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The Journal of Neuroscience, October 27, 2004, 24(43):9648-9657; doi:10.1523/JNEUROSCI.2363-04.2004

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Development/Plasticity/Repair
Filamin A and FILIP (Filamin A-Interacting Protein) Regulate Cell Polarity and Motility in Neocortical Subventricular and Intermediate Zones during Radial Migration

Takashi Nagano,¹ Soichi Morikubo,^1,2 and Makoto Sato^1,3

¹Division of Cell Biology and Neuroscience, Department of Morphological and Physiological Sciences, and ²Division of Ophthalmology, Department of Sensory and Locomotor Medicine, Faculty of Medical Sciences, University of Fukui, Matsuoka, Fukui 910-1193, Japan, and ³Solution Oriented Research for Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan

In the developing neocortex, most excitatory neurons are supplied and arranged through radial migration. Because neurons show global morphological changes and complicated behavior during that migration, precise regulation of cell shape and polarity is essential for proper migration and correct neocortical formation; however, how cell shape and polarity are regulated in migrating neuron remains elusive. We show here that Filamin A, a well known actin-binding protein, determines the shape of neocortical neurons during radial migration in vivo. Dysfunction of Filamin A, caused by a mutant Filamin A expression, prevents cells from acquiring consistent polarity toward specific direction and decreases motility in the subventricular and intermediate zones. In contrast, Filamin A overexpression, achieved by a short interfering RNA for Filamin A-interacting protein that induces Filamin A degradation (FILIP), promotes the development and maintenance of a bipolar shape also in the subventricular and intermediate zones. These results suggest that the amount of Filamin A helps migrating neurons determine their mode of migration, multipolar or bipolar, before entering the cortical plate and that FILIP is responsible, at least in part, for Filamin A content. In addition, our results also give a possible clue to understanding the pathogenesis of human malformation periventricular heterotopia, which is caused by various "loss-of-function" mutations in the filamin A gene.

Key words: cortex; migration; multipolar migration; actin; cytoskeleton; periventricular heterotopia

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Received June 16, 2004; revised August 18, 2004; accepted September 10, 2004.

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