B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments

Antibody production depends on B cell internalization and presentation of antigens to helper T cells. To acquire antigens displayed by antigen-presenting cells, B cells form immune synapses and extract antigens by the mechanical activity of the acto-myosin cytoskeleton. While cytoskeleton organizati...

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Main Authors: Sophie I Roper, Laabiah Wasim, Dessislava Malinova, Michael Way, Susan Cox, Pavel Tolar
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/48093
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spelling doaj-80a5204862284d08adc409cfd600e3382021-05-05T18:09:52ZengeLife Sciences Publications LtdeLife2050-084X2019-12-01810.7554/eLife.48093B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filamentsSophie I Roper0https://orcid.org/0000-0001-7776-7670Laabiah Wasim1Dessislava Malinova2Michael Way3https://orcid.org/0000-0001-7207-2722Susan Cox4Pavel Tolar5https://orcid.org/0000-0003-4693-7299Immune Receptor Activation Laboratory, The Francis Crick Institute, London, United KingdomImmune Receptor Activation Laboratory, The Francis Crick Institute, London, United KingdomImmune Receptor Activation Laboratory, The Francis Crick Institute, London, United Kingdom; Division of Immunology and Inflammation, Department of Medicine, Imperial College London, London, United KingdomCellular Signalling and Cytoskeletal Function Laboratory, The Francis Crick Institute, London, United KingdomRandall Centre for Cell and Molecular Biophysics, King’s College London, London, United KingdomImmune Receptor Activation Laboratory, The Francis Crick Institute, London, United Kingdom; Division of Immunology and Inflammation, Department of Medicine, Imperial College London, London, United KingdomAntibody production depends on B cell internalization and presentation of antigens to helper T cells. To acquire antigens displayed by antigen-presenting cells, B cells form immune synapses and extract antigens by the mechanical activity of the acto-myosin cytoskeleton. While cytoskeleton organization driving the initial formation of the B cell synapse has been studied, how the cytoskeleton supports antigen extraction remains poorly understood. Here we show that after initial cell spreading, F-actin in synapses of primary mouse B cells and human B cell lines forms a highly dynamic pattern composed of actin foci interspersed with linear filaments and myosin IIa. The foci are generated by Arp2/3-mediated branched-actin polymerization and stochastically associate with antigen clusters to mediate internalization. However, antigen extraction also requires the activity of formins, which reside near the foci and produce the interspersed filaments. Thus, a cooperation of branched-actin foci supported by linear filaments underlies B cell mechanics during antigen extraction.https://elifesciences.org/articles/48093B cellimmune synapseantigenendocytosisactin cytoskeletonB cell receptor
collection DOAJ
language English
format Article
sources DOAJ
author Sophie I Roper
Laabiah Wasim
Dessislava Malinova
Michael Way
Susan Cox
Pavel Tolar
spellingShingle Sophie I Roper
Laabiah Wasim
Dessislava Malinova
Michael Way
Susan Cox
Pavel Tolar
B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
eLife
B cell
immune synapse
antigen
endocytosis
actin cytoskeleton
B cell receptor
author_facet Sophie I Roper
Laabiah Wasim
Dessislava Malinova
Michael Way
Susan Cox
Pavel Tolar
author_sort Sophie I Roper
title B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
title_short B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
title_full B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
title_fullStr B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
title_full_unstemmed B cells extract antigens at Arp2/3-generated actin foci interspersed with linear filaments
title_sort b cells extract antigens at arp2/3-generated actin foci interspersed with linear filaments
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-12-01
description Antibody production depends on B cell internalization and presentation of antigens to helper T cells. To acquire antigens displayed by antigen-presenting cells, B cells form immune synapses and extract antigens by the mechanical activity of the acto-myosin cytoskeleton. While cytoskeleton organization driving the initial formation of the B cell synapse has been studied, how the cytoskeleton supports antigen extraction remains poorly understood. Here we show that after initial cell spreading, F-actin in synapses of primary mouse B cells and human B cell lines forms a highly dynamic pattern composed of actin foci interspersed with linear filaments and myosin IIa. The foci are generated by Arp2/3-mediated branched-actin polymerization and stochastically associate with antigen clusters to mediate internalization. However, antigen extraction also requires the activity of formins, which reside near the foci and produce the interspersed filaments. Thus, a cooperation of branched-actin foci supported by linear filaments underlies B cell mechanics during antigen extraction.
topic B cell
immune synapse
antigen
endocytosis
actin cytoskeleton
B cell receptor
url https://elifesciences.org/articles/48093
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AT dessislavamalinova bcellsextractantigensatarp23generatedactinfociinterspersedwithlinearfilaments
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