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Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos

Cytoplasmic flows are widely emerging as key functional players in development. In early Drosophila embryos, flows drive the spreading of nuclei across the embryo. Here, we combine hydrodynamic modeling with quantitative imaging to develop a two-fluid model that features an active actomyosin gel and...

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Autores principales: López, Claudio Hernández, Puliafito, Alberto, Xu, Yitong, Lu, Ziqi, Di Talia, Stefano, Vergassola, Massimo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055070/
https://www.ncbi.nlm.nih.gov/pubmed/36993669
http://dx.doi.org/10.1101/2023.03.16.532979
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author López, Claudio Hernández
Puliafito, Alberto
Xu, Yitong
Lu, Ziqi
Di Talia, Stefano
Vergassola, Massimo
author_facet López, Claudio Hernández
Puliafito, Alberto
Xu, Yitong
Lu, Ziqi
Di Talia, Stefano
Vergassola, Massimo
author_sort López, Claudio Hernández
collection PubMed
description Cytoplasmic flows are widely emerging as key functional players in development. In early Drosophila embryos, flows drive the spreading of nuclei across the embryo. Here, we combine hydrodynamic modeling with quantitative imaging to develop a two-fluid model that features an active actomyosin gel and a passive viscous cytosol. Gel contractility is controlled by the cell cycle oscillator, the two fluids being coupled by friction. In addition to recapitulating experimental flow patterns, our model explains observations that remained elusive, and makes a series of new predictions. First, the model captures the vorticity of cytosolic flows, which highlights deviations from Stokes’ flow that were observed experimentally but remained unexplained. Second, the model reveals strong differences in the gel and cytosol motion. In particular, a micron-sized boundary layer is predicted close to the cortex, where the gel slides tangentially whilst the cytosolic flow cannot slip. Third, the model unveils a mechanism that stabilizes the spreading of nuclei with respect to perturbations of their initial positions. This self-correcting mechanism is argued to be functionally important for proper nuclear spreading. Fourth, we use our model to analyze the effects of flows on the transport of the morphogen Bicoid, and the establishment of its gradients. Finally, the model predicts that the flow strength should be reduced if the shape of the domain is more round, which is experimentally confirmed in Drosophila mutants. Thus, our two-fluid model explains flows and nuclear positioning in early Drosophila, while making predictions that suggest novel future experiments.
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spelling pubmed-100550702023-03-30 Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos López, Claudio Hernández Puliafito, Alberto Xu, Yitong Lu, Ziqi Di Talia, Stefano Vergassola, Massimo bioRxiv Article Cytoplasmic flows are widely emerging as key functional players in development. In early Drosophila embryos, flows drive the spreading of nuclei across the embryo. Here, we combine hydrodynamic modeling with quantitative imaging to develop a two-fluid model that features an active actomyosin gel and a passive viscous cytosol. Gel contractility is controlled by the cell cycle oscillator, the two fluids being coupled by friction. In addition to recapitulating experimental flow patterns, our model explains observations that remained elusive, and makes a series of new predictions. First, the model captures the vorticity of cytosolic flows, which highlights deviations from Stokes’ flow that were observed experimentally but remained unexplained. Second, the model reveals strong differences in the gel and cytosol motion. In particular, a micron-sized boundary layer is predicted close to the cortex, where the gel slides tangentially whilst the cytosolic flow cannot slip. Third, the model unveils a mechanism that stabilizes the spreading of nuclei with respect to perturbations of their initial positions. This self-correcting mechanism is argued to be functionally important for proper nuclear spreading. Fourth, we use our model to analyze the effects of flows on the transport of the morphogen Bicoid, and the establishment of its gradients. Finally, the model predicts that the flow strength should be reduced if the shape of the domain is more round, which is experimentally confirmed in Drosophila mutants. Thus, our two-fluid model explains flows and nuclear positioning in early Drosophila, while making predictions that suggest novel future experiments. Cold Spring Harbor Laboratory 2023-03-20 /pmc/articles/PMC10055070/ /pubmed/36993669 http://dx.doi.org/10.1101/2023.03.16.532979 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
López, Claudio Hernández
Puliafito, Alberto
Xu, Yitong
Lu, Ziqi
Di Talia, Stefano
Vergassola, Massimo
Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title_full Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title_fullStr Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title_full_unstemmed Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title_short Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos
title_sort two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early drosophila embryos
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055070/
https://www.ncbi.nlm.nih.gov/pubmed/36993669
http://dx.doi.org/10.1101/2023.03.16.532979
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