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Long-term retention of antigens in germinal centres is controlled by the spatial organisation of the follicular dendritic cell network

View ORCID ProfileAna Martinez-Riano, Shenshen Wang, Stefan Boeing, Sophie Minoughan, Antonio Casal, View ORCID ProfileKatelyn M Spillane, View ORCID ProfileBurkhard Ludewig, View ORCID ProfilePavel Tolar
doi: https://doi.org/10.1101/2022.09.06.506650
Ana Martinez-Riano
1Immune Receptor Activation Laboratory, The Francis Crick Institute, London, UK
2Division of Infection and Immunity, Institute of Immunity and Transplantation, University College London, London, UK
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Shenshen Wang
3Department of Physics and Astronomy, University of California Los Angeles, Los Angeles, CA, USA
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Stefan Boeing
4Bioinformatics and Biostatistics Science Technology Platform, The Francis Crick Institute, UK
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Sophie Minoughan
2Division of Infection and Immunity, Institute of Immunity and Transplantation, University College London, London, UK
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Antonio Casal
2Division of Infection and Immunity, Institute of Immunity and Transplantation, University College London, London, UK
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Katelyn M Spillane
5Department of Physics, King’s College London, London, UK
6Randall Centre for Cell and Molecular Biophysics, King’s College London, UK
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Burkhard Ludewig
7Institute of Immunobiology, Medical Research Center, Kantonsspital St. Gallen, St. Gallen, Switzerland
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Pavel Tolar
1Immune Receptor Activation Laboratory, The Francis Crick Institute, London, UK
2Division of Infection and Immunity, Institute of Immunity and Transplantation, University College London, London, UK
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ABSTRACT

Germinal centers (GCs) require sustained availability of antigens to promote antibody affinity maturation against pathogens and vaccines. A key source of antigens for GC B cells are immune complexes (ICs) displayed on follicular dendritic cells (FDCs). Here we show that FDC spatial organization regulates antigen dynamics in the GC. We show the existence of two light zone (LZ) FDC populations, which differ in the duration of antigen retention. While the entire light zone (LZ) FDC network captures ICs initially, only the central cells of the network function as a long-term antigen reservoir, where different antigens arriving from subsequent immunizations co-localize. Mechanistically, central FDCs constitutively express subtly higher CR2 membrane densities than peripheral FDCs, which strongly increases the IC retention half-life. Even though repeated immunizations gradually saturate central FDCs, B cell responses remain efficient because new antigens partially displace old ones. These results reveal the principles shaping antigen display on FDCs during the GC reaction.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted September 07, 2022.
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Long-term retention of antigens in germinal centres is controlled by the spatial organisation of the follicular dendritic cell network
Ana Martinez-Riano, Shenshen Wang, Stefan Boeing, Sophie Minoughan, Antonio Casal, Katelyn M Spillane, Burkhard Ludewig, Pavel Tolar
bioRxiv 2022.09.06.506650; doi: https://doi.org/10.1101/2022.09.06.506650
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Long-term retention of antigens in germinal centres is controlled by the spatial organisation of the follicular dendritic cell network
Ana Martinez-Riano, Shenshen Wang, Stefan Boeing, Sophie Minoughan, Antonio Casal, Katelyn M Spillane, Burkhard Ludewig, Pavel Tolar
bioRxiv 2022.09.06.506650; doi: https://doi.org/10.1101/2022.09.06.506650

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