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Originally published In Press as doi:10.1074/jbc.M207525200 on August 22, 2002

J. Biol. Chem., Vol. 277, Issue 44, 41473-41479, November 1, 2002
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The Role of Putative Phosphorylation Sites in the Targeting and Shuttling of the Aquaporin-2 Water Channel*

Bas W. M. van BalkomDagger §, Paul J. M. SavelkoulDagger §, Daniel MarkovichDagger , Erik HofmanDagger , Soren Nielsen||, Peter van der Sluijs**, and Peter M. T. DeenDagger Dagger Dagger

From the Dagger  Department of Cell Physiology, Nijmegen Center for Molecular Life Sciences, 6500 HB Nijmegen, The Netherlands, the  Department of Physiology and Pharmacology, School of Biomedical Sciences, University of Queensland, Queensland 4072, Brisbane, Australia, the || Water and Salt Research Center, University of Aarhus, DK-8000 Aarhus, Denmark, and the ** Department of Cell Biology, University of Utrecht, 3584 CX Utrecht, The Netherlands

In renal collecting ducts, a vasopressin-induced cAMP increase results in the phosphorylation of aquaporin-2 (AQP2) water channels at Ser-256 and its redistribution from intracellular vesicles to the apical membrane. Hormones that activate protein kinase C (PKC) proteins counteract this process. To determine the role of the putative kinase sites in the trafficking and hormonal regulation of human AQP2, three putative casein kinase II (Ser-148, Ser-229, Thr-244), one PKC (Ser-231), and one protein kinase A (Ser-256) site were altered to mimic a constitutively non-phosphorylated/phosphorylated state and were expressed in Madin-Darby canine kidney cells. Except for Ser-256 mutants, seven correctly folded AQP2 kinase mutants trafficked as wild-type AQP2 to the apical membrane via forskolin-sensitive intracellular vesicles. With or without forskolin, AQP2-Ser-256A was localized in intracellular vesicles, whereas AQP2-S256D was localized in the apical membrane. Phorbol 12-myristate 13-acetate-induced PKC activation following forskolin treatment resulted in vesicular distribution of all AQP2 kinase mutants, while all were still phosphorylated at Ser-256. Our data indicate that in collecting duct cells, AQP2 trafficking to vasopressin-sensitive vesicles is phosphorylation-independent, that phosphorylation of Ser-256 is necessary and sufficient for expression of AQP2 in the apical membrane, and that PMA-induced PKC-mediated endocytosis of AQP2 is independent of the AQP2 phosphorylation state.

* This work was supported by Dutch Organization of Scientific Research Grant NWO-MW 902-18-092 (to P. M. T. D. and P. v. d. S.), European Union Grant QLRT-2000-00778 (to P. M. T. D.), the Danish National Research Foundation (to S. N.), the Australian Research Council, the National Health and Medical Research Council, and the University of Queensland (to D. M.).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.

§ Both authors contributed equally to this work.

Dagger Dagger To whom correspondence should be addressed: 160, Dept. of Cell Physiology, Research Tower, 7th Floor, UMC St. Radboud, P. O. Box 9101, 6500 HB Nijmegen, The Netherlands. Tel.: 31-243617347; Fax: 31-243616413; E-mail: p.deen@ncmls.kun.nl.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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