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Originally published In Press as doi:10.1074/jbc.M105673200 on July 23, 2001

J. Biol. Chem., Vol. 276, Issue 38, 35622-35628, September 21, 2001
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Involvement of Phospholipase D in Sphingosine 1-Phosphate-induced Activation of Phosphatidylinositol 3-Kinase and Akt in Chinese Hamster Ovary Cells Overexpressing EDG3*

Yoshiko BannoDagger §, Yoh Takuwa, Yukihiro Akao||, Hiroyuki Okamoto, Yosuke Osawa**, Takashi NaganawaDagger , Shigeru NakashimaDagger , Pann-Ghill SuhDagger Dagger , and Yoshinori Nozawa||

From the Departments of Dagger  Biochemistry and ** Internal Medicine, Gifu University School of Medicine, Gifu 500-8705, Japan,  Department of Physiology, Kanazawa University School of Medicine, Kanazawa 920-8640, Japan, || Gifu International Institute of Biotechnology and Institute of Applied Biochemistry, Mitake, Gifu 505-0116, Japan, and Dagger Dagger  Department of Life Science, Division of Molecular and Life Sciences, Pohang University of Science & Technology, Pohang 790-784, South Korea

Phospholipase D (PLD), phosphatidylinositol 3-kinase (PI3K), and Akt are known to be involved in cellular signaling related to proliferation and cell survival. In this report, we provide evidence that PLD links sphingosine 1-phosphate (S1P)-induced activation of the G protein-coupled EDG3 receptor to stimulation of PI3K and its downstream effector Akt in Chinese hamster ovary (CHO) cells. S1P stimulation of EDG3-overexpressing CHO cells but not vector-transfected cells induced activation of PLD, PI3K, and Akt in a time- and dose-dependent manner. Akt phosphorylation was prevented by the PI3K inhibitors wortmannin and LY294002 (2-(4-monrpholinyl)-8-phenyl-4H-1-benzopyran-4-one), indicating that Akt activation was dependent on PI3K. S1P-induced activation of PI3K and Akt was abrogated by 1-butanol, which inhibited S1P-induced accumulation of phosphatidic acid by serving as a phosphatidyl group acceptor in the transphosphatidylation reaction catalyzed by PLD, whereas both PI3K and Akt activation were not inhibited by 2-butanol without such reaction. Co-expression of wild-type PLD2 with myc-Akt resulted in increased Akt activation in response to S1P. In contrast, co-expression of a catalytically inactive mutant of PLD2 eliminated the S1P-induced Akt activation. The treatment of EDG3-expressing CHO cells with exogenous Streptomyces chromofuscus PLD, which caused an accumulation of phosphatidic acid, resulted in increases in PI3K activity and the phosphorylation of Akt, the latter of which was completely abolished by LY294002. Furthermore, S1P-induced membrane ruffling, which was dependent on PI3K and Rac, was inhibited by 1-butanol, but not by 2-butanol. These results demonstrate that PLD participates in the activation of PI3K and Akt stimulation of EDG3 receptor.

* This work was supported in part by Grants-in-aid for Scientific Research on Priority Areas 09273104 and 10212204 and Grants-in-aid for Scientific Research (C) 12680633 from the Ministry of Education, Science, Sports, and Culture of Japan.The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Dept. of Biochemistry, Gifu University School of Medicine, Tsukasamachi-40, Gifu, 500-8705, Japan. Tel.: 81-58-267-2229; Fax: 81-58-265-9002; E-mail; banno@cc.gifu-u.ac.jp.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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