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The Journal of Neuroscience, March 15, 2006, 26(11):2971-2980; doi:10.1523/JNEUROSCI.5453-05.2006

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Development/Plasticity/Repair
Regulation of Dendritic Branching and Spine Maturation by Semaphorin3A-Fyn Signaling

Asa Morita,¹ Naoya Yamashita,¹ Yukio Sasaki,¹ Yutaka Uchida,¹ Oumi Nakajima,¹ Fumio Nakamura,¹ Takeshi Yagi,³ Masahiko Taniguchi,⁴ Hiroshi Usui,¹ Ritsuko Katoh-Semba,⁵ Kohtaro Takei,^1,2 and Yoshio Goshima^1,2

¹Department of Molecular Pharmacology and Neurobiology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan, ²Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan, ³KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University, Suita 565-0871, Japan, ⁴Department of Biochemistry and Molecular Biology Graduate School of Medicine, University of Tokyo, Tokyo 113-0033, Japan, and ⁵Institute for Developmental Research, Aichi Human Service Center, Aichi 480-0392, 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

A member of semaphorin family, semaphorin3A (Sema3A), acts as a chemorepellent or chemoattractant on a wide variety of axons and dendrites in the development of the nervous systems. We here show that Sema3A induces clustering of both postsynaptic density-95 (PSD-95) and presynaptic synapsin I in cultured cortical neurons without changing the density of spines or filopodia. Neuropilin-1 (NRP-1), a receptor for Sema3A, is present on both axons and dendrites. When the cultured neurons are exposed to Sema3A, the cluster size of PSD-95 is markedly enhanced, and an extensive colocalization of PSD-95 and NRP-1 or actin-rich protrusion is seen. The effects of Sema3A on spine morphology are blocked by PP2, an Src type tyrosine kinase inhibitor, but not by the PP3, the inactive-related compound. In the cultured cortical neurons from fyn^–/– mice, dendrites bear few spines, and Sema3A does not induce PSD-95 cluster formation on the dendrites. Sema3A and its receptor genes are highly expressed during the synaptogenic period of postnatal days 10 and 15. The cortical neurons in layer V, but not layer III, show a lowered density of synaptic bouton-like structure on dendrites in sema3A- and fyn-deficient mice. The neurons of the double-heterozygous mice show the lowered spine density, whereas those of single heterozygous mice show similar levels of the spine density as the wild type. These findings suggest that the Sema3A signaling pathway plays an important role in the regulation of dendritic spine maturation in the cerebral cortex neurons.

Key words: Sema3A; Fyn; dendrite; spine; cerebral cortex; axon guidance

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Received April 30, 2005; revised Jan. 27, 2006; accepted Jan. 27, 2006.

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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