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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...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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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. |
format | Online Article Text |
id | pubmed-9363008 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT sugawaratakeshi chemophoresisengineageneralmechanismofatpasedrivencargotransport AT kanekokunihiko chemophoresisengineageneralmechanismofatpasedrivencargotransport |