A dynamic partitioning mechanism polarizes membrane protein distribution

The plasma membrane is widely regarded as the hub of the numerous signal transduction activities. Yet, the fundamental biophysical mechanisms that spatiotemporally compartmentalize different classes of membrane proteins remain unclear. Using multimodal live-cell imaging, here we first show that seve...

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Autores principales: Banerjee, Tatsat, Matsuoka, Satomi, Biswas, Debojyoti, Miao, Yuchuan, Pal, Dhiman Sankar, Kamimura, Yoichiro, Ueda, Masahiro, Devreotes, Peter N., Iglesias, Pablo A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689845/
https://www.ncbi.nlm.nih.gov/pubmed/38036511
http://dx.doi.org/10.1038/s41467-023-43615-2
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author Banerjee, Tatsat
Matsuoka, Satomi
Biswas, Debojyoti
Miao, Yuchuan
Pal, Dhiman Sankar
Kamimura, Yoichiro
Ueda, Masahiro
Devreotes, Peter N.
Iglesias, Pablo A.
author_facet Banerjee, Tatsat
Matsuoka, Satomi
Biswas, Debojyoti
Miao, Yuchuan
Pal, Dhiman Sankar
Kamimura, Yoichiro
Ueda, Masahiro
Devreotes, Peter N.
Iglesias, Pablo A.
author_sort Banerjee, Tatsat
collection PubMed
description The plasma membrane is widely regarded as the hub of the numerous signal transduction activities. Yet, the fundamental biophysical mechanisms that spatiotemporally compartmentalize different classes of membrane proteins remain unclear. Using multimodal live-cell imaging, here we first show that several lipid-anchored membrane proteins are consistently depleted from the membrane regions where the Ras/PI3K/Akt/F-actin network is activated. The dynamic polarization of these proteins does not depend upon the F-actin-based cytoskeletal structures, recurring shuttling between membrane and cytosol, or directed vesicular trafficking. Photoconversion microscopy and single-molecule measurements demonstrate that these lipid-anchored molecules have substantially dissimilar diffusion profiles in different regions of the membrane which enable their selective segregation. When these diffusion coefficients are incorporated into an excitable network-based stochastic reaction-diffusion model, simulations reveal that the altered affinity mediated selective partitioning is sufficient to drive familiar propagating wave patterns. Furthermore, normally uniform integral and lipid-anchored membrane proteins partition successfully when membrane domain-specific peptides are optogenetically recruited to them. We propose “dynamic partitioning” as a new mechanism that can account for large-scale compartmentalization of a wide array of lipid-anchored and integral membrane proteins during various physiological processes where membrane polarizes.
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spelling pubmed-106898452023-12-02 A dynamic partitioning mechanism polarizes membrane protein distribution Banerjee, Tatsat Matsuoka, Satomi Biswas, Debojyoti Miao, Yuchuan Pal, Dhiman Sankar Kamimura, Yoichiro Ueda, Masahiro Devreotes, Peter N. Iglesias, Pablo A. Nat Commun Article The plasma membrane is widely regarded as the hub of the numerous signal transduction activities. Yet, the fundamental biophysical mechanisms that spatiotemporally compartmentalize different classes of membrane proteins remain unclear. Using multimodal live-cell imaging, here we first show that several lipid-anchored membrane proteins are consistently depleted from the membrane regions where the Ras/PI3K/Akt/F-actin network is activated. The dynamic polarization of these proteins does not depend upon the F-actin-based cytoskeletal structures, recurring shuttling between membrane and cytosol, or directed vesicular trafficking. Photoconversion microscopy and single-molecule measurements demonstrate that these lipid-anchored molecules have substantially dissimilar diffusion profiles in different regions of the membrane which enable their selective segregation. When these diffusion coefficients are incorporated into an excitable network-based stochastic reaction-diffusion model, simulations reveal that the altered affinity mediated selective partitioning is sufficient to drive familiar propagating wave patterns. Furthermore, normally uniform integral and lipid-anchored membrane proteins partition successfully when membrane domain-specific peptides are optogenetically recruited to them. We propose “dynamic partitioning” as a new mechanism that can account for large-scale compartmentalization of a wide array of lipid-anchored and integral membrane proteins during various physiological processes where membrane polarizes. Nature Publishing Group UK 2023-11-30 /pmc/articles/PMC10689845/ /pubmed/38036511 http://dx.doi.org/10.1038/s41467-023-43615-2 Text en © The Author(s) 2023 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
Banerjee, Tatsat
Matsuoka, Satomi
Biswas, Debojyoti
Miao, Yuchuan
Pal, Dhiman Sankar
Kamimura, Yoichiro
Ueda, Masahiro
Devreotes, Peter N.
Iglesias, Pablo A.
A dynamic partitioning mechanism polarizes membrane protein distribution
title A dynamic partitioning mechanism polarizes membrane protein distribution
title_full A dynamic partitioning mechanism polarizes membrane protein distribution
title_fullStr A dynamic partitioning mechanism polarizes membrane protein distribution
title_full_unstemmed A dynamic partitioning mechanism polarizes membrane protein distribution
title_short A dynamic partitioning mechanism polarizes membrane protein distribution
title_sort dynamic partitioning mechanism polarizes membrane protein distribution
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689845/
https://www.ncbi.nlm.nih.gov/pubmed/38036511
http://dx.doi.org/10.1038/s41467-023-43615-2
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