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Cytoplasmic organization promotes protein diffusion in Xenopus extracts

The cytoplasm is highly organized. However, the extent to which this organization influences the dynamics of cytoplasmic proteins is not well understood. Here, we use Xenopus laevis egg extracts as a model system to study diffusion dynamics in organized versus disorganized cytoplasm. Such extracts a...

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Autores principales: Huang, William Y. C., Cheng, Xianrui, Ferrell, James E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508076/
https://www.ncbi.nlm.nih.gov/pubmed/36151204
http://dx.doi.org/10.1038/s41467-022-33339-0
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author Huang, William Y. C.
Cheng, Xianrui
Ferrell, James E.
author_facet Huang, William Y. C.
Cheng, Xianrui
Ferrell, James E.
author_sort Huang, William Y. C.
collection PubMed
description The cytoplasm is highly organized. However, the extent to which this organization influences the dynamics of cytoplasmic proteins is not well understood. Here, we use Xenopus laevis egg extracts as a model system to study diffusion dynamics in organized versus disorganized cytoplasm. Such extracts are initially homogenized and disorganized, and self-organize into cell-like units over the course of tens of minutes. Using fluorescence correlation spectroscopy, we observe that as the cytoplasm organizes, protein diffusion speeds up by about a factor of two over a length scale of a few hundred nanometers, eventually approaching the diffusion time measured in organelle-depleted cytosol. Even though the ordered cytoplasm contained organelles and cytoskeletal elements that might interfere with diffusion, the convergence of protein diffusion in the cytoplasm toward that in organelle-depleted cytosol suggests that subcellular organization maximizes protein diffusivity. The effect of organization on diffusion varies with molecular size, with the effects being largest for protein-sized molecules, and with the time scale of the measurement. These results show that cytoplasmic organization promotes the efficient diffusion of protein molecules in a densely packed environment.
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spelling pubmed-95080762022-09-25 Cytoplasmic organization promotes protein diffusion in Xenopus extracts Huang, William Y. C. Cheng, Xianrui Ferrell, James E. Nat Commun Article The cytoplasm is highly organized. However, the extent to which this organization influences the dynamics of cytoplasmic proteins is not well understood. Here, we use Xenopus laevis egg extracts as a model system to study diffusion dynamics in organized versus disorganized cytoplasm. Such extracts are initially homogenized and disorganized, and self-organize into cell-like units over the course of tens of minutes. Using fluorescence correlation spectroscopy, we observe that as the cytoplasm organizes, protein diffusion speeds up by about a factor of two over a length scale of a few hundred nanometers, eventually approaching the diffusion time measured in organelle-depleted cytosol. Even though the ordered cytoplasm contained organelles and cytoskeletal elements that might interfere with diffusion, the convergence of protein diffusion in the cytoplasm toward that in organelle-depleted cytosol suggests that subcellular organization maximizes protein diffusivity. The effect of organization on diffusion varies with molecular size, with the effects being largest for protein-sized molecules, and with the time scale of the measurement. These results show that cytoplasmic organization promotes the efficient diffusion of protein molecules in a densely packed environment. Nature Publishing Group UK 2022-09-23 /pmc/articles/PMC9508076/ /pubmed/36151204 http://dx.doi.org/10.1038/s41467-022-33339-0 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
Huang, William Y. C.
Cheng, Xianrui
Ferrell, James E.
Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title_full Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title_fullStr Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title_full_unstemmed Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title_short Cytoplasmic organization promotes protein diffusion in Xenopus extracts
title_sort cytoplasmic organization promotes protein diffusion in xenopus extracts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508076/
https://www.ncbi.nlm.nih.gov/pubmed/36151204
http://dx.doi.org/10.1038/s41467-022-33339-0
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