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The Journal of Neuroscience, August 15, 2007, 27(33):8866-8876; doi:10.1523/JNEUROSCI.1047-07.2007

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Development/Plasticity/Repair
Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Yutaka Furutani,^1,2 Hitomi Matsuno,^1,2 Miwa Kawasaki,¹ Takehiko Sasaki,³ Kensaku Mori,⁴ and Yoshihiro Yoshihara^1,2

¹Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, Saitama 351-0198, Japan, ²Core Research Evolutional Science and Technology, Japan Science and Technology Agency, Osaka 560-0082, Japan, ³Department of Pathology and Immunology, Akita University School of Medicine, Akita 010-8543, Japan, and ⁴Department of Physiology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-0033, Japan

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

Dendritic filopodia are long, thin, actin-rich, and dynamic protrusions that are thought to play a critical role as a precursor of spines during neural development. We reported previously that a telencephalon-specific cell adhesion molecule, telencephalin (TLCN) [intercellular adhesion molecule-5 (ICAM-5)], is highly expressed in dendritic filopodia, facilitates the filopodia formation, and slows spine maturation. Here we demonstrate that TLCN cytoplasmic region binds ERM (ezrin/radixin/moesin) family proteins that link membrane proteins to actin cytoskeleton. In cultured hippocampal neurons, phosphorylated active forms of ERM proteins are colocalized with TLCN in dendritic filopodia, whereas -actinin, another binding partner of TLCN, is colocalized with TLCN at surface membranes of soma and dendritic shafts. Expression of constitutively active ezrin induces dendritic filopodia formation, whereas small interference RNA-mediated knockdown of ERM proteins decreases filopodia density and accelerates spine maturation. These results indicate the important role of TLCN–ERM interaction in the formation of dendritic filopodia, which leads to subsequent synaptogenesis and establishment of functional neural circuitry in the developing brain.

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

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Received March 8, 2007; revised June 14, 2007; accepted July 5, 2007.

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

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