The EMBO Journal (2011) 30, 1690 - 1704
doi:10.1038/emboj.2011.81
Published online: 25 March 2011
There is a Have you seen? (May 2011) associated with this Article.
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Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain
EMBO Open
Yoichi Kosodo1,2, Taeko Suetsugu1, Masumi Suda2, Yuko Mimori-Kiyosue3, Kazunori Toida2, Shoji A Baba4, Akatsuki Kimura5 and Fumio Matsuzaki1
Laboratory for Cell Asymmetry, RIKEN Center for Developmental Biology, Kobe, Japan
Department of Anatomy, Kawasaki Medical School, Kurashiki, Japan
Optical Image Analysis Unit, RIKEN Center for Developmental Biology, Kobe, Japan
Department of Biology, Ochanomizu University, Tokyo, Japan
Cell Architecture Laboratory, Center for Frontier Research, National Institute of Genetics, Shizuoka, Japan
Correspondence to:
Yoichi Kosodo, Department of Anatomy, Kawasaki Medical School, 577 Matsushima, Kurashiki 701-0192, Japan. Tel.: +81 86 462 1111; Fax: +81 86 462 1199; E-mail:kosodo@med.kawasaki-m.ac.jp
Fumio Matsuzaki, Laboratory for Cell Asymmetry, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-Minamimachi, Chuou-ku, Kobe 650-0047, Japan. Tel.: +81 78 306 3217; Fax: +81 78 306 3215; E-mail: fumio@cdb.riken.jp
Received 19 May 2010; Accepted 23 February 2011
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.
Keywords: cell cycle; computational model; microtubule; neuroepithelial cell; Tpx2
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The EMBO Journal is published by Nature Publishing Group on behalf of European Molecular Biology Organization
This article is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 Unported License
