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The Journal of Neuroscience, November 14, 2007, 27(46):12546-12554; doi:10.1523/JNEUROSCI.3463-07.2007

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Development/Plasticity/Repair
Regulation of Spine Development by Semaphorin3A through Cyclin-Dependent Kinase 5 Phosphorylation of Collapsin Response Mediator Protein 1

Naoya Yamashita,¹ Asa Morita,¹ Yutaka Uchida,¹ Fumio Nakamura,¹ Hiroshi Usui,¹ Toshio Ohshima,² Masahiko Taniguchi,³ Jérôme Honnorat,⁴ Nicole Thomasset,⁴ Kohtaro Takei,^1,7 Takuya Takahashi,⁵ Pappachan Kolattukudy,⁶ and Yoshio Goshima^1,7

¹Department of Molecular Pharmacology and Neurobiology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan, ²Department of Life Science and Medical BioScience, Faculty of Science and Engineering, Waseda University, Tokyo 169-8555, Japan, ³Department of Biochemistry, Cancer Research Institute, Sapporo Medical University, Sapporo 060-8556, Japan, ⁴Unité Mixte de Recherche INSERM, U842, Lyon, F-69003 France, ⁵Department of Physiology and Neuroendocrinology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan, ⁶Biomolecular Science Center, University of Central Florida, Orlando, Florida 32816, and ⁷Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Correspondence should be addressed to Yoshio Goshima, Department of Molecular Pharmacology and Neurobiology, Yokohama City University, School of Medicine, Fuku-ura 3-9, Kanazawa Ward, Yokohama City 236-0004, Japan. Email: goshima{at}med.yokohama-cu.ac.jp

Collapsin response mediator protein 1 (CRMP1) is one of the CRMP family members that mediates signal transduction of axonal guidance and neuronal migration. We show here evidence that CRMP1 is involved in semaphorin3A (Sema3A)-induced spine development in the cerebral cortex. In the cultured cortical neurons from crmp1^+/– mice, Sema3A increased the density of clusters of synapsin I and postsynaptic density-95, but this increase was markedly attenuated in crmp1^–/– mice. This attenuation was also seen in cyclin-dependent kinase 5 (cdk5)^–/– neurons. Furthermore, the introduction of wild-type CRMP1 but not CRMP1-T509A/S522A, (Thr 509 and Ser 522 were replaced by Ala), a mutant that cannot be phosphorylated by Cdk5, into crmp1^–/– neurons rescued the defect in Sema3A responsiveness. The Golgi-impregnation method showed that the crmp1^–/– layer V cortical neurons showed a lower density of synaptic bouton-like structures and that this phenotype had genetic interaction with sema3A. These findings suggest that Sema3A-induced spine development is regulated by phosphorylation of CRMP1 by Cdk5.

Key words: CRMP; Sema3A; Cdk5; spine; PSD-95; synapsin I; cerebral cortex

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Received Oct. 20, 2006; revised Oct. 2, 2007; accepted Oct. 4, 2007.

Correspondence should be addressed to Yoshio Goshima, Department of Molecular Pharmacology and Neurobiology, Yokohama City University, School of Medicine, Fuku-ura 3-9, Kanazawa Ward, Yokohama City 236-0004, Japan. Email: goshima{at}med.yokohama-cu.ac.jp

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