Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain |
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Authors: | Kosodo Yoichi Suetsugu Taeko Suda Masumi Mimori-Kiyosue Yuko Toida Kazunori Baba Shoji A Kimura Akatsuki Matsuzaki Fumio |
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Institution: | 1Laboratory for Cell Asymmetry, RIKEN Center for Developmental Biology, Kobe, Japan;2Department of Anatomy, Kawasaki Medical School, Kurashiki, Japan;3Optical Image Analysis Unit, RIKEN Center for Developmental Biology, Kobe, Japan;4Department of Biology, Ochanomizu University, Tokyo, Japan;5Cell Architecture Laboratory, Center for Frontier Research, National Institute of Genetics, Shizuoka, Japan |
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Abstract: | A hallmark of neurogenesis in the vertebrate brain is the apical-basal nuclear oscillation in polarized neural progenitor cells. Known as interkinetic nuclear migration (INM), these movements are synchronized with the cell cycle such that nuclei move basally during G1-phase and apically during G2-phase. However, it is unknown how the direction of movement and the cell cycle are tightly coupled. Here, we show that INM proceeds through the cell cycle-dependent linkage of cell-autonomous and non-autonomous mechanisms. During S to G2 progression, the microtubule-associated protein Tpx2 redistributes from the nucleus to the apical process, and promotes nuclear migration during G2-phase by altering microtubule organization. Thus, Tpx2 links cell-cycle progression and autonomous apical nuclear migration. In contrast, in vivo observations of implanted microbeads, acute S-phase arrest of surrounding cells and computational modelling suggest that the basal migration of G1-phase nuclei depends on a displacement effect by G2-phase nuclei migrating apically. Our model for INM explains how the dynamics of neural progenitors harmonize their extensive proliferation with the epithelial architecture in the developing brain. |
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Keywords: | cell cycle computational model microtubule neuroepithelial cell Tpx2 |
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