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MOLECULAR AND GENOMIC |
1 Section of Developmental Neurophysiology, Okazaki Institute for Integrative Bioscience
2 National Institute for Physiological Sciences, National Institutes of Natural Sciences
3 Graduate University for Advanced Studies, Higashiyama 5-1, Myodaijicho, Okazaki, Aichi 444-8787, Japan
Voltage-evoked signals play critical roles in neural activities, muscle contraction and exocytosis. Ciona voltage-sensor containing phosphatase (Ci-VSP) consists of the transmembrane voltage sensor domain (VSD) and a cytoplasmic domain of phosphoinositide phosphatase, homologous to phosphatase and tensin homologue deleted on chromosome 10 (PTEN). Previous experiments utilizing potassium channels as the sensor for phosphoinositides have demonstrated that phosphatase activities of Ci-VSP are voltage dependent. However, it still remained unclear whether enzyme activity is activated by depolarization or hyperpolarization. Further, a large gap in voltage dependency was found between the charge movement of the VSD and potassium channel-reporting phosphatase activities. In this study, voltage-dependent dynamics of phosphoinositides mediated by Ci-VSP were examined by confocal imaging and electrical measurements in Xenopus oocytes. Imaging of phosphatidylinositol-4,5-bisphosphate (PtdIns(4,5)P2) using green fluorescent protein (GFP)-tagged pleckstrin homology (PH) domains from phospholipase C 
subunit (PLC-) showed that PtdIns(4,5)P2 concentration is reduced during depolarization. In the presence of Ci-VSP, IRK1 channels with higher sensitivity to phosphoinositide than GIRK2 channels decreased their magnitude during depolarization over 0 mV, indicating that the PtdIns(4,5)P2 level is reduced upon depolarization. KCNQ2/3 channels coexpressed with Ci-VSP exhibited voltage-dependent decay of the outward current that became sharper with higher depolarization in a voltage range up to 100 mV. These results indicate that Ci-VSP has an activity that depletes PtdIns(4,5)P2 unlike PTEN and that depolarization-activated voltage sensor movement is translated into activation of phosphatase activity.
(Received 18 April 2007;
accepted after revision 3 July 2007;
first published online 5 July 2007)
Corresponding author Y. Okamura: Section of Developmental Neurophysiology, Okazaki Institute for Integrative Bioscience and National Institute for Physiological Sciences, National Institutes of Natural Sciences, Higashiyama 5-1, Myodaijicho, Okazaki, Aichi 444-8787, Japan. Email: yokamura{at}nips.ac.jp*Present address: Department of Physiology I, Tohoku University Graduate School of Medicine, Sendai 980–8575, Japan
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