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Vol. 19, Issue 10, 4213-4223, October 2008

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Rapid Turnover Rate of Phosphoinositides at the Front of Migrating MDCK Cells

Teruko Nishioka^*, Kazuhiro Aoki^*, Kazuhiro Hikake^*, Hisayoshi Yoshizaki, Etsuko Kiyokawa^*, and Michiyuki Matsuda^*

*Laboratory of Bioimaging and Cell Signaling, Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan; and Department of Structural Analysis, National Cardiovascular Center Research Institute, Suita, Osaka 565-8565, Japan

Submitted March 25, 2008; Revised July 14, 2008; Accepted July 29, 2008
Monitoring Editor: Mark H. Ginsberg

InCytes from MBC

Phosphoinositides (PtdInss) play key roles in cell polarization and motility. With a series of biosensors based on Förster resonance energy transfer, we examined the distribution and metabolism of PtdInss and diacylglycerol (DAG) in stochastically migrating Madin-Darby canine kidney (MDCK) cells. The concentrations of phosphatidylinositol (4,5)-bisphosphate, phosphatidylinositol (3,4,5)-trisphosphate (PIP₃), phosphatidylinositol (3,4)-bisphosphate, and DAG were higher at the plasma membrane in the front of the cell than at the plasma membrane of the rear of the cell. The difference in the concentrations of PtdInss was estimated to be less than twofold between the front and rear of the migrating MDCK cells. To decode the spatial activities of PtdIns metabolic enzymes from the obtained concentration maps of PtdInss, we developed a one-dimensional reaction diffusion model of PtdIns metabolism. In this model, the activities of phosphatidylinositol monophosphate 5-kinase, phosphatidylinositol 3-kinase, phospholipase C, and PIP₃ 5-phosphatases were higher at the plasma membrane of the front than at the plasma membrane of the rear of the cell. This result suggests that, although the difference in the steady-state level of PtdInss is less than twofold, PtdInss were more rapidly turned over at the front than the rear of the migrating MDCK cells.

Address correspondence to: Etsuko Kiyokawa (kiyokawa{at}lif.kyoto-u.ac.jp)

Abbreviations used: PtdInss, phosphoinositides; PI(4,5)P₂, phosphatidylinositol (4,5)-bisphosphate; PIP, phosphatidylinositol monophosphate; IP₃, inositol (1,4,5)-trisphosphate; DAG, diacylglycerol; PIP₃, phosphatidylinositol (3,4,5)-trisphosphate; PH, pleckstrin homology; GFP, green fluorescent protein; FRET, Förster resonance energy transfer; PI(3,4)P₂, phosphatidylinositol (3,4)-bisphosphate; Pippi, phosphatidylinositol phosphate indicator; PLC, phospholipase C; CFP, cyan fluorescent protein; YFP, yellow fluorescent protein; PDGF, platelet-derived growth factor; Digda, diacylglycerol indicator; OAG, 1-oleoyl-2-acetylglycerol; PI(4)P, phosphatidylinositol (4)-monophosphate; PAO, phenylarsine oxide; PI 4-kinase, phosphatidylinositol 4-kinase; FKBP, FK506-binding protein; 5ptase, phosphoinositide 5-phosphatase; FRB, fragment of mammalian target of rapamycin; PI3-kinase, phosphatidylinositol 3-kinase; PA, phosphatidic acid; PI(4)P 5-kinase, phosphatidylinositol (4)-monophosphate 5-kinase; PIP₂ 5-Pase, PIP₂ 5-phosphatase; PTEN, phosphatase and tensin homologue; PIP₃ 5-Pase, PIP₃ 5-phosphatase.

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