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Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations

The interaction between TNFα and TNFR1 is essential in maintaining tissue development and immune responses. While TNFR1 is a cell surface receptor, TNFα exists in both soluble and membrane-bound forms. Interestingly, it was found that the activation of TNFR1-mediated signaling pathways is preferenti...

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Autores principales: Su, Zhaoqian, Dhusia, Kalyani, Wu, Yinghao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8917213/
https://www.ncbi.nlm.nih.gov/pubmed/35277586
http://dx.doi.org/10.1038/s42003-022-03179-1
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author Su, Zhaoqian
Dhusia, Kalyani
Wu, Yinghao
author_facet Su, Zhaoqian
Dhusia, Kalyani
Wu, Yinghao
author_sort Su, Zhaoqian
collection PubMed
description The interaction between TNFα and TNFR1 is essential in maintaining tissue development and immune responses. While TNFR1 is a cell surface receptor, TNFα exists in both soluble and membrane-bound forms. Interestingly, it was found that the activation of TNFR1-mediated signaling pathways is preferentially through the soluble form of TNFα, which can also induce the clustering of TNFR1 on plasma membrane of living cells. We developed a multiscale simulation framework to compare receptor clustering induced by soluble and membrane-bound ligands. Comparing with the freely diffusive soluble ligands, we hypothesize that the conformational dynamics of membrane-bound ligands are restricted, which affects the clustering of ligand-receptor complexes at cell-cell interfaces. Our simulation revealed that only small clusters can form if TNFα is bound on cell surface. In contrast, the clustering triggered by soluble TNFα is more dynamic, and the size of clusters is statistically larger. We therefore demonstrated the impact of membrane-bound ligand on dynamics of receptor clustering. Moreover, considering that larger TNFα-TNFR1 clusters is more likely to provide spatial platform for downstream signaling pathway, our studies offer new mechanistic insights about why the activation of TNFR1-mediated signaling pathways is not preferred by membrane-bound form of TNFα.
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spelling pubmed-89172132022-03-30 Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations Su, Zhaoqian Dhusia, Kalyani Wu, Yinghao Commun Biol Article The interaction between TNFα and TNFR1 is essential in maintaining tissue development and immune responses. While TNFR1 is a cell surface receptor, TNFα exists in both soluble and membrane-bound forms. Interestingly, it was found that the activation of TNFR1-mediated signaling pathways is preferentially through the soluble form of TNFα, which can also induce the clustering of TNFR1 on plasma membrane of living cells. We developed a multiscale simulation framework to compare receptor clustering induced by soluble and membrane-bound ligands. Comparing with the freely diffusive soluble ligands, we hypothesize that the conformational dynamics of membrane-bound ligands are restricted, which affects the clustering of ligand-receptor complexes at cell-cell interfaces. Our simulation revealed that only small clusters can form if TNFα is bound on cell surface. In contrast, the clustering triggered by soluble TNFα is more dynamic, and the size of clusters is statistically larger. We therefore demonstrated the impact of membrane-bound ligand on dynamics of receptor clustering. Moreover, considering that larger TNFα-TNFR1 clusters is more likely to provide spatial platform for downstream signaling pathway, our studies offer new mechanistic insights about why the activation of TNFR1-mediated signaling pathways is not preferred by membrane-bound form of TNFα. Nature Publishing Group UK 2022-03-11 /pmc/articles/PMC8917213/ /pubmed/35277586 http://dx.doi.org/10.1038/s42003-022-03179-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Su, Zhaoqian
Dhusia, Kalyani
Wu, Yinghao
Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title_full Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title_fullStr Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title_full_unstemmed Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title_short Understanding the functional role of membrane confinements in TNF-mediated signaling by multiscale simulations
title_sort understanding the functional role of membrane confinements in tnf-mediated signaling by multiscale simulations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8917213/
https://www.ncbi.nlm.nih.gov/pubmed/35277586
http://dx.doi.org/10.1038/s42003-022-03179-1
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