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Chemophoresis engine: A general mechanism of ATPase-driven cargo transport

Cell polarity regulates the orientation of the cytoskeleton members that directs intracellular transport for cargo-like organelles, using chemical gradients sustained by ATP or GTP hydrolysis. However, how cargo transports are directly mediated by chemical gradients remains unknown. We previously pr...

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Detalles Bibliográficos
Autores principales: Sugawara, Takeshi, Kaneko, Kunihiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9363008/
https://www.ncbi.nlm.nih.gov/pubmed/35877681
http://dx.doi.org/10.1371/journal.pcbi.1010324
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author Sugawara, Takeshi
Kaneko, Kunihiko
author_facet Sugawara, Takeshi
Kaneko, Kunihiko
author_sort Sugawara, Takeshi
collection PubMed
description Cell polarity regulates the orientation of the cytoskeleton members that directs intracellular transport for cargo-like organelles, using chemical gradients sustained by ATP or GTP hydrolysis. However, how cargo transports are directly mediated by chemical gradients remains unknown. We previously proposed a physical mechanism that enables directed movement of cargos, referred to as chemophoresis. According to the mechanism, a cargo with reaction sites is subjected to a chemophoresis force in the direction of the increased concentration. Based on this, we introduce an extended model, the chemophoresis engine, as a general mechanism of cargo motion, which transforms chemical free energy into directed motion through the catalytic ATP hydrolysis. We applied the engine to plasmid motion in a ParABS system to demonstrate the self-organization system for directed plasmid movement and pattern dynamics of ParA-ATP concentration, thereby explaining plasmid equi-positioning and pole-to-pole oscillation observed in bacterial cells and in vitro experiments. We mathematically show the existence and stability of the plasmid-surfing pattern, which allows the cargo-directed motion through the symmetry-breaking transition of the ParA-ATP spatiotemporal pattern. We also quantitatively demonstrate that the chemophoresis engine can work even under in vivo conditions. Finally, we discuss the chemophoresis engine as one of the general mechanisms of hydrolysis-driven intracellular transport.
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spelling pubmed-93630082022-08-10 Chemophoresis engine: A general mechanism of ATPase-driven cargo transport Sugawara, Takeshi Kaneko, Kunihiko PLoS Comput Biol Research Article Cell polarity regulates the orientation of the cytoskeleton members that directs intracellular transport for cargo-like organelles, using chemical gradients sustained by ATP or GTP hydrolysis. However, how cargo transports are directly mediated by chemical gradients remains unknown. We previously proposed a physical mechanism that enables directed movement of cargos, referred to as chemophoresis. According to the mechanism, a cargo with reaction sites is subjected to a chemophoresis force in the direction of the increased concentration. Based on this, we introduce an extended model, the chemophoresis engine, as a general mechanism of cargo motion, which transforms chemical free energy into directed motion through the catalytic ATP hydrolysis. We applied the engine to plasmid motion in a ParABS system to demonstrate the self-organization system for directed plasmid movement and pattern dynamics of ParA-ATP concentration, thereby explaining plasmid equi-positioning and pole-to-pole oscillation observed in bacterial cells and in vitro experiments. We mathematically show the existence and stability of the plasmid-surfing pattern, which allows the cargo-directed motion through the symmetry-breaking transition of the ParA-ATP spatiotemporal pattern. We also quantitatively demonstrate that the chemophoresis engine can work even under in vivo conditions. Finally, we discuss the chemophoresis engine as one of the general mechanisms of hydrolysis-driven intracellular transport. Public Library of Science 2022-07-25 /pmc/articles/PMC9363008/ /pubmed/35877681 http://dx.doi.org/10.1371/journal.pcbi.1010324 Text en © 2022 Sugawara, Kaneko https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sugawara, Takeshi
Kaneko, Kunihiko
Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title_full Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title_fullStr Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title_full_unstemmed Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title_short Chemophoresis engine: A general mechanism of ATPase-driven cargo transport
title_sort chemophoresis engine: a general mechanism of atpase-driven cargo transport
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9363008/
https://www.ncbi.nlm.nih.gov/pubmed/35877681
http://dx.doi.org/10.1371/journal.pcbi.1010324
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