Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.

The polyclonal, T-dependent nature of hypergammaglobulinemia during murine infection with LCMV is well defined, however the mechanism by which polyclonal B cells acquire antigens for presentation remains unknown. Here we use LCMV-specific CD4 + transgenic T cells to explore several hypotheses for B...

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Main Authors: Gabriel Chamberlain, Guillaume L Lopez, Léa Bourguignon, Xavier Laulhé, Yasmine Adda-Bouchard, Tania Charpentier, Rebekah Honce, Jason W Botten, Alain Lamarre
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-07-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1013345
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author Gabriel Chamberlain
Guillaume L Lopez
Léa Bourguignon
Xavier Laulhé
Yasmine Adda-Bouchard
Tania Charpentier
Rebekah Honce
Jason W Botten
Alain Lamarre
author_facet Gabriel Chamberlain
Guillaume L Lopez
Léa Bourguignon
Xavier Laulhé
Yasmine Adda-Bouchard
Tania Charpentier
Rebekah Honce
Jason W Botten
Alain Lamarre
author_sort Gabriel Chamberlain
collection DOAJ
description The polyclonal, T-dependent nature of hypergammaglobulinemia during murine infection with LCMV is well defined, however the mechanism by which polyclonal B cells acquire antigens for presentation remains unknown. Here we use LCMV-specific CD4 + transgenic T cells to explore several hypotheses for B cell antigen uptake. We found that antigens produced by cells infected with LCMV in vitro are available to polyclonal B cells and their presentation to CD4+ T cells enabled robust co-activation. The in vitro nature of our model demonstrates that in vivo factors such as cytokine milieu and antigen release by NK/CD8+ are not required. We show that non-replicative UVC-irradiated LCMV enables antigen access to B cells, thus productive infection of B cells is not required for antigen acquisition. B cells loaded with LCMV antigens in vitro can efficiently present these antigens to CD4+ T cells in LCMV-infected mice, thereby validating our model in vivo. Using transmission electron microscopy we identified LCMV-GP bearing particles of various sizes including <50nm, a size accessible to B cells via pinocytosis. The particles morphologically resemble exosomes or viral particles (infective or defective interfering). We show that polyclonal B cell access to Ag is maintained when exosome release or viral defective interfering particle release is inhibited. Finally, we used a monovalent Fab derived from the LCMV-neutralizing antibody KL25 to show that access to the viral GP1 protein is important in order for polyclonal B cells to efficiently acquire LCMV antigen for presentation, suggesting the presence of a GP1 receptor on B cells.
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institution Kabale University
issn 1553-7366
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language English
publishDate 2025-07-01
publisher Public Library of Science (PLoS)
record_format Article
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spelling doaj-art-1e5033d0a5fd4225ba3fb9dd239604bd2025-08-20T03:27:28ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-07-01217e101334510.1371/journal.ppat.1013345Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.Gabriel ChamberlainGuillaume L LopezLéa BourguignonXavier LaulhéYasmine Adda-BouchardTania CharpentierRebekah HonceJason W BottenAlain LamarreThe polyclonal, T-dependent nature of hypergammaglobulinemia during murine infection with LCMV is well defined, however the mechanism by which polyclonal B cells acquire antigens for presentation remains unknown. Here we use LCMV-specific CD4 + transgenic T cells to explore several hypotheses for B cell antigen uptake. We found that antigens produced by cells infected with LCMV in vitro are available to polyclonal B cells and their presentation to CD4+ T cells enabled robust co-activation. The in vitro nature of our model demonstrates that in vivo factors such as cytokine milieu and antigen release by NK/CD8+ are not required. We show that non-replicative UVC-irradiated LCMV enables antigen access to B cells, thus productive infection of B cells is not required for antigen acquisition. B cells loaded with LCMV antigens in vitro can efficiently present these antigens to CD4+ T cells in LCMV-infected mice, thereby validating our model in vivo. Using transmission electron microscopy we identified LCMV-GP bearing particles of various sizes including <50nm, a size accessible to B cells via pinocytosis. The particles morphologically resemble exosomes or viral particles (infective or defective interfering). We show that polyclonal B cell access to Ag is maintained when exosome release or viral defective interfering particle release is inhibited. Finally, we used a monovalent Fab derived from the LCMV-neutralizing antibody KL25 to show that access to the viral GP1 protein is important in order for polyclonal B cells to efficiently acquire LCMV antigen for presentation, suggesting the presence of a GP1 receptor on B cells.https://doi.org/10.1371/journal.ppat.1013345
spellingShingle Gabriel Chamberlain
Guillaume L Lopez
Léa Bourguignon
Xavier Laulhé
Yasmine Adda-Bouchard
Tania Charpentier
Rebekah Honce
Jason W Botten
Alain Lamarre
Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
PLoS Pathogens
title Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
title_full Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
title_fullStr Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
title_full_unstemmed Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
title_short Polyclonal B cells acquire LCMV antigens in a GP1-dependent manner.
title_sort polyclonal b cells acquire lcmv antigens in a gp1 dependent manner
url https://doi.org/10.1371/journal.ppat.1013345
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