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.
Highlights
Formation of large brains such as the mammalian cerebral cortex depends on continuous and efficient cell production by neural progenitor cells (NPCs) [1, 2, 3]
One possibility is that nuclei/somata of early G1-phase cells in the subapical space of the ventricular zone (VZ) are propelled through direct soma–soma collision or pushing by G2- or M-phase cells (Fig 2A)
We found that the subapical space had no extracellular gaps and that apical processes were more abundant than somata, whereas the process/soma ratio decreased in deeper VZ regions
Summary
Formation of large brains such as the mammalian cerebral cortex depends on continuous and efficient cell production by neural progenitor cells (NPCs) [1, 2, 3]. NPCs are elongated, spanning a developing brain wall (up to 300 μm thick in mice), and divide at the apical surface [4, 5, 6, 7, 8] (Fig 1A). They individually move the nuclei and somata in a cell cycle– dependent manner (apical during G2 and basal during G1), and these nuclear/somal movements are called interkinetic nuclear migration (IKNM) [9, 10, 11, 12] (Fig 1A–1C, S1 Movie). The high pseudostratification of the cerebral cortical VZs has led to it becoming a model system to study “production logistics” in organogenesis
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