Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers

Summary: Germinal centers (GCs) are sites where plasma and memory B cells form to generate high-affinity, Ig class-switched antibodies. Specialized stromal cells called follicular dendritic cells (FDCs) are essential for GC formation. During systemic Salmonella Typhimurium (STm) infection GCs are ab...

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Main Authors: Edith Marcial-Juárez, Marisol Pérez-Toledo, Saba Nayar, Elena Pipi, Areej Alshayea, Ruby Persaud, Sian E. Jossi, Rachel Lamerton, Francesca Barone, Ian R. Henderson, Adam F. Cunningham
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004223003875
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author Edith Marcial-Juárez
Marisol Pérez-Toledo
Saba Nayar
Elena Pipi
Areej Alshayea
Ruby Persaud
Sian E. Jossi
Rachel Lamerton
Francesca Barone
Ian R. Henderson
Adam F. Cunningham
author_facet Edith Marcial-Juárez
Marisol Pérez-Toledo
Saba Nayar
Elena Pipi
Areej Alshayea
Ruby Persaud
Sian E. Jossi
Rachel Lamerton
Francesca Barone
Ian R. Henderson
Adam F. Cunningham
author_sort Edith Marcial-Juárez
collection DOAJ
description Summary: Germinal centers (GCs) are sites where plasma and memory B cells form to generate high-affinity, Ig class-switched antibodies. Specialized stromal cells called follicular dendritic cells (FDCs) are essential for GC formation. During systemic Salmonella Typhimurium (STm) infection GCs are absent, whereas extensive extrafollicular and switched antibody responses are maintained. The mechanisms that underpin the absence of GC formation are incompletely understood. Here, we demonstrate that STm induces a reversible disruption of niches within the splenic microenvironment, including the T and B cell compartments and the marginal zone. Alongside these effects after infection, mature FDC networks are strikingly absent, whereas immature FDC precursors, including marginal sinus pre-FDCs (MadCAM-1+) and perivascular pre-FDCs (PDGFRβ+) are enriched. As normal FDC networks re-establish, extensive GCs become detectable throughout the spleen. Therefore, the reorganization of FDC networks and the loss of GC responses are key, parallel features of systemic STm infections.
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spelling doaj.art-66b78e952b064cdaa6f3dbdd10691c6c2023-03-16T05:06:00ZengElsevieriScience2589-00422023-04-01264106310Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centersEdith Marcial-Juárez0Marisol Pérez-Toledo1Saba Nayar2Elena Pipi3Areej Alshayea4Ruby Persaud5Sian E. Jossi6Rachel Lamerton7Francesca Barone8Ian R. Henderson9Adam F. Cunningham10Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United Kingdom; Corresponding authorInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomRheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomRheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United KingdomRheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, West Midlands, B15 2TT, United Kingdom; National Institute for Health Research (NIHR) Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, UK and Sandwell and West Birmingham Trust, Birmingham, West Midlands, B15 2TH, United KingdomInstitute for Molecular Bioscience, University of Queensland, Brisbane, QLD4072, AustraliaInstitute of Immunology and Immunotherapy, University of Birmingham, Birmingham, West Midlands, B15 2TT, United Kingdom; Corresponding authorSummary: Germinal centers (GCs) are sites where plasma and memory B cells form to generate high-affinity, Ig class-switched antibodies. Specialized stromal cells called follicular dendritic cells (FDCs) are essential for GC formation. During systemic Salmonella Typhimurium (STm) infection GCs are absent, whereas extensive extrafollicular and switched antibody responses are maintained. The mechanisms that underpin the absence of GC formation are incompletely understood. Here, we demonstrate that STm induces a reversible disruption of niches within the splenic microenvironment, including the T and B cell compartments and the marginal zone. Alongside these effects after infection, mature FDC networks are strikingly absent, whereas immature FDC precursors, including marginal sinus pre-FDCs (MadCAM-1+) and perivascular pre-FDCs (PDGFRβ+) are enriched. As normal FDC networks re-establish, extensive GCs become detectable throughout the spleen. Therefore, the reorganization of FDC networks and the loss of GC responses are key, parallel features of systemic STm infections.http://www.sciencedirect.com/science/article/pii/S2589004223003875ImmunologyImmune responseComponents of the immune systemMicrobiologyCell biology
spellingShingle Edith Marcial-Juárez
Marisol Pérez-Toledo
Saba Nayar
Elena Pipi
Areej Alshayea
Ruby Persaud
Sian E. Jossi
Rachel Lamerton
Francesca Barone
Ian R. Henderson
Adam F. Cunningham
Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
iScience
Immunology
Immune response
Components of the immune system
Microbiology
Cell biology
title Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
title_full Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
title_fullStr Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
title_full_unstemmed Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
title_short Salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
title_sort salmonella infection induces the reorganization of follicular dendritic cell networks concomitant with the failure to generate germinal centers
topic Immunology
Immune response
Components of the immune system
Microbiology
Cell biology
url http://www.sciencedirect.com/science/article/pii/S2589004223003875
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