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Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter
Neural progenitor cells (NPCs), which are apicobasally elongated and densely packed in the developing brain, systematically move their nuclei/somata in a cell cycle–dependent manner, called interkinetic nuclear migration (IKNM): apical during G2 and basal during G1. Although intracellular molecular...
Autores principales: | , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5931692/ https://www.ncbi.nlm.nih.gov/pubmed/29677184 http://dx.doi.org/10.1371/journal.pbio.2004426 |
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author | Shinoda, Tomoyasu Nagasaka, Arata Inoue, Yasuhiro Higuchi, Ryo Minami, Yoshiaki Kato, Kagayaki Suzuki, Makoto Kondo, Takefumi Kawaue, Takumi Saito, Kanako Ueno, Naoto Fukazawa, Yugo Nagayama, Masaharu Miura, Takashi Adachi, Taiji Miyata, Takaki |
author_facet | Shinoda, Tomoyasu Nagasaka, Arata Inoue, Yasuhiro Higuchi, Ryo Minami, Yoshiaki Kato, Kagayaki Suzuki, Makoto Kondo, Takefumi Kawaue, Takumi Saito, Kanako Ueno, Naoto Fukazawa, Yugo Nagayama, Masaharu Miura, Takashi Adachi, Taiji Miyata, Takaki |
author_sort | Shinoda, Tomoyasu |
collection | PubMed |
description | Neural progenitor cells (NPCs), which are apicobasally elongated and densely packed in the developing brain, systematically move their nuclei/somata in a cell cycle–dependent manner, called interkinetic nuclear migration (IKNM): apical during G2 and basal during G1. Although intracellular molecular mechanisms of individual IKNM have been explored, how heterogeneous IKNMs are collectively coordinated is unknown. Our quantitative cell-biological and in silico analyses revealed that tissue elasticity mechanically assists an initial step of basalward IKNM. When the soma of an M-phase progenitor cell rounds up using actomyosin within the subapical space, a microzone within 10 μm from the surface, which is compressed and elastic because of the apical surface’s contractility, laterally pushes the densely neighboring processes of non–M-phase cells. The pressed processes then recoil centripetally and basally to propel the nuclei/somata of the progenitor’s daughter cells. Thus, indirect neighbor-assisted transfer of mechanical energy from mother to daughter helps efficient brain development. |
format | Online Article Text |
id | pubmed-5931692 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-59316922018-05-11 Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter Shinoda, Tomoyasu Nagasaka, Arata Inoue, Yasuhiro Higuchi, Ryo Minami, Yoshiaki Kato, Kagayaki Suzuki, Makoto Kondo, Takefumi Kawaue, Takumi Saito, Kanako Ueno, Naoto Fukazawa, Yugo Nagayama, Masaharu Miura, Takashi Adachi, Taiji Miyata, Takaki PLoS Biol Research Article Neural progenitor cells (NPCs), which are apicobasally elongated and densely packed in the developing brain, systematically move their nuclei/somata in a cell cycle–dependent manner, called interkinetic nuclear migration (IKNM): apical during G2 and basal during G1. Although intracellular molecular mechanisms of individual IKNM have been explored, how heterogeneous IKNMs are collectively coordinated is unknown. Our quantitative cell-biological and in silico analyses revealed that tissue elasticity mechanically assists an initial step of basalward IKNM. When the soma of an M-phase progenitor cell rounds up using actomyosin within the subapical space, a microzone within 10 μm from the surface, which is compressed and elastic because of the apical surface’s contractility, laterally pushes the densely neighboring processes of non–M-phase cells. The pressed processes then recoil centripetally and basally to propel the nuclei/somata of the progenitor’s daughter cells. Thus, indirect neighbor-assisted transfer of mechanical energy from mother to daughter helps efficient brain development. Public Library of Science 2018-04-20 /pmc/articles/PMC5931692/ /pubmed/29677184 http://dx.doi.org/10.1371/journal.pbio.2004426 Text en © 2018 Shinoda et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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 Shinoda, Tomoyasu Nagasaka, Arata Inoue, Yasuhiro Higuchi, Ryo Minami, Yoshiaki Kato, Kagayaki Suzuki, Makoto Kondo, Takefumi Kawaue, Takumi Saito, Kanako Ueno, Naoto Fukazawa, Yugo Nagayama, Masaharu Miura, Takashi Adachi, Taiji Miyata, Takaki Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title | Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title_full | Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title_fullStr | Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title_full_unstemmed | Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title_short | Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
title_sort | elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5931692/ https://www.ncbi.nlm.nih.gov/pubmed/29677184 http://dx.doi.org/10.1371/journal.pbio.2004426 |
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