Abstract
The kidneys participate in whole-body homeostasis, regulating acid–base balance, electrolyte concentrations, extracellular fluid volume, and regulation of blood pressure. Many of the kidney’s functions are accomplished by relatively simple mechanisms of filtration, reabsorption, and secretion, which take place in the nephron. The kidneys generate 140–180 l of primary urine per day, while reabsorbing a large percentage, allowing for only the excretion of approximately 2 l of urine. Within the nephron, the majority of the filtered water and solutes are reabsorbed. This is mainly facilitated by specialized transporters and channels which are localized at different segments of the nephron and asymmetrically localized within the polarized epithelial cells. The asymmetric localization of these transporters and channels is essential for the physiological tasks of the renal tissues. One family of these proteins are the water-permeable aquaporins which are selectively expressed in cells along the nephron and localized at different compartments. Here, we discuss potential molecular links between mechanisms involved in the establishment of cell polarity and the members of the aquaporin family. In the first part of this review, we will focus on aspects of apical cell polarity. In the second part, we will review the motifs identified so far that are involved in aquaporin sorting and point out potential molecular links.
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References
Adachi M, Hamazaki Y, Kobayashi Y, Itoh M, Tsukita S, Furuse M, Tsukita S (2009) Similar and distinct properties of MUPP1 and Patj, two homologous PDZ domain-containing tight-junction proteins. Mol Cell Biol 29:2372–2389
Alpi E, Landi E, Barilari M, Serresi M, Salvadori P, Bachi A, Dente L (2009) Channel-interacting PDZ protein, ‘CIPP’, interacts with proteins involved in cytoskeletal dynamics. Biochem J 419:289–300
Anzai N, Deval E, Schaefer L, Friend V, Lazdunski M, Lingueglia E (2002) The multivalent PDZ domain-containing protein CIPP is a partner of acid-sensing ion channel 3 in sensory neurons. J Biol Chem 277:16655–16661
Assemat E, Bazellieres E, Pallesi-Pocachard E, Le BA, Massey-Harroche D (2008) Polarity complex proteins. Biochim Biophys Acta 1778:614–630
Balklava Z, Pant S, Fares H, Grant BD (2007) Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 9:1066–1073
Barile M, Pisitkun T, Yu MJ, Chou CL, Verbalis MJ, Shen RF, Knepper MA (2005) Large scale protein identification in intracellular aquaporin-2 vesicles from renal inner medullary collecting duct. Mol Cell Proteomics 4:1095–1106
Becamel C, Gavarini S, Chanrion B, Alonso G, Galeotti N, Dumuis A, Bockaert J, Marin P (2004) The serotonin 5-HT2A and 5-HT2C receptors interact with specific sets of PDZ proteins. J Biol Chem 279:20257–20266
Beitz E, Liu K, Ikeda M, Guggino WB, Agre P, Yasui M (2006) Determinants of AQP6 trafficking to intracellular sites versus the plasma membrane in transfected mammalian cells. Biol Cell 98:101–109
Boone M, Deen P (2008) Physiology and pathophysiology of the vasopressin-regulated renal water reabsorption. Pflügers Archiv Eur J Physiol 456:1005–1024
Bryant DM, Datta A, Rodriguez-Fraticelli AE, Peranen J, Martin-Belmonte F, Mostov KE (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12:1035–1045
Campbell K, Knust E, Skaer H (2009) Crumbs stabilises epithelial polarity during tissue remodelling. J Cell Sci 122:2604–2612
Colosimo PF, Liu X, Kaplan NA, Tolwinski NS (2010) GSK3+| affects apicalΓÇôbasal polarity and cellΓÇôcell adhesion by regulating aPKC levels. Dev Dyn 239:115–125
Conner MT, Conner AC, Brown JEP, Bill RM (2010) Membrane trafficking of aquaporin 1 is mediated by protein kinase C via microtubules and regulated by tonicity. Biochemistry 49:821–823
De MF, Savelkoul PJ, Kamsteeg EJ, Konings IB, van der Sluijs P, Mallmann R, Oksche A, Deen PM (2005) Lack of arginine vasopressin-induced phosphorylation of aquaporin-2 mutant AQP2-R254L explains dominant nephrogenic diabetes insipidus. J Am Soc Nephrol 16:2872–2880
Djiane A, Yogev S, Mlodzik M (2005) The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell 121:621–631
Duning K, Schurek EM, Schluter M, Bayer M, Reinhardt HC, Schwab A, Schaefer L, Benzing T, Schermer B, Saleem MA, Huber TB et al (2008) KIBRA modulates directional migration of podocytes. J Am Soc Nephrol 19:1891–1903
Elkjar ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frokiar J, Nielsen S (2001) Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Ren Physiol 281:F1047–F1057
Engel A, Fujiyoshi Y, Gonen T, Walz T (2008) Junction-forming aquaporins. Curr Opin Struct Biol 18:229–235
Ernkvist M, Luna PN, Audebert S, Lecine P, Sinha I, Liu M, Schlueter M, Horowitz A, Aase K, Weide T, Borg JP et al (2009) The Amot/Patj/Syx signaling complex spatially controls RhoA GTPase activity in migrating endothelial cells. Blood 113:244–253
Etienne-Manneville S (2008) Polarity proteins in migration and invasion. Oncogene 27:6970–6980
Eto K, Noda Y, Horikawa S, Uchida S, Sasaki S (2010) Phosphorylation of aquaporin-2 regulates its water permeability. J Biol Chem 285:40777–40784
Fan S, Fogg V, Wang Q, Chen XW, Liu CJ, Margolis B (2007) A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J Cell Biol 178:387–398
Fenton RA, Moeller HB, Hoffert JD, Yu MJ, Nielsen S, Knepper MA (2008) Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin. Proc Natl Acad Sci U S A 105:3134–3139
Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GR, Srivastava S, Baldwin SA, Prekeris R, Gould GW (2005) Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 24:3389–3399
Fliegauf M, Benzing T, Omran H (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8:880–893
Fujiwara TM, Bichet DG (2005) Molecular biology of hereditary diabetes insipidus. J Am Soc Nephrol 16:2836–2846
Funaki H, Yamamoto T, Koyama Y, Kondo D, Yaoita E, Kawasaki K, Kobayashi H, Sawaguchi S, Abe H, Kihara I (1998) Localization and expression of AQP5 in cornea, serous salivary glands, and pulmonary epithelial cells. Am J Physiol 275:C1151–C1157
Garcia F, Kierbel A, Larocca MC, Gradilone SA, Splinter P, LaRusso NF, Marinelli RA (2001) The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J Biol Chem 276:12147–12152
Godde NJ, Galea RC, Elsum IA, Humbert PO (2010) Cell polarity in motion: redefining mammary tissue organization through EMT and cell polarity transitions. J Mammary Gland Biol Neoplasia 15:149–168
Golachowska MR, Hoekstra D, van IJzendoorn SC (2010) Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol 20:618–626
Gosens I, den Hollander AI, Cremers FP, Roepman R (2008) Composition and function of the Crumbs protein complex in the mammalian retina. Exp Eye Res 86:713–726
Gosens I, Sessa A, den Hollander AI, Letteboer SJ, Belloni V, Arends ML, Le BA, Cremers FP, Broccoli V, Roepman R (2007) FERM protein EPB41L5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp Cell Res 313:3959–3970
Grunfeld JP, Rossier BC (2009) Lithium nephrotoxicity revisited. Nat Rev Nephrol 5:270–276
Grusche FA, Richardson HE, Harvey KF (2010) Upstream regulation of the hippo size control pathway. Curr Biol 20:R574–R582
Guan XG, Su WH, Yi F, Zhang D, Hao F, Zhang HG, Liu YJ, Feng XC, Ma TH (2010) NPA motifs play a key role in plasma membrane targeting of aquaporin-4. IUBMB Life 62:222–226
Hara-Chikuma M, Verkman AS (2005) Aquaporin-3 functions as a glycerol transporter in mammalian skin. Biol Cell 97:479–486
Hara-Chikuma M, Verkman AS (2008) Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol 28:326–332
Heller B, du-Gyamfi E, Smith-Kinnaman W, Babbey C, Vora M, Xue Y, Bittman R, Stahelin RV, Wells CD (2010) Amot recognizes a juxtanuclear endocytic recycling compartment via a novel lipid binding domain. J Biol Chem 285:12308–12320
Henn V, Edemir B, Stefan E, Wiesner B, Lorenz D, Theilig F, Schmitt R, Vossebein L, Tamma G, Beyermann M, Krause E et al (2004) Identification of a novel A-kinase anchoring protein 18 isoform and evidence for its role in the vasopressin-induced aquaporin-2 shuttle in renal principal cells. J Biol Chem 279:26654–26665
Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pisitkun T, Chen F, Knepper MA (2008) Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283:24617–24627
Hoffert JD, Pisitkun T, Wang G, Shen RF, Knepper MA (2006) Quantitative phosphoproteomics of vasopressin-sensitive renal cells: regulation of aquaporin-2 phosphorylation at two sites. Proc Natl Acad Sci U S A 103:7159–7164
Hurd TW, Gao L, Roh MH, Macara IG, Margolis B (2003) Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol 5:137–142
Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J Biol Chem 277:39873–39879
Illarionova NB, Gunnarson E, Li Y, Brismar H, Bondar A, Zelenin S, Aperia A (2010) Functional and molecular interactions between aquaporins and Na, K-ATPase. Neuroscience 168:915–925
Inoue T, Nielsen S, Mandon B, Terris J, Kishore BK, Knepper MA (1998) SNAP-23 in rat kidney: colocalization with aquaporin-2 in collecting duct vesicles. Am J Physiol 275:F752–F760
Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117
Ishibashi K, Imai M, Sasaki S (2000) Cellular localization of aquaporin 7 in the rat kidney. Exp Nephrol 8:252–257
Jensen AM, Westerfield M (2004) Zebrafish mosaic eyes is a novel FERM protein required for retinal lamination and retinal pigmented epithelial tight junction formation. Curr Biol 14:711–717
Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531–539
Kamberov E, Makarova O, Roh M, Liu A, Karnak D, Straight S, Margolis B (2000) Molecular cloning and characterization of Pals, proteins associated with mLin-7. J Biol Chem 275:11425–11431
Kamsteeg EJ, Savelkoul PJ, Hendriks G, Konings IB, Nivillac NM, Lagendijk AK, van der Sluijs P, Deen PM (2008) Missorting of the aquaporin-2 mutant E258K to multivesicular bodies/lysosomes in dominant NDI is associated with its monoubiquitination and increased phosphorylation by PKC but is due to the loss of E258. Pflugers Arch 455:1041–1054
Kamsteeg EJ, Wormhoudt TA, Rijss JP, van Os CH, Deen PM (1999) An impaired routing of wild-type aquaporin-2 after tetramerization with an aquaporin-2 mutant explains dominant nephrogenic diabetes insipidus. EMBO J 18:2394–2400
Kamsteeg EJ, Duffield AS, Konings IBM, Spencer J, Pagel P, Deen PMT, Caplan MJ (2007) MAL decreases the internalization of the aquaporin-2 water channel. PNAS 104:16696–16701
Katsura T, Gustafson CE, Ausiello DA, Brown D (1997) Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am J Physiol 272:F817–F822
Kawedia JD, Nieman ML, Boivin GP, Melvin JE, Kikuchi KI, Hand AR, Lorenz JN, Menon AG (2007) Interaction between transcellular and paracellular water transport pathways through aquaporin 5 and the tight junction complex. PNAS 104:3621–3626
Kemphues KJ, Priess JR, Morton DG, Cheng NS (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311–320
Kim M, Datta A, Brakeman P, Yu W, Mostov KE (2007) Polarity proteins PAR6 and aPKC regulate cell death through GSK-3beta in 3D epithelial morphogenesis. J Cell Sci 120:2309–2317
Klokkers J, Langehanenberg P, Kemper B, Kosmeier S, von BG, Riethmuller C, Wunder F, Sindic A, Pavenstadt H, Schlatter E, Edemir B (2009) Atrial natriuretic peptide and nitric oxide signaling antagonizes vasopressin-mediated water permeability in inner medullary collecting duct cells. Am J Physiol Ren Physiol 297:F693–F703
Klussmann E, Maric K, Wiesner B, Beyermann M, Rosenthal W (1999) Protein kinase A anchoring proteins are required for vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J Biol Chem 274:4934–4938
Kosugi-Tanaka C, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K (2006) Protein kinase A-regulated membrane trafficking of a green fluorescent protein-aquaporin 5 chimera in MDCK cells. Biochim Biophys Acta BBA Mol Cell Res 1763:337–344
Kurschner C, Mermelstein PG, Holden WT, Surmeier DJ (1998) CIPP, a novel multivalent PDZ domain protein, selectively interacts with Kir4.0 family members, NMDA receptor subunits, neurexins, and neuroligins. Mol Cell Neurosci 11:161–172
Kuwahara M, Iwai K, Ooeda T, Igarashi T, Ogawa E, Katsushima Y, Shinbo I, Uchida S, Terada Y, Arthus MF, Lonergan M et al (2001) Three families with autosomal dominant nephrogenic diabetes insipidus caused by aquaporin-2 mutations in the C-terminus. Am J Hum Genet 69:738–748
Laforenza U, Gastaldi G, Grazioli M, Cova E, Tritto S, Faelli A, Calamita G, Ventura U (2005) Expression and immunolocalization of aquaporin-7 in rat gastrointestinal tract. Biol Cell 97:605–613
Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, Tepass U (2006) The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell 11:363–374
Lemmers C, Medina E, Delgrossi MH, Michel D, Arsanto JP, Le BA (2002) hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J Biol Chem 277:25408–25415
Lemmers C, Michel D, Lane-Guermonprez L, Delgrossi MH, Medina E, Arsanto JP, Le BA (2004) CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol Biol Cell 15:1324–1333
Li Z, Wang L, Hays TS, Cai Y (2008) Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity. J Cell Biol 180:31–38
Lu DC, Zhang H, Zador Z, Verkman AS (2008) Impaired olfaction in mice lacking aquaporin-4 water channels. FASEB J 22:3216–3223
Lu H, Sun TX, Bouley R, Blackburn K, McLaughlin M, Brown D (2004) Inhibition of endocytosis causes phosphorylation (S256)-independent plasma membrane accumulation of AQP2. Am J Physiol Ren Physiol 286:F233–F243
Lu HAJ, Sun TX, Matsuzaki T, Yi XH, Eswara J, Bouley R, McKee M, Brown D (2007) Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. J Biol Chem 282:28721–28732
Lu HJ, Matsuzaki T, Bouley R, Hasler U, Qin QH, Brown D (2008) The phosphorylation state of serine 256 is dominant over that of serine 261 in the regulation of AQP2 trafficking in renal epithelial cells. Am J Physiol Ren Physiol 295:F290–F294
Ma T, Yang B, Matthay MA, Verkman AS (1998) Evidence against a role of mouse, rat, and two cloned human t1alpha isoforms as a water channel or a regulator of aquaporin-type water channels. Am J Respir Cell Mol Biol 19:143–149
Macara IG (2004) Parsing the polarity code. Nat Rev Mol Cell Biol 5:220–231
Madrid R, Le Maout S, Barrault MB, Janvier K, Benichou S, Merot J (2001) Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J 20:7008–7021
Makarova O, Roh MH, Liu CJ, Laurinec S, Margolis B (2003) Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302:21–29
Marazuela M, Alonso MA (2004) Expression of MAL and MAL2, two elements of the protein machinery for raft-mediated transport, in normal and neoplastic human tissue. Histol Histopathol 19:925–933
Marples D, Barber B, Taylor A (1996) Effect of a dynein inhibitor on vasopressin action in toad urinary bladder. J Physiol 490:767–774
Marples D, Schroer TA, Ahrens N, Taylor A, Knepper MA, Nielsen S (1998) Dynein and dynactin colocalize with AQP2 water channels in intracellular vesicles from kidney collecting duct. Am J Physiol Ren Physiol 274:F384–F394
Massari S, Perego C, Padovano V, DΓÇÖAmico A, Raimondi A, Francolini M, Pietrini G (2009) LIN7 mediates the recruitment of IRSp53 to tight junctions. Traffic 10:246–257
McNeill H (2009) Planar cell polarity and the kidney. J Am Soc Nephrol 20:2104–2111
Mistry AC, Mallick R, Klein JD, Weimbs T, Sands JM, Frohlich O (2009) Syntaxin specificity of aquaporins in the inner medullary collecting duct. Am J Physiol Ren Physiol 297:F292–F300
Moeller HB, Knepper MA, Fenton RA (2009) Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells. Kidney Int 75:295–303
Moeller HB, Macaulay N, Knepper MA, Fenton RA (2009) Role of multiple phosphorylation sites in the COOH-terminal tail of aquaporin-2 for water transport: evidence against channel gating. Am J Physiol Ren Physiol 296:F649–F657
Monzani E, Bazzotti R, Perego C, La Porta CAM (2009) AQP1 is not only a water channel: it contributes to cell migration through Lin7/Beta-Catenin. PLoS ONE 4:e6167
Mulders SM, van der Kemp AJ, Terlouw SA, van Boxtel HAF, van Os CH, Deen PMT (1998) The exchange of functional domains among aquaporins with different transport characteristics. Pflugers Arch 436:599–607
Nagai K, Watanabe M, Seto M, Hisatsune A, Miyata T, Isohama Y (2007) Nitric oxide decreases cell surface expression of aquaporin-5 and membrane water permeability in lung epithelial cells. Biochem Biophys Res Commun 354:579–584
Nedvetsky PI, Tamma G, Beulshausen S, Valenti G, Rosenthal W, Klussmann E (2009) Regulation of aquaporin-2 trafficking. Handb Exp Pharmacol (190):133–157
Nedvetsky PI, Stefan E, Frische S, Santamaria K, Wiesner B, Valenti G, Hammer JA, Nielsen S, Goldenring JR, Rosenthal W, Klussmann E (2007) A role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle. Traffic 8:110–123
Nedvetsky PI, Tabor V, Tamma G, Beulshausen S, Skroblin P, Kirschner A, Mutig K, Boltzen M, Petrucci O, Vossenkämper A, Wiesner B et al (2010) Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAP kinase. J Am Soc Nephrol 21:1645–1656
Nejsum LN, Nelson WJ (2007) A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J Cell Biol 178:323–335
Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci U S A 92:1013–1017
Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW (1993) Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. PNAS 90:11663–11667
Nielsen S, Frøkiaer J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82:205–244
Nielsen S, Kwon TH, Christensen BM, Promeneur D, FrokiAEr J, Marples D (1999) Physiology and pathophysiology of renal aquaporins. J Am Soc Nephrol 10:647–663
Nielsen S, Marples D, Birn H, Mohtashami M, Dalby NO, Trimble M, Knepper M (1995) Expression of VAMP-2-like protein in kidney collecting duct intracellular vesicles. Colocalization with aquaporin-2 water channels. J Clin Invest 96:1834–1844
Nielsen S, Pallone T, Smith BL, Christensen EI, Agre P, Maunsbach AB (1995) Aquaporin-1 water channels in short and long loop descending thin limbs and in descending vasa recta in rat kidney. Am J Physiol 268:F1023–F1037
Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993) CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120:371–383
Nielsen S, Frokiar J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82:205–244
Noda Y, Sasaki S (2005) Trafficking mechanism of water channel aquaporin-2. Biol Cell 97:885–892
Noda Y, Sohara E, Ohta E, Sasaki S (2010) Aquaporins in kidney pathophysiology. Nat Rev Nephrol 6:168–178
Noda Y, Horikawa S, Kanda E, Yamashita M, Meng H, Eto K, Li Y, Kuwahara M, Hirai K, Pack C, Kinjo M et al (2008) Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking. J Cell Biol 182:587–601
O’Brien LE, Zegers MMP, Mostov KE (2002) Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3:531–537
Papadopoulos M, Verkman A (2007) Aquaporin-4 and brain edema. Pediatr Nephrol 22:778–784
Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci U S A 88:11110–11114
Procino G, Barbieri C, Tamma G, De Benedictis L, Pessin JE, Svelto M, Valenti G (2008) AQP2 exocytosis in the renal collecting duct—involvement of SNARE isoforms and the regulatory role of Munc18b. J Cell Sci 121:2097–2106
Quaggin SE, Kreidberg JA (2008) Development of the renal glomerulus: good neighbors and good fences. Development 135:609–620
Rai T, Sasaki S, Uchida S (2006) Polarized trafficking of the aquaporin-3 water channel is mediated by an NH2-terminal sorting signal. Am J Physiol Cell Physiol 290:C298–C304
Rao R, Patel S, Hao C, Woodgett J, Harris R (2010) GSK3{beta} mediates renal response to vasopressin by modulating adenylate cyclase activity. J Am Soc Nephrol 21:428–437
Roeth JF, Sawyer JK, Wilner DA, Peifer M (2009) Rab11 helps maintain apical crumbs and adherens junctions in the Drosophila embryonic ectoderm. PLoS ONE 4:e7634
Roh MH, Liu CJ, Laurinec S, Margolis B (2002) The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions. J Biol Chem 277:27501–27509
Roh MH, Makarova O, Liu CJ, Shin K, Lee S, Laurinec S, Goyal M, Wiggins R, Margolis B (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of crumbs and discs lost. J Cell Biol 157:161–172
Rohr S, Bit-Avragim N, Bdelilah-Seyfried S (2006) Heart and soul/PRKCi and nagie oko/Mpp 5 regulate myocardial coherence and remodeling during cardiac morphogenesis. Development 133:107–115
Rojek A, Praetorius J, Frøkiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327
Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792
Savelkoul PJ, De MF, Li Y, Kamsteeg EJ, Konings IB, van der SP, Deen PM (2009) p.R254Q mutation in the aquaporin-2 water channel causing dominant nephrogenic diabetes insipidus is due to a lack of arginine vasopressin-induced phosphorylation. Hum Mutat 30:E891–E903
Schlüter MA, Margolis B (2009) Apical lumen formation in renal epithelia. J Am Soc Nephrol 20:1444–1452
Schlüter MA, Pfarr CS, Pieczynski J, Whiteman EL, Hurd TW, Fan S, Liu CJ, Margolis B (2009) Trafficking of crumbs3 during cytokinesis is crucial for lumen formation. Mol Biol Cell 20(22):4652–4663
Schnermann J, Chou CL, Ma T, Traynor T, Knepper MA, Verkman AS (1998) Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice. Proc Natl Acad Sci U S A 95:9660–9664
Schrier RW, Berl T, Anderson RJ (1979) Osmotic and nonosmotic control of vasopressin release. Am J Physiol 236:F321–F332
Shin K, Fogg VC, Margolis B (2006) Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207–235
Shin K, Straight S, Margolis B (2005) PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J Cell Biol 168:705–711
Shin K, Wang Q, Margolis B (2007) PATJ regulates directional migration of mammalian epithelial cells. EMBO Rep 8:158–164
Shivas JM, Morrison HA, Bilder D, Skop AR (2010) Polarity and endocytosis: reciprocal regulation. Trends Cell Biol 20:445–452
Sohara E, Rai T, Sasaki S, Uchida S (2006) Physiological roles of AQP7 in the kidney: lessons from AQP7 knockout mice. Biochim Biophys Acta BBA Biomembr 1758:1106–1110
Straight SW, Shin K, Fogg VC, Fan S, Liu CJ, Roh M, Margolis B (2004) Loss of PALS1 expression leads to tight junction and polarity defects. Mol Biol Cell 15:1981–1990
Sun TX, Van HA, Huang Y, Bouley R, McLaughlin M, Brown D (2002) Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin. Am J Physiol Ren Physiol 282:F998–F1011
Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979–987
Tabuse Y, Izumi Y, Piano F, Kemphues KJ, Miwa J, Ohno S (1998) Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125:3607–3614
Tajika Y, Matsuzaki T, Suzuki T, Ablimit A, Aoki T, Hagiwara H, Kuwahara M, Sasaki S, Takata K (2005) Differential regulation of AQP2 trafficking in endosomes by microtubules and actin filaments. Histochem Cell Biol 124:1–12
Tajika Y, Matsuzaki T, Suzuki T, Aoki T, Hagiwara H, Kuwahara M, Sasaki S, Takata K (2004) Aquaporin-2 is retrieved to the apical storage compartment via early endosomes and phosphatidylinositol 3-kinase-dependent pathway. Endocrinology 145:4375–4383
Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83
Tamma G, Klussmann E, Oehlke J, Krause E, Rosenthal W, Svelto M, Valenti G (2005) Actin remodeling requires ERM function to facilitate AQP2 apical targeting. J Cell Sci 118:3623–3630
Tamma G, Robben JH, Trimpert C, Boone M, Deen PMT (2011) Regulation of AQP2 localization by Ser256 and S261 phosphorylation and ubiquitination. Am J Physiol Cell Physiol (in press)
Tepass U (2009) FERM proteins in animal morphogenesis. Curr Opin Genet Dev 19:357–367
Tepass U, Knust E (1993) Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev Biol 159:311–326
Valenti G, Hugon JS, Bourguet J (1988) To what extent is microtubular network involved in antidiuretic response? Am J Physiol Ren Physiol 255:F1098–F1106
van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, van der SP, Deen PM (2002) The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277:41473–41479
Verkman AS (2009) Aquaporins: translating bench research to human disease. J Exp Biol 212:1707–1715
Wallingford JB (2010) Planar cell polarity signaling, cilia and polarized ciliary beating. Curr Opin Cell Biol 22:597–604
Wang Q, Chen XW, Margolis B (2007) PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol Biol Cell 18:874–885
Wang Q, Margolis B (2007) Apical junctional complexes and cell polarity. Kidney Int 72:1448–1458
Wei X, Malicki J (2002) Nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet 31:150–157
Weisz OA, Rodriguez-Boulan E (2009) Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 122:4253–4266
Wellner RB, Hoque AT, Goldsmith CM, Baum BJ (2000) Evidence that aquaporin-8 is located in the basolateral membrane of rat submandibular gland acinar cells. Pflugers Arch 441:49–56
Wellner RB, Baum BJ (2001) Polarized sorting of aquaporins 5 and 8 in stable MDCK-II transfectants. Biochem Biophys Res Commun 285:1253–1258
Wellner RB, Hong S, Cotrim AP, Swaim WD, Baum BJ (2005) Modifying the NH2 and COOH termini of aquaporin-5: effects on localization in polarized epithelial cells. Tissue Eng 11:1449–1458
Wells CD, Fawcett JP, Traweger A, Yamanaka Y, Goudreault M, Elder K, Kulkarni S, Gish G, Virag C, Lim C, Colwill K et al (2006) A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125:535–548
Welte MA (2004) Bidirectional transport along microtubules. Curr Biol 14:R525–R537
Yamanaka T, Ohno S (2008) Role of Lgl/Dlg/Scribble in the regulation of epithelial junction, polarity and growth. Front Biosci 13:6693–6707
Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P (1999) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–187
Yasui M, Kwon TH, Knepper MA, Nielsen S, Agre P (1999) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci U S A 96:5808–5813
Zhang W, Zitron E, Hömme M, Kihm L, Morath C, Scherer D, Hegge S, Thomas D, Schmitt CP, Zeier M, Katus H et al (2007) Aquaporin-1 channel function is positively regulated by protein kinase C. J Biol Chem 282:20933–20940
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We thank Dr. Marc Schlüter for careful and critical reading of the manuscript and all members of our laboratories for helpful discussion.
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Edemir, B., Pavenstädt, H., Schlatter, E. et al. Mechanisms of cell polarity and aquaporin sorting in the nephron. Pflugers Arch - Eur J Physiol 461, 607–621 (2011). https://doi.org/10.1007/s00424-011-0928-3
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DOI: https://doi.org/10.1007/s00424-011-0928-3