phagocytosisControl of asymptomatic malaria infectionBenin
spellingShingle Abdou Khadre Dit Jadir Fall
Ikhlaq Hussain Kana
Célia Dechavanne
Asier Garcia-Senosiain
Evelyne Guitard
Jacqueline Milet
Achille Massougbodji
André Garcia
Jean-Michel Dugoujon
Florence Migot-Nabias
Michael Theisen
David Courtin
Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
Malaria Journal
IgG
Gm allotypes
Opsonic phagocytosis
Control of asymptomatic malaria infection
Benin
title Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
title_full Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
title_fullStr Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
title_full_unstemmed Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
title_short Naturally acquired antibodies from Beninese infants promote Plasmodium falciparum merozoite-phagocytosis by human blood leukocytes: implications for control of asymptomatic malaria infections
title_sort naturally acquired antibodies from beninese infants promote plasmodium falciparum merozoite phagocytosis by human blood leukocytes implications for control of asymptomatic malaria infections
topic IgG
Gm allotypes
Opsonic phagocytosis
Control of asymptomatic malaria infection
Benin
url https://doi.org/10.1186/s12936-022-04361-w
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