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Synthetic control of actin polymerization and symmetry breaking in active protocells

Non-linear biomolecular interactions on the membranes drive membrane remodeling that underlies fundamental biological processes including chemotaxis, cytokinesis, and endocytosis. The multitude of biomolecules, the redundancy in their interactions, and the importance of spatiotemporal context in mem...

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Autores principales: Razavi, Shiva, Wong, Felix, Abubaker-Sharif, Bedri, Matsubayashi, Hideaki T., Nakamura, Hideki, Sandoval, Eduardo, Robinson, Douglas N., Chen, Baoyu, Liu, Jian, Iglesias, Pablo A., Inoue, Takanari
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542490/
https://www.ncbi.nlm.nih.gov/pubmed/37790449
http://dx.doi.org/10.1101/2023.09.22.559060
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author Razavi, Shiva
Wong, Felix
Abubaker-Sharif, Bedri
Matsubayashi, Hideaki T.
Nakamura, Hideki
Sandoval, Eduardo
Robinson, Douglas N.
Chen, Baoyu
Liu, Jian
Iglesias, Pablo A.
Inoue, Takanari
author_facet Razavi, Shiva
Wong, Felix
Abubaker-Sharif, Bedri
Matsubayashi, Hideaki T.
Nakamura, Hideki
Sandoval, Eduardo
Robinson, Douglas N.
Chen, Baoyu
Liu, Jian
Iglesias, Pablo A.
Inoue, Takanari
author_sort Razavi, Shiva
collection PubMed
description Non-linear biomolecular interactions on the membranes drive membrane remodeling that underlies fundamental biological processes including chemotaxis, cytokinesis, and endocytosis. The multitude of biomolecules, the redundancy in their interactions, and the importance of spatiotemporal context in membrane organization hampers understanding the physical principles governing membrane mechanics. A minimal, in vitro system that models the functional interactions between molecular signaling and membrane remodeling, while remaining faithful to cellular physiology and geometry is powerful yet remains unachieved. Here, inspired by the biophysical processes underpinning chemotaxis, we reconstituted externally-controlled actin polymerization inside giant unilamellar vesicles, guiding self-organization on the membrane. We show that applying undirected external chemical inputs to this system results in directed actin polymerization and membrane deformation that are uncorrelated with upstream biochemical cues, indicating symmetry breaking. A biophysical model of the dynamics and mechanics of both actin polymerization and membrane shape suggests that inhomogeneous distributions of actin generate membrane shape deformations in a non-linear fashion, a prediction consistent with experimental measurements and subsequent local perturbations. The active protocellular system demonstrates the interplay between actin dynamics and membrane shape in a symmetry breaking context that is relevant to chemotaxis and a suite of other biological processes.
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spelling pubmed-105424902023-10-03 Synthetic control of actin polymerization and symmetry breaking in active protocells Razavi, Shiva Wong, Felix Abubaker-Sharif, Bedri Matsubayashi, Hideaki T. Nakamura, Hideki Sandoval, Eduardo Robinson, Douglas N. Chen, Baoyu Liu, Jian Iglesias, Pablo A. Inoue, Takanari bioRxiv Article Non-linear biomolecular interactions on the membranes drive membrane remodeling that underlies fundamental biological processes including chemotaxis, cytokinesis, and endocytosis. The multitude of biomolecules, the redundancy in their interactions, and the importance of spatiotemporal context in membrane organization hampers understanding the physical principles governing membrane mechanics. A minimal, in vitro system that models the functional interactions between molecular signaling and membrane remodeling, while remaining faithful to cellular physiology and geometry is powerful yet remains unachieved. Here, inspired by the biophysical processes underpinning chemotaxis, we reconstituted externally-controlled actin polymerization inside giant unilamellar vesicles, guiding self-organization on the membrane. We show that applying undirected external chemical inputs to this system results in directed actin polymerization and membrane deformation that are uncorrelated with upstream biochemical cues, indicating symmetry breaking. A biophysical model of the dynamics and mechanics of both actin polymerization and membrane shape suggests that inhomogeneous distributions of actin generate membrane shape deformations in a non-linear fashion, a prediction consistent with experimental measurements and subsequent local perturbations. The active protocellular system demonstrates the interplay between actin dynamics and membrane shape in a symmetry breaking context that is relevant to chemotaxis and a suite of other biological processes. Cold Spring Harbor Laboratory 2023-09-23 /pmc/articles/PMC10542490/ /pubmed/37790449 http://dx.doi.org/10.1101/2023.09.22.559060 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Razavi, Shiva
Wong, Felix
Abubaker-Sharif, Bedri
Matsubayashi, Hideaki T.
Nakamura, Hideki
Sandoval, Eduardo
Robinson, Douglas N.
Chen, Baoyu
Liu, Jian
Iglesias, Pablo A.
Inoue, Takanari
Synthetic control of actin polymerization and symmetry breaking in active protocells
title Synthetic control of actin polymerization and symmetry breaking in active protocells
title_full Synthetic control of actin polymerization and symmetry breaking in active protocells
title_fullStr Synthetic control of actin polymerization and symmetry breaking in active protocells
title_full_unstemmed Synthetic control of actin polymerization and symmetry breaking in active protocells
title_short Synthetic control of actin polymerization and symmetry breaking in active protocells
title_sort synthetic control of actin polymerization and symmetry breaking in active protocells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542490/
https://www.ncbi.nlm.nih.gov/pubmed/37790449
http://dx.doi.org/10.1101/2023.09.22.559060
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