Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter

  • Tomoyasu Shinoda
  • , Arata Nagasaka
  • , Yasuhiro Inoue
  • , Ryo Higuchi
  • , Yoshiaki Minami
  • , Kagayaki Kato
  • , Makoto Suzuki
  • , Takefumi Kondo
  • , Takumi Kawaue
  • , Kanako Saito
  • , Naoto Ueno
  • , Yugo Fukazawa
  • , Masaharu Nagayama
  • , Takashi Miura
  • , Taiji Adachi
  • , Takaki Miyata

Research output: Contribution to journalArticlepeer-review

20 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article numbere2004426
JournalPLoS Biology
Volume16
Issue number4
DOIs
Publication statusPublished - 20-04-2018
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • General Neuroscience
  • General Biochemistry,Genetics and Molecular Biology
  • General Immunology and Microbiology
  • General Agricultural and Biological Sciences

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