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J. Biol. Chem., Vol. 279, Issue 47, 48976-48982, November 19, 2004

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Lateral Diffusion of Inositol 1,4,5-Trisphosphate Receptor Type 1 Is Regulated by Actin Filaments and 4.1N in Neuronal Dendrites^*

Kazumi Fukatsu, Hiroko Bannai, Songbai Zhang¶, Hideki Nakamura||, Takafumi Inoue¶**, and Katsuhiko Mikoshiba¶

From the Division of Molecular Neurobiology and Division of Neural Signal Information Nippon Telegraph and Telephone Company-The Institute of Medical Science, The University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan, the Laboratory for Developmental Neurobiology, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan, the ^¶Calcium Oscillation Project, ICORP, Japan Science and Technology Corporation, 3-4-4 Shirokanedai, Minato-ku, Tokyo 108-0071, Japan, and the ^||Department of Physics, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

Inositol 1,4,5-trisphosphate receptor type1 (IP₃R1) plays an important role in neuronal functions; however, the lateral diffusion of IP₃R1 on the endoplasmic reticulum membrane and its regulation in the living neurons remain unknown. We expressed green fluorescent protein-tagged IP₃R1 in cultured rat hippocampal neurons and observed the lateral diffusion by the fluorescence recovery after photobleaching technique. IP₃R1 showed lateral diffusion with an effective diffusion constant of 0.3 µm²/s. Depletion of actin filaments increased the diffusion constant of IP₃R1, suggesting that the diffusion of IP₃R1 is regulated negatively through actin filaments. We also found that protein 4.1N, which binds to IP₃R1 and contains an actin-spectrin-binding region, was responsible for this actin regulation of the IP₃R1 diffusion constant. Overexpression of dominant-negative 4.1N and blockade of 4.1N binding to IP₃R1 increased the IP₃R1 diffusion constant. The diffusion of IP₃R type 3 (IP₃R3), one of the isoforms of IP₃Rs lacking the binding ability to 4.1N, was not dependent on actin filaments but became dependent on actin filaments after the addition of a 4.1N-binding sequence. These data suggest that 4.1N serves as a linker protein between IP₃R1 and actin filaments. This actin filament-dependent regulation of IP₃R1 diffusion may be important for the spatiotemporal regulation of intracellular Ca²⁺ signaling.

Received for publication, July 23, 2004 , and in revised form, September 9, 2004.

^* This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to T. I. and K. M.), the Ministry of Health, Labour and Welfare of Japan (to T. I.), and the 21st Century COE Program, Center for Integrated Brain Medical Science, from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to K. F. and H. N.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^** To whom correspondence should be addressed. Tel.: 81-3-5449-5320; Fax: 81-3-5449-5420; E-mail: tinoue{at}ims.u-tokyo.ac.jp.

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