TY - JOUR
T1 - Elasticity-based boosting of neuroepithelial nucleokinesis via indirect energy transfer from mother to daughter
AU - Shinoda, Tomoyasu
AU - Nagasaka, Arata
AU - Inoue, Yasuhiro
AU - Higuchi, Ryo
AU - Minami, Yoshiaki
AU - Kato, Kagayaki
AU - Suzuki, Makoto
AU - Kondo, Takefumi
AU - Kawaue, Takumi
AU - Saito, Kanako
AU - Ueno, Naoto
AU - Fukazawa, Yugo
AU - Nagayama, Masaharu
AU - Miura, Takashi
AU - Adachi, Taiji
AU - Miyata, Takaki
N1 - Publisher Copyright:
© 2018 Shinoda et al.
PY - 2018/4/20
Y1 - 2018/4/20
N2 - 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.
AB - 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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U2 - 10.1371/journal.pbio.2004426
DO - 10.1371/journal.pbio.2004426
M3 - Article
C2 - 29677184
AN - SCOPUS:85046438236
SN - 1544-9173
VL - 16
JO - PLoS Biology
JF - PLoS Biology
IS - 4
M1 - e2004426
ER -