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The Journal of Neuroscience, October 18, 2006, 26(42):10916-10924; doi:10.1523/JNEUROSCI.3269-06.2006

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Cellular/Molecular
Inositol 1,4,5-Trisphosphate Receptor Type 1 in Granule Cells, Not in Purkinje Cells, Regulates the Dendritic Morphology of Purkinje Cells through Brain-Derived Neurotrophic Factor Production

Chihiro Hisatsune,^1,3 Yukiko Kuroda,³ Takumi Akagi,² Takashi Torashima,⁴ Hirokazu Hirai,⁴ Tsutomu Hashikawa,² Takafumi Inoue,^3,5 and Katsuhiko Mikoshiba^1,3,5

Laboratories for ¹Developmental Neurobiology and ²Neural Architecture, RIKEN Brain Science Institute, Wako City, Saitama 351-0198, Japan, ³Division of Molecular Neurobiology, Institute of Medical Science, The University of Tokyo, Minato-ku, Tokyo 108-8639, Japan, ⁴Innovative Brain Science Project, Advanced Science Research Center, Kanazawa University, Kanazawa 920-8640, Japan, and ⁵Calcium Oscillation Project, International Cooperative Research Project, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0084, Japan

Correspondence should be addressed to Dr. Chihiro Hisatsune, Division of Molecular Neurobiology, Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokane-dai, Minato-ku, Tokyo 108-8639, Japan. Email: chihiro{at}ims.u-tokyo.ac.jp

Here, we show that cultured Purkinje cells from inositol 1,4,5-trisphosphate receptor type 1 knock-out (IP₃R1KO) mice exhibited abnormal dendritic morphology. Interestingly, despite the huge amount of IP₃R1 expression in Purkinje cells, IP₃R1 in granule cells, not in the Purkinje cells, was responsible for the shape of Purkinje cell dendrites. We also found that BDNF application rescued the dendritic abnormality of IP₃R1KO Purkinje cells, and that the increase in BDNF expression in response to activation of AMPA receptor (AMPAR) and metabotropic glutamate receptor (mGluR) was impaired in IP₃R1KO cerebellar granule cells. In addition, we observed abnormalities in the dendritic morphology of Purkinje cells and in the ultrastructure of parallel fiber–Purkinje cell (PF-PC) synapses in IP₃R1KO mice in vivo. We concluded that activation of AMPAR and mGluR increases BDNF expression through IP₃R1-mediated signaling in cerebellar granule cells, which contributes to the dendritic outgrowth of Purkinje cells intercellularly, possibly by modifying PF-PC synaptic efficacy.

Key words: dendrite outgrowth; IP₃ receptor; BDNF; Purkinje cell; granule cell; Ca²⁺ release

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Received July 29, 2006; revised Sept. 12, 2006; accepted Sept. 14, 2006.

Correspondence should be addressed to Dr. Chihiro Hisatsune, Division of Molecular Neurobiology, Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokane-dai, Minato-ku, Tokyo 108-8639, Japan. Email: chihiro{at}ims.u-tokyo.ac.jp

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