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Abstract
In renal collecting ducts, vasopressin increases the expression of and redistributes aquaporin-2 (AQP2) water channels from intracellular vesicles to the apical membrane, leading to urine concentration. However, basolateral membrane expression of AQP2, in addition to AQP3 and AQP4, is often detected in inner medullary principal cells in vivo. Here, potential mechanisms that regulate apical versus basolateral targeting of AQP2 were examined. The lack of AQP2-4 association into heterotetramers and the complete apical expression of AQP2 when highly expressed in Madin-Darby canine kidney cells indicated that neither heterotetramerization of AQP2 with AQP3 and/or AQP4, nor high expression levels of AQP2 explained the basolateral AQP2 localization. However, long term hypertonicity, a feature of the inner medullary interstitium, resulted in an insertion of AQP2 into the basolateral membrane of Madin-Darby canine kidney cells after acute forskolin stimulation. Similarly, a marked insertion of AQP2 into the basolateral membrane of principal cells was observed in the distal inner medulla from normal rats and Brattleboro rats after acute vasopressin treatment of tissue slices that had been chronically treated with vasopressin to increase interstitial osmolality in the medulla, but not in tissues from vasopressin-deficient Brattleboro rats. These data reveal for the first time that chronic hypertonicity can program cells in vitro and in vivo to change the insertion of a protein into the basolateral membrane instead of the apical membrane.
Highlights
The renal collecting duct is involved in urine concentration via a process that is regulated by the antidiuretic hormone arginine vasopressin (AVP).1 After binding to its receptor on
Aquaporin-3 Is Expressed as Tetramers—To be able to address this hypothesis, it is essential that AQP2, AQP3, and AQP4 are all expressed as tetramers and that the tetramers are not disrupted by the membrane isolation and extraction procedure
Whereas it has been shown that AQP2 and AQP4 form homotetramers (16, 37), this has not been reported for AQP3
Summary
The renal collecting duct is involved in urine concentration via a process that is regulated by the antidiuretic hormone arginine vasopressin (AVP). After binding to its receptor on. The majority of AQP2 is located in the apical plasma membrane under “steady-state” conditions in normally hydrated animals, immunocytochemical studies have shown that AQP2 antigenicity can be detected in the basolateral plasma membrane of collecting duct principal cells in these rats. This basolateral staining pattern becomes more prominent with increased AVP levels or water deprivation in rats, and is especially prominent in the principal cells of the inner medulla (11). Our data indicate that long term exposure of cells to hypertonicity primes epithelial cells to insert AQP2 into the basolateral membrane upon acute stimulation with AVP and/or forskolin
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