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A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens

Aggregation of cell surface receptor proteins by multivalent antigens is an essential early step for immune cell signalling. A number of experimental and modelling studies in the past have investigated multivalent ligand-mediated aggregation of IgE receptors (FcɛRI) in the plasma membrane of mast ce...

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Autores principales: Shahinuzzaman, Md, Khetan, Jawahar, Barua, Dipak
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170560/
https://www.ncbi.nlm.nih.gov/pubmed/30839725
http://dx.doi.org/10.1098/rsos.180190
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author Shahinuzzaman, Md
Khetan, Jawahar
Barua, Dipak
author_facet Shahinuzzaman, Md
Khetan, Jawahar
Barua, Dipak
author_sort Shahinuzzaman, Md
collection PubMed
description Aggregation of cell surface receptor proteins by multivalent antigens is an essential early step for immune cell signalling. A number of experimental and modelling studies in the past have investigated multivalent ligand-mediated aggregation of IgE receptors (FcɛRI) in the plasma membrane of mast cells. However, understanding of the mechanisms of FcɛRI aggregation remains incomplete. Experimental reports indicate that FcɛRI forms relatively small and finite-sized clusters when stimulated by a multivalent ligand. By contrast, modelling studies have shown that receptor cross-linking by a trivalent ligand may lead to the formation of large receptor superaggregates that may potentially give rise to hyperactive cellular responses. In this work, we have developed a Brownian dynamics-based spatio-temporal model to analyse FcɛRI aggregation by a trivalent antigen. Unlike the existing models, which implemented non-spatial simulation approaches, our model explicitly accounts for the coarse-grained site-specific features of the multivalent species (molecules and complexes). The model incorporates membrane diffusion, steric collisions and sub-nanometre-scale site-specific interaction of the time-evolving species of arbitrary structures. Using the model, we investigated temporal evolution of the species and their diffusivities. Consistent with a recent experimental report, our model predicted sharp decay in species mobility in the plasma membrane in response receptor cross-linking by a multivalent antigen. We show that, due to such decay in the species mobility, post-stimulation receptor aggregation may become self-limiting. Our analysis reveals a potential regulatory mechanism suppressing hyperactivation of immune cells in response to multivalent antigens.
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spelling pubmed-61705602018-10-18 A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens Shahinuzzaman, Md Khetan, Jawahar Barua, Dipak R Soc Open Sci Cellular and Molecular Biology Aggregation of cell surface receptor proteins by multivalent antigens is an essential early step for immune cell signalling. A number of experimental and modelling studies in the past have investigated multivalent ligand-mediated aggregation of IgE receptors (FcɛRI) in the plasma membrane of mast cells. However, understanding of the mechanisms of FcɛRI aggregation remains incomplete. Experimental reports indicate that FcɛRI forms relatively small and finite-sized clusters when stimulated by a multivalent ligand. By contrast, modelling studies have shown that receptor cross-linking by a trivalent ligand may lead to the formation of large receptor superaggregates that may potentially give rise to hyperactive cellular responses. In this work, we have developed a Brownian dynamics-based spatio-temporal model to analyse FcɛRI aggregation by a trivalent antigen. Unlike the existing models, which implemented non-spatial simulation approaches, our model explicitly accounts for the coarse-grained site-specific features of the multivalent species (molecules and complexes). The model incorporates membrane diffusion, steric collisions and sub-nanometre-scale site-specific interaction of the time-evolving species of arbitrary structures. Using the model, we investigated temporal evolution of the species and their diffusivities. Consistent with a recent experimental report, our model predicted sharp decay in species mobility in the plasma membrane in response receptor cross-linking by a multivalent antigen. We show that, due to such decay in the species mobility, post-stimulation receptor aggregation may become self-limiting. Our analysis reveals a potential regulatory mechanism suppressing hyperactivation of immune cells in response to multivalent antigens. The Royal Society 2018-09-26 /pmc/articles/PMC6170560/ /pubmed/30839725 http://dx.doi.org/10.1098/rsos.180190 Text en © 2018 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Cellular and Molecular Biology
Shahinuzzaman, Md
Khetan, Jawahar
Barua, Dipak
A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title_full A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title_fullStr A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title_full_unstemmed A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title_short A spatio-temporal model reveals self-limiting FcɛRI cross-linking by multivalent antigens
title_sort spatio-temporal model reveals self-limiting fcɛri cross-linking by multivalent antigens
topic Cellular and Molecular Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170560/
https://www.ncbi.nlm.nih.gov/pubmed/30839725
http://dx.doi.org/10.1098/rsos.180190
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