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The Journal of Neuroscience, February 8, 2006, 26(6):1776-1786; doi:10.1523/JNEUROSCI.2651-05.2006

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Development/Plasticity/Repair
Telencephalin Slows Spine Maturation

Hitomi Matsuno,^1,2 Shigeo Okabe,⁴ Masayoshi Mishina,⁵ Toshio Yanagida,^2,3 Kensaku Mori,⁶ and Yoshihiro Yoshihara^1,7

¹Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, Saitama 351-0198, Japan, ²Department of Systems and Human Science, Graduate School of Engineering Science, and ³Nanobiology Laboratories, Graduate School of Frontier Biosciences, Osaka University, Osaka 560-8531, Japan, ⁴Department of Anatomy and Cell Biology, School of Medicine, Tokyo Medical and Dental University, Tokyo 113-8519, Japan, ⁵Departments of Molecular Neurobiology and Pharmacology and ⁶Physiology, Graduate School of Medicine, University of Tokyo, Tokyo 113-0033, Japan, and ⁷Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Osaka 560-0082, Japan

Correspondence should be addressed to Dr. Yoshihiro Yoshihara, Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. Email: yoshihara{at}brain.riken.jp

Dendritic filopodia are highly dynamic structures, and morphological maturation from dendritic filopodia to spines is intimately associated with the stabilization and strengthening of synapses during development. Here, we report that telencephalin (TLCN), a cell adhesion molecule belonging to the Ig superfamily, is a negative regulator of spine maturation. Using cultured hippocampal neurons, we examined detailed localization and functions of TLCN in spine development and synaptogenesis. At early stages of synaptogenesis, TLCN immunoreactivity gradually increased and was present in dendritic shafts and filopodia. At later stages, TLCN tended to be excluded from mature spine synapses in which PSD-95 (postsynaptic density-95) clusters were apposed to presynaptic synaptophysin clusters. To elucidate the function of TLCN in spine maturation, we analyzed the dendrite morphology of TLCN-overexpressing and TLCN-deficient neurons. Overexpression of TLCN caused a dramatic increase in the density of dendritic filopodia and a concomitant decrease in the density of spines. Conversely, TLCN-deficient mice showed a decreased density of filopodia and an acceleration of spine maturation in vitro as well as in vivo. These results demonstrate that TLCN normally slows spine maturation by promoting the filopodia formation and negatively regulating the filopodia-to-spine transition. In addition, we found that spine heads of mature neurons were wider in TLCN-deficient mice compared with wild-type mice. Thus, the preservation of immature synapses by TLCN may be an essential step for refinement of functional neural circuits in the telencephalon, that take charge of higher brain functions such as learning, memory, and emotion.

Key words: telencephalin; cell adhesion molecule; synaptogenesis; dendritic filopodia; spine; hippocampus

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Received April 8, 2005; revised Dec. 20, 2005; accepted Dec. 21, 2005.

Correspondence should be addressed to Dr. Yoshihiro Yoshihara, Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. Email: yoshihara{at}brain.riken.jp

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