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Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos

The Drosophila melanogaster embryo, an elongated multi-nucleated cell, is a classical model system for eukaryotic development and morphogenesis. Recent work has shown that bulk cytoplasmic flows, driven by cortical contractions along the walls of the embryo, enable the uniform spreading of nuclei al...

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Autores principales: Htet, Pyae Hein, Lauga, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645513/
https://www.ncbi.nlm.nih.gov/pubmed/37963561
http://dx.doi.org/10.1098/rsif.2023.0428
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author Htet, Pyae Hein
Lauga, Eric
author_facet Htet, Pyae Hein
Lauga, Eric
author_sort Htet, Pyae Hein
collection PubMed
description The Drosophila melanogaster embryo, an elongated multi-nucleated cell, is a classical model system for eukaryotic development and morphogenesis. Recent work has shown that bulk cytoplasmic flows, driven by cortical contractions along the walls of the embryo, enable the uniform spreading of nuclei along the anterior–posterior axis necessary for proper embryonic development. Here, we propose two mathematical models to characterize cytoplasmic flows driven by tangential cortical contractions in elongated cells. Assuming Newtonian fluid flow at low Reynolds number in a spheroidal cell, we first compute the flow field exactly, thereby bypassing the need for numerical computations. We then apply our results to recent experiments on nuclear transport in cell cycles 4–6 of Drosophila embryo development. By fitting the cortical contractions in our model to measurements, we reveal that experimental cortical flows enable near-optimal axial spreading of nuclei. A second mathematical approach, applicable to general elongated cell geometries, exploits a long-wavelength approximation to produce an even simpler solution, with errors below [Formula: see text] compared with the full model. An application of this long-wavelength result to transport leads to fully analytical solutions for the nuclear concentration that capture the essential physics of the system, including optimal axial spreading of nuclei.
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spelling pubmed-106455132023-11-15 Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos Htet, Pyae Hein Lauga, Eric J R Soc Interface Life Sciences–Mathematics interface The Drosophila melanogaster embryo, an elongated multi-nucleated cell, is a classical model system for eukaryotic development and morphogenesis. Recent work has shown that bulk cytoplasmic flows, driven by cortical contractions along the walls of the embryo, enable the uniform spreading of nuclei along the anterior–posterior axis necessary for proper embryonic development. Here, we propose two mathematical models to characterize cytoplasmic flows driven by tangential cortical contractions in elongated cells. Assuming Newtonian fluid flow at low Reynolds number in a spheroidal cell, we first compute the flow field exactly, thereby bypassing the need for numerical computations. We then apply our results to recent experiments on nuclear transport in cell cycles 4–6 of Drosophila embryo development. By fitting the cortical contractions in our model to measurements, we reveal that experimental cortical flows enable near-optimal axial spreading of nuclei. A second mathematical approach, applicable to general elongated cell geometries, exploits a long-wavelength approximation to produce an even simpler solution, with errors below [Formula: see text] compared with the full model. An application of this long-wavelength result to transport leads to fully analytical solutions for the nuclear concentration that capture the essential physics of the system, including optimal axial spreading of nuclei. The Royal Society 2023-11-15 /pmc/articles/PMC10645513/ /pubmed/37963561 http://dx.doi.org/10.1098/rsif.2023.0428 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Life Sciences–Mathematics interface
Htet, Pyae Hein
Lauga, Eric
Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title_full Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title_fullStr Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title_full_unstemmed Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title_short Cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in Drosophila embryos
title_sort cortex-driven cytoplasmic flows in elongated cells: fluid mechanics and application to nuclear transport in drosophila embryos
topic Life Sciences–Mathematics interface
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645513/
https://www.ncbi.nlm.nih.gov/pubmed/37963561
http://dx.doi.org/10.1098/rsif.2023.0428
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