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Originally published In Press as doi:10.1074/jbc.M401004200 on March 17, 2004

J. Biol. Chem., Vol. 279, Issue 21, 22654-22663, May 21, 2004
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Direct Activation of the Epithelial Na+ Channel by Phosphatidylinositol 3,4,5-Trisphosphate and Phosphatidylinositol 3,4-Bisphosphate Produced by Phosphoinositide 3-OH Kinase*

Qiusheng Tong, Nikita Gamper, Jorge L. Medina, Mark S. Shapiro, and James D. Stockand{ddagger}

From the Department of Physiology, University of Texas Health Science Center, San Antonio, Texas 78229-3900

The phospholipid phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) is accepted to be a direct modulator of ion channel activity. The products of phosphoinositide 3-OH kinase (PI3K), PtdIns(3,4)P2 and phosphatidylinositol 3,4,5-trisphosphate (PtdIns(3,4,5)P3), in contrast, are not. We report here activation of the epithelial Na+ channel (ENaC) reconstituted in Chinese hamster ovary cells by PI3K. Insulin-like growth factor-I also activated reconstituted ENaC and increased Na+ reabsorption across renal A6 epithelial cell monolayers via PI3K. Neither IGF-I nor PI3K affected the levels of ENaC in the plasma membrane. The effects of PI3K and IGF-I on ENaC activity paralleled changes in the plasma membrane levels of the PI3K product phospholipids, PtdIns(3,4)P2/PtdIns(3,4,5)P3, as measured by evanescent field fluorescence microscopy. Both PtdIns(3,4)P2 and PtdIns(3,4,5)P3 activated ENaC in excised patches. Activation of ENaC by PI3K and its phospholipid products corresponded to changes in channel open probability. We conclude that PI3K directly modulates ENaC activity via PtdIns(3,4)P2 and PtdIns(3,4,5)P3. This represents a novel transduction pathway whereby growth factors, such as IGF-I, rapidly modulate target proteins independent of signaling elicited by kinases downstream of PI3K.

Received for publication, January 29, 2004 , and in revised form, March 16, 2004.

* This work was supported by National Institutes of Health (NIH) Grant RO1-DK59594, American Heart Association-Texas Affiliate Grant 0355012Y, and the American Society of Nephrology Carl W. Gottschalk Research Scholar Grant (to J. D. S.), by NIH Grant RO1-NS43394 (to M. S. S.), and by American Heart Association Texas Affiliate Grant 0325120Y (to N. G.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

{ddagger} To whom correspondence should be addressed: Dept. of Physiology 7756, University of Texas Health Science Center, 7703 Floyd Curl Dr., San Antonio, TX 78229-3900. Tel.: 210-567-4332; Fax: 210-567-4410; E-mail: stockand{at}uthscsa.edu.


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