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The Journal of Neuroscience, February 11, 2004, 24(6):1486-1496; doi:10.1523/JNEUROSCI.4029-03.2004

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Development/Plasticity/Repair
ORP150/HSP12A Regulates Purkinje Cell Survival: A Role for Endoplasmic Reticulum Stress in Cerebellar Development

Yasuko Kitao,¹ Kouichi Hashimoto,² Tomohiro Matsuyama,⁴ Hiroyuki Iso,⁵ Takeshi Tamatani,¹ Osamu Hori,^1,3 David M. Stern,⁶ Masanobu Kano,² Kentaro Ozawa,¹ and Satoshi Ogawa^1,3

Departments of ¹Neuroanatomy and ²Cellular Neurophysiology, Graduate School of Medical Science, Kanazawa University, Kanazawa 920-8640, Japan, ³Core Research for Evolutional Science and Technology, Japan Science and Technology, Kawaguchi 332-0012, Japan, Departments of ⁴Internal Medicine and ⁵Behavior Science, Hyogo College of Medicine, Nishinomiya 663-8501, Hyogo, Japan, and ⁶Dean's Office, Medical College of Georgia, Augusta, Georgia 30912

The endoplasmic reticulum (ER) stress response contributes to neuronal survival in ischemia and neurodegenerative processes. ORP150 (oxygen-regulated protein 150)/HSP12A (heat shock protein 12A), a novel stress protein located in the ER, was markedly induced in Purkinje cells maximally at 4-8 d after birth, a developmental period corresponding to their vulnerability to cell death. Both terminal deoxynucleotidyl transferase-mediated biotinylated UTP nick end-labeling analysis and immunostaining using anti-activated caspase-3 antibody revealed that transgenic mice with targeted neuronal overexpression of ORP150 (Tg ORP150) displayed diminished cell death in the Purkinje cell layer and increased numbers of Purkinje cells up to 40 d after birth (p < 0.01), compared with those observed in heterozygous ORP150/HSP12A-deficient (ORP150^+/-) mice and wild-type littermates (ORP150^+/+). Cultured Purkinje cells from Tg ORP150 mice displayed resistance to both hypoxia- and AMPA-induced stress. Behavioral analysis, using rotor rod tasks, indicated impairment of cerebellar function in Tg ORP150 animals, consistent with the concept that enhanced survival of Purkinje cells results in dysfunction. These data suggest that ER chaperones have a pivotal role in Purkinje cell survival and death and thus may highlight the importance of ER stress in neuronal development.

Key words: apoptosis; [Ca]; cerebellum; death; Purkinje cell; glutamate; neuronal cell death; calbindin; cerebellar ataxia

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Received Sep 2, 2003; revised December 15, 2003; accepted December 15, 2003.

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