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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
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.
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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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