Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.

HIV-1 infection leads to chronic disease requiring life-long treatment and therefore alternative therapeutics, a cure and/or a protective vaccine are needed. Antibody-mediated effector functions could have a role in the fight against HIV-1. However, the properties underlying the potential beneficial...

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Main Authors: Marloes Grobben, Margreet Bakker, Angela I Schriek, Liesbeth J J Levels, Jeffrey C Umotoy, Khadija Tejjani, Mariëlle J van Breemen, Ryan N Lin, Steven W de Taeye, Gabriel Ozorowski, Neeltje A Kootstra, Andrew B Ward, Stephen J Kent, P Mark Hogarth, Bruce D Wines, Rogier W Sanders, Amy W Chung, Marit J van Gils
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-12-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012739
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author Marloes Grobben
Margreet Bakker
Angela I Schriek
Liesbeth J J Levels
Jeffrey C Umotoy
Khadija Tejjani
Mariëlle J van Breemen
Ryan N Lin
Steven W de Taeye
Gabriel Ozorowski
Neeltje A Kootstra
Andrew B Ward
Stephen J Kent
P Mark Hogarth
Bruce D Wines
Rogier W Sanders
Amy W Chung
Marit J van Gils
author_facet Marloes Grobben
Margreet Bakker
Angela I Schriek
Liesbeth J J Levels
Jeffrey C Umotoy
Khadija Tejjani
Mariëlle J van Breemen
Ryan N Lin
Steven W de Taeye
Gabriel Ozorowski
Neeltje A Kootstra
Andrew B Ward
Stephen J Kent
P Mark Hogarth
Bruce D Wines
Rogier W Sanders
Amy W Chung
Marit J van Gils
author_sort Marloes Grobben
collection DOAJ
description HIV-1 infection leads to chronic disease requiring life-long treatment and therefore alternative therapeutics, a cure and/or a protective vaccine are needed. Antibody-mediated effector functions could have a role in the fight against HIV-1. However, the properties underlying the potential beneficial effects of antibodies during HIV-1 infection are poorly understood. To identify a specific profile of antibody features associated with delayed disease progression, we studied antibody polyfunctionality during untreated HIV-1 infection in the well-documented Amsterdam Cohort Studies. Serum samples were analyzed from untreated individuals with HIV-1 at approximately 6 months (n = 166) and 3 years (n = 382) post-seroconversion (post-SC). A Luminex antibody Fc array was used to profile 15 different Fc features for serum antibodies against 20 different HIV-1 envelope glycoprotein antigens and the resulting data was also compared with data on neutralization breadth. We found that high HIV-1 specific IgG1 levels and low IgG2 and IgG4 levels at 3 years post-SC were associated with delayed disease progression. Moreover, delayed disease progression was associated with a broad and polyfunctional antibody response. Specifically, the capacity to interact with all Fc γ receptors (FcγRs) and C1q, and in particular with FcγRIIa, correlated positively with delayed disease progression. There were strong correlations between antibody Fc features and neutralization breadth and several antibody features that were associated with delayed disease progression were also associated with the development of broad and potent antibody neutralization. In summary, we identified a strong association between broad, polyfunctional antibodies and delayed disease progression. These findings contribute new information for the fight against HIV-1, especially for new antibody-based therapy and cure strategies.
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spelling doaj-art-b7fc8d66d7814d5bb991e391aaec82f32025-08-20T02:23:15ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742024-12-012012e101273910.1371/journal.ppat.1012739Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.Marloes GrobbenMargreet BakkerAngela I SchriekLiesbeth J J LevelsJeffrey C UmotoyKhadija TejjaniMariëlle J van BreemenRyan N LinSteven W de TaeyeGabriel OzorowskiNeeltje A KootstraAndrew B WardStephen J KentP Mark HogarthBruce D WinesRogier W SandersAmy W ChungMarit J van GilsHIV-1 infection leads to chronic disease requiring life-long treatment and therefore alternative therapeutics, a cure and/or a protective vaccine are needed. Antibody-mediated effector functions could have a role in the fight against HIV-1. However, the properties underlying the potential beneficial effects of antibodies during HIV-1 infection are poorly understood. To identify a specific profile of antibody features associated with delayed disease progression, we studied antibody polyfunctionality during untreated HIV-1 infection in the well-documented Amsterdam Cohort Studies. Serum samples were analyzed from untreated individuals with HIV-1 at approximately 6 months (n = 166) and 3 years (n = 382) post-seroconversion (post-SC). A Luminex antibody Fc array was used to profile 15 different Fc features for serum antibodies against 20 different HIV-1 envelope glycoprotein antigens and the resulting data was also compared with data on neutralization breadth. We found that high HIV-1 specific IgG1 levels and low IgG2 and IgG4 levels at 3 years post-SC were associated with delayed disease progression. Moreover, delayed disease progression was associated with a broad and polyfunctional antibody response. Specifically, the capacity to interact with all Fc γ receptors (FcγRs) and C1q, and in particular with FcγRIIa, correlated positively with delayed disease progression. There were strong correlations between antibody Fc features and neutralization breadth and several antibody features that were associated with delayed disease progression were also associated with the development of broad and potent antibody neutralization. In summary, we identified a strong association between broad, polyfunctional antibodies and delayed disease progression. These findings contribute new information for the fight against HIV-1, especially for new antibody-based therapy and cure strategies.https://doi.org/10.1371/journal.ppat.1012739
spellingShingle Marloes Grobben
Margreet Bakker
Angela I Schriek
Liesbeth J J Levels
Jeffrey C Umotoy
Khadija Tejjani
Mariëlle J van Breemen
Ryan N Lin
Steven W de Taeye
Gabriel Ozorowski
Neeltje A Kootstra
Andrew B Ward
Stephen J Kent
P Mark Hogarth
Bruce D Wines
Rogier W Sanders
Amy W Chung
Marit J van Gils
Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
PLoS Pathogens
title Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
title_full Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
title_fullStr Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
title_full_unstemmed Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
title_short Polyfunctionality and breadth of HIV-1 antibodies are associated with delayed disease progression.
title_sort polyfunctionality and breadth of hiv 1 antibodies are associated with delayed disease progression
url https://doi.org/10.1371/journal.ppat.1012739
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