The Subcellular Localization of an Aquaporin-2 Tetramer Depends on the Stoichiometry of Phosphorylated and Nonphosphorylated Monomers

doi:10.1083/jcb.151.4.919

Published online 13 November 2000. doi:10.1083/jcb.151.4.919

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© The Rockefeller University Press, 0021-9525/2000//919 $5.00
The Journal of Cell Biology, Volume 151, Number 4, , 2000 919-930

Original Article

The Subcellular Localization of an Aquaporin-2 Tetramer Depends on the Stoichiometry of Phosphorylated and Nonphosphorylated Monomers

E.J. Kamsteeg^a, I. Heijnen^a, C.H. van Os^a, and P.M.T. Deen^a

^a Department of Cell Physiology, University Medical Center, St. Radboud, 6500HB Nijmegen, The Netherlands
Department of Cell Physiology, UMC St. Radboud, P.O. Box 9101, 6500HB Nijmegen, The Netherlands.31-24-354052531-24-3617347

In renal principal cells, vasopressin regulates the shuttlingof the aquaporin (AQP)2 water channel between intracellularvesicles and the apical plasma membrane. Vasopressin-inducedphosphorylation of AQP2 at serine 256 (S256) by protein kinaseA (PKA) is essential for its localization in the membrane. However,phosphorylated AQP2 (p-AQP2) has also been detected in intracellularvesicles of noninduced principal cells. As AQP2 is expressedas homotetramers, we hypothesized that the number of p-AQP2monomers in a tetramer might be critical for the its steadystate distribution. Expressed in oocytes, AQP2-S256D and AQP2-S256Amimicked p-AQP2 and non–p-AQP2, respectively, as routingand function of AQP2-S256D and wild-type AQP2 (wt-AQP2) wereidentical, whereas AQP2-S256A was retained intracellularly.In coinjection experiments, AQP2-S256A and AQP2-S256D formedheterotetramers. Coinjection of different ratios of AQP2-S256Aand AQP2-S256D cRNAs revealed that minimally three AQP2-S256Dmonomers in an AQP2 tetramer were essential for its plasma membranelocalization. Therefore, our results suggest that in principalcells, minimally three monomers per AQP2 tetramer have to bephosphorylated for its steady state localization in the apicalmembrane. As other multisubunit channels are also regulatedby phosphorylation, it is anticipated that the stoichiometryof their phosphorylated and nonphosphorylated subunits may fine-tunethe activity or subcellular localization of these complexes.

Key Words: oocytes • trafficking • water channels • kidney • oligomerization

Abbreviations used in this paper: AQP, aquaporin; AVP, argininevasopressin; HbA, homogenization buffer A; MBS, modified Barth'ssolution; MBSS, MED buffered saline for silica; MSB, membranesolubilization buffer; NDI, nephrogenic diabetes mellitus; p-AQP2,PKA-phosphorylated AQP2; Pf, osmotic water permeability; PKA,protein kinase A; PLP, periodate-lysine-paraformaldehyde; wt-AQP2,wild-type AQP2.

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