Aquaporin 2: From its discovery to molecular structure and medical implications

Abraham, 2006, Aquaretic effect of lixivaptan, an oral, non-peptide, selective V2 receptor vasopressin antagonist, in New York Heart Association functional class II and III chronic heart failure patients, J. Am. Coll. Cardiol., 47, 1615, 10.1016/j.jacc.2005.11.071

Agre, 1998, The aquaporins, blueprints for cellular plumbing systems, J. Biol. Chem., 273, 14659, 10.1074/jbc.273.24.14659

Agre, 1993, Aquaporins: a family of water channel proteins, Am. J. Physiol., 265, F461

Asahina, 1995, Increased gene expression of water channel in cirrhotic rat kidneys, Hepatology, 21, 169, 10.1002/hep.1840210128

Asai, 2003, Pathogenesis of nephrogenic diabetes insipidus by aquaporin-2 C-terminus mutations, Kidney Int., 64, 2, 10.1046/j.1523-1755.2003.00049.x

Babey, 2011, Familial forms of diabetes insipidus: clinical and molecular characteristics, Nat. Rev. Endocrinol., 7, 701, 10.1038/nrendo.2011.100

Bai, 1996, Structure of aquaporin-2 vasopressin water channel, J. Biol. Chem., 271, 5171, 10.1074/jbc.271.9.5171

Benga, 1986, P-(Chloromercuri)benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes, Biochemistry, 25, 1535, 10.1021/bi00355a011

Bouley, 2000, Nitric oxide and atrial natriuretic factor stimulate cGMP-dependent membrane insertion of aquaporin 2 in renal epithelial cells, J. Clin. Invest., 106, 1115, 10.1172/JCI9594

Bouley, 2006, Aquaporin 2 (AQP2) and vasopressin type 2 receptor (V2R) endocytosis in kidney epithelial cells: AQP2 is located in ‘endocytosis-resistant’ membrane domains after vasopressin treatment, Biol. Cell, 98, 215, 10.1042/BC20040054

Brown, 2008, Phosphorylation events and the modulation of aquaporin 2 cell surface expression, Curr. Opin. Nephrol. Hypertens., 17, 491, 10.1097/MNH.0b013e3283094eb1

Buemi, 2001, Urinary excretion of aquaporin-2 water channel during pregnancy, Cell Physiol. Biochem., 11, 203, 10.1159/000047807

Chevalier, 1974, Membrane associated particles: distribution in frog urinary bladder epithelium at rest and after oxytocin treatment, Cell Tissue Res., 152, 129, 10.1007/BF00224690

Deen, 1995, Water channels encoded by mutant aquaporin-2 genes in nephrogenic diabetes insipidus are impaired in their cellular routing, J. Clin. Invest., 95, 2291, 10.1172/JCI117920

Deen, 1994, Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine, Science, 264, 92, 10.1126/science.8140421

DiGiovanni, 1994, Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat, Proc. Natl. Acad. Sci. USA, 91, 8984, 10.1073/pnas.91.19.8984

Domeniconi, 2008, Immunolocalization of aquaporins 1, 2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog, Cell Tissue Res., 332, 329, 10.1007/s00441-008-0592-x

Fenton, 2008, Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin, Proc. Natl. Acad. Sci. USA, 105, 3134, 10.1073/pnas.0712338105

Fushimi, 1997, Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel, J. Biol. Chem., 272, 14800, 10.1074/jbc.272.23.14800

Fushimi, 1994, Functional characterization and cell immunolocalization of AQP-CD water channel in kidney collecting duct, Am. J. Physiol., 267, F573

Fushimi, 1993, Cloning and expression of apical membrane water channel of rat kidney collecting tubule, Nature, 361, 549, 10.1038/361549a0

Gheorghiade, M., Konstam, M.A., Burnett, J.C., Grinfeld, L., Maggioni, A.P., Swedberg, K., Udelson, J.E., Zannad, F., Cook, T., Ouyang, J., Zimmer, C., Orlandi, C., Investigators, E.o.V.A.i.H.F.O.S.W.T., 2007. Short-term clinical effects of tolvaptan, an oral vasopressin antagonist, in patients hospitalized for heart failure: the EVEREST Clinical Status Trials. JAMA 297 (12), 1332–1343.

Gorin, 1984, The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning, Cell, 39, 49, 10.1016/0092-8674(84)90190-9

Handler, 1988, Antidiuretic hormone moves membranes, Am. J. Physiol., 255, F375

Harris, 1988, Identification of specific apical membrane polypeptides associated with the antidiuretic hormone-elicited water permeability increase in the toad urinary bladder, Proc. Natl. Acad. Sci. USA, 85, 1942, 10.1073/pnas.85.6.1942

Hasler, 2006, Posttranscriptional control of aquaporin-2 abundance by vasopressin in renal collecting duct principal cells, Am. J. Physiol. Renal Physiol., 290, F177, 10.1152/ajprenal.00056.2005

Hayashi, 1994, Expression and distribution of aquaporin of collecting duct are regulated by vasopressin V2 receptor in rat kidney, J. Clin. Invest., 94, 1778, 10.1172/JCI117525

Hayashi, 1997, Expression and localization of the water channels in human autosomal dominant polycystic kidney disease, Nephron, 75, 321, 10.1159/000189556

Hedfalk, 2006, Aquaporin gating, Curr. Opin. Struct. Biol., 16, 447, 10.1016/j.sbi.2006.06.009

Hoffert, 2009, Aquaporin-2 in the “-omics” era, J. Biol. Chem., 284, 14683, 10.1074/jbc.R900006200

Hoffert, 2007, Dynamics of aquaporin-2 serine-261 phosphorylation in response to short-term vasopressin treatment in collecting duct, Am. J. Physiol. Renal Physiol., 292, F691, 10.1152/ajprenal.00284.2006

Hoffert, 2006, Quantitative phosphoproteomics of vasopressin-sensitive renal cells: regulation of aquaporin-2 phosphorylation at two sites, Proc. Natl. Acad. Sci. USA, 103, 7159, 10.1073/pnas.0600895103

Ishibashi, 2009, Aquaporin water channels in mammals, Clin. Exp. Nephrol., 13, 107, 10.1007/s10157-008-0118-6

Ishibashi, 1994, Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells, Proc. Natl. Acad. Sci. USA, 91, 6269, 10.1073/pnas.91.14.6269

Ishikawa, 2001, Close association of urinary excretion of aquaporin-2 with appropriate and inappropriate arginine vasopressin-dependent antidiuresis in hyponatremia in elderly subjects, J. Clin. Endocrinol. Metab., 86, 1665

Ivarsen, 2003, Increased urinary excretion of aquaporin 2 in patients with liver cirrhosis, Gut, 52, 1194, 10.1136/gut.52.8.1194

Jung, 1994, Molecular structure of the water channel through aquaporin CHIP. The hourglass model, J. Biol. Chem., 269, 14648, 10.1016/S0021-9258(17)36674-7

Kachadorian, 1975, Vasopressin: induced structural change in toad bladder luminal membrane, Science, 190, 67, 10.1126/science.809840

Kamsteeg, 2003, Reversed polarized delivery of an aquaporin-2 mutant causes dominant nephrogenic diabetes insipidus, J. Cell Biol., 163, 1099, 10.1083/jcb.200309017

Kamsteeg, 2000, The subcellular localization of an aquaporin-2 tetramer depends on the stoichiometry of phosphorylated and nonphosphorylated monomers, J. Cell Biol., 151, 919, 10.1083/jcb.151.4.919

Kamsteeg, 2006, Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel, Proc. Natl. Acad. Sci. USA, 103, 18344, 10.1073/pnas.0604073103

Kamsteeg, 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, 10.1007/s00424-007-0364-6

Kasono, 2005, Hypertonicity regulates the aquaporin-2 promoter independently of arginine vasopressin, Nephrol. Dial. Transplant., 20, 509, 10.1093/ndt/gfh677

Katsura, 1997, Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells, Am. J. Physiol., 272, F817

Kishore, 1996, Rat renal arcade segment expresses vasopressin-regulated water channel and vasopressin V2 receptor, J. Clin. Invest., 97, 2763, 10.1172/JCI118731

Kuwahara, 1995, CAMP-dependent phosphorylation stimulates water permeability of aquaporin-collecting duct water channel protein expressed in Xenopus oocytes, J. Biol. Chem., 270, 10384, 10.1074/jbc.270.18.10384

Kuwahara, 2001, Three families with autosomal dominant nephrogenic diabetes insipidus caused by aquaporin-2 mutations in the C-terminus, Am. J. Hum. Genet., 69, 738, 10.1086/323643

Lande, 1996, Phosphorylation of aquaporin-2 does not alter the membrane water permeability of rat papillary water channel-containing vesicles, J. Biol. Chem., 271, 5552, 10.1074/jbc.271.10.5552

Li, 2003, Downregulation of renal aquaporins in response to unilateral ureteral obstruction, Am. J. Physiol. Renal Physiol., 284, F1066, 10.1152/ajprenal.00090.2002

Loonen, 2008, Aquaporin 2 mutations in nephrogenic diabetes insipidus, Semin. Nephrol., 28, 252, 10.1016/j.semnephrol.2008.03.006

López-Rodríguez, 2004, Loss of NFAT5 results in renal atrophy and lack of tonicity-responsive gene expression, Proc. Natl. Acad. Sci. USA, 101, 2392, 10.1073/pnas.0308703100

Lu, 2004, Inhibition of endocytosis causes phosphorylation (S256)-independent plasma membrane accumulation of AQP2, Am. J. Physiol. Renal Physiol., 286, F233, 10.1152/ajprenal.00179.2003

Lu, 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. Renal Physiol., 295, F290, 10.1152/ajprenal.00072.2008

Ma, 2000, Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels, Proc. Natl. Acad. Sci. USA, 97, 4386, 10.1073/pnas.080499597

Ma, 1997, Closely spaced tandem arrangement of AQP2, AQP5, and AQP6 genes in a 27-kilobase segment at chromosome locus 12q13, Genomics, 43, 387, 10.1006/geno.1997.4836

Maekawa, 2010, Expression and translocation of aquaporin-2 in the endolymphatic sac in patients with Meniere’s disease, J. Neuroendocrinol., 22, 1157, 10.1111/j.1365-2826.2010.02060.x

Marr, 2002, Heteroligomerization of an aquaporin-2 mutant with wild-type aquaporin-2 and their misrouting to late endosomes/lysosomes explains dominant nephrogenic diabetes insipidus, Hum. Mol. Genet., 11, 779, 10.1093/hmg/11.7.779

Matsumura, 1999, Overt nephrogenic diabetes insipidus in mice lacking the CLC-K1 chloride channel, Nat. Genet., 21, 95, 10.1038/5036

Matsumura, 1997, Transcriptional regulation of aquaporin-2 water channel gene by cAMP, J. Am. Soc. Nephrol., 8, 861, 10.1681/ASN.V86861

Mhatre, 2002, Aquaporin-2 expression in the mammalian cochlea and investigation of its role in Meniere’s disease, Hear. Res., 170, 59, 10.1016/S0378-5955(02)00452-5

Moeller, 2009, Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells, Kidney Int., 75, 295, 10.1038/ki.2008.505

Moeller, 2009, Role of multiple phosphorylation sites in the COOH-terminal tail of aquaporin-2 for water transport: evidence against channel gating, Am. J. Physiol. Renal Physiol., 296, F649, 10.1152/ajprenal.90682.2008

Mulders, 1998, An aquaporin-2 water channel mutant which causes autosomal dominant nephrogenic diabetes insipidus is retained in the Golgi complex, J. Clin. Invest, 102, 57, 10.1172/JCI2605

Murata, 2000, Structural determinants of water permeation through aquaporin-1, Nature, 407, 599, 10.1038/35036519

Nielsen, 1995, Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane, Proc. Natl. Acad. Sci. USA, 92, 1013, 10.1073/pnas.92.4.1013

Nielsen, 1993, Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney, Proc. Natl. Acad. Sci. USA, 90, 11663, 10.1073/pnas.90.24.11663

Nielsen, 2008, Proteomic analysis of lithium-induced nephrogenic diabetes insipidus: mechanisms for aquaporin 2 down-regulation and cellular proliferation, Proc. Natl. Acad. Sci. USA, 105, 3634, 10.1073/pnas.0800001105

Nielsen, 1997, Congestive heart failure in rats is associated with increased expression and targeting of aquaporin-2 water channel in collecting duct, Proc. Natl. Acad. Sci. USA, 94, 5450, 10.1073/pnas.94.10.5450

Noda, 2004, Aquaporin-2 trafficking is regulated by PDZ-domain containing protein SPA-1, FEBS Lett., 568, 139, 10.1016/j.febslet.2004.05.021

Noda, 2008, Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking, J. Cell Biol., 182, 587, 10.1083/jcb.200709177

Noda, 2004, Water channel aquaporin-2 directly binds to actin, Biochem. Biophys. Res. Commun., 322, 740, 10.1016/j.bbrc.2004.07.195

Noda, 2005, Identification of a multiprotein “motor” complex binding to water channel aquaporin-2, Biochem. Biophys. Res. Commun., 330, 1041, 10.1016/j.bbrc.2005.03.079

Noda, 2010, Aquaporins in kidney pathophysiology, Nat. Rev. Nephrol., 6, 168, 10.1038/nrneph.2009.231

Orloff, 1967, The role of adenosine 3′,5′-phosphate in the action of antidiuretic hormone, Am. J. Med., 42, 757, 10.1016/0002-9343(67)90093-9

Pisitkun, 2004, Identification and proteomic profiling of exosomes in human urine, Proc. Natl. Acad. Sci. USA, 101, 13368, 10.1073/pnas.0403453101

Preston, 1991, Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family, Proc. Natl. Acad. Sci. USA, 88, 11110, 10.1073/pnas.88.24.11110

Preston, 1992, Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein, Science, 256, 385, 10.1126/science.256.5055.385

Rai, 1997, Urinary excretion of aquaporin-2 water channel protein in human and rat, J. Am. Soc. Nephrol., 8, 1357, 10.1681/ASN.V891357

Rojek, 2006, Severe urinary concentrating defect in renal collecting duct-selective AQP2 conditional-knockout mice, Proc. Natl. Acad. Sci. USA, 103, 6037, 10.1073/pnas.0511324103

Russo, 2006, Methyl-beta-cyclodextrin induces vasopressin-independent apical accumulation of aquaporin-2 in the isolated, perfused rat kidney, Am. J. Physiol. Renal Physiol., 291, F246, 10.1152/ajprenal.00437.2005

Sabolić, 1995, The AQP2 water channel: effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats, J. Membr. Biol., 143, 165, 10.1007/BF00233445

Saito, 1995, Human AQP2 and MIP genes, two members of the MIP family, map within chromosome band 12q13 on the basis of two-color FISH, Cytogenet. Cell Genet., 68, 45, 10.1159/000133885

Sasaki, 2004, Nephrogenic diabetes insipidus: update of genetic and clinical aspects, Nephrol. Dial. Transplant., 19, 1351, 10.1093/ndt/gfh172

Sasaki, 1998, Aquaporin-2 and -3: representatives of two subgroups of the aquaporin family colocalized in the kidney collecting duct, Annu. Rev. Physiol., 60, 199, 10.1146/annurev.physiol.60.1.199

Sasaki, 2007, Aquaporin-2 protein dynamics within the cell, Curr. Opin. Nephrol. Hypertens., 16, 348, 10.1097/MNH.0b013e32818b27bf

Sasaki, 2011, Daily variance of urinary excretion of AQP2 determined by sandwich ELISA method, Clin. Exp. Nephrol.

Savelkoul, 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, 10.1002/humu.21082

Schenk, 2005, The 4.5 A structure of human AQP2, J. Mol. Biol., 350, 278, 10.1016/j.jmb.2005.04.030

Schrier, 2008, Vasopressin and aquaporin 2 in clinical disorders of water homeostasis, Semin. Nephrol., 28, 289, 10.1016/j.semnephrol.2008.03.009

Sohara, 2006, Pathogenesis and treatment of autosomal-dominant nephrogenic diabetes insipidus caused by an aquaporin 2 mutation, Proc. Natl. Acad. Sci. USA, 103, 14217, 10.1073/pnas.0602331103

Stevens, 2000, Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens, Am. J. Physiol. Cell Physiol., 278, C791, 10.1152/ajpcell.2000.278.4.C791

Sun, 2002, Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin, Am. J. Physiol. Renal Physiol., 282, F998, 10.1152/ajprenal.00257.2001

Taguchi, 2007, Expressions of aquaporin-2, vasopressin type 2 receptor, transient receptor potential channel vanilloid (TRPV)1, and TRPV4 in the human endolymphatic sac, Laryngoscope, 117, 695, 10.1097/mlg.0b013e318031c802

Tajika, 2005, Differential regulation of AQP2 trafficking in endosomes by microtubules and actin filaments, Histochem. Cell Biol., 124, 1, 10.1007/s00418-005-0010-3

Tajika, 2004, Aquaporin-2 is retrieved to the apical storage compartment via early endosomes and phosphatidylinositol 3-kinase-dependent pathway, Endocrinology, 145, 4375, 10.1210/en.2004-0073

Terris, 1996, Long-term regulation of four renal aquaporins in rats, Am. J. Physiol., 271, F414

Törnroth-Horsefield, 2006, Structural mechanism of plant aquaporin gating, Nature, 439, 688, 10.1038/nature04316

Uchida, 1993, Molecular cloning of a chloride channel that is regulated by dehydration and expressed predominantly in kidney medulla, J. Biol. Chem., 269, 19192, 10.1016/S0021-9258(17)32293-7

Uchida, 1994, Isolation of human aquaporin-CD gene, J. Biol. Chem., 269, 23451, 10.1016/S0021-9258(17)31537-5

Umenishi, 2002, Comparison of three methods to quantify urinary aquaporin-2 protein, Kidney Int., 62, 2288, 10.1046/j.1523-1755.2002.00686.x

Valenti, 2005, Minireview: aquaporin 2 trafficking, Endocrinology, 146, 5063, 10.1210/en.2005-0868

Wang, 2002, AQP3, p-AQP2, and AQP2 expression is reduced in polyuric rats with hypercalcemia: prevention by cAMP-PDE inhibitors, Am. J. Physiol. Renal Physiol., 283, F1313, 10.1152/ajprenal.00040.2002

Werten, 2001, Large-scale purification of functional recombinant human aquaporin-2, FEBS Lett., 504, 200, 10.1016/S0014-5793(01)02703-X

Xie, 2010, Quantitative analysis of aquaporin-2 phosphorylation, Am. J. Physiol. Renal Physiol., 298, F1018, 10.1152/ajprenal.00580.2009

Xu, 1997, Upregulation of aquaporin-2 water channel expression in chronic heart failure rat, J. Clin. Invest., 99, 1500, 10.1172/JCI119312

Yamamoto, 1995, Vasopressin increases AQP-CD water channel in apical membrane of collecting duct cells in Brattleboro rats, Am. J. Physiol., 268, C1546, 10.1152/ajpcell.1995.268.6.C1546

Yamamoto, 1995, Localization and expression of a collecting duct water channel, aquaporin, in hydrated and dehydrated rats, Exp. Nephrol., 3, 193

Yu, 2009, Systems-level analysis of cell-specific AQP2 gene expression in renal collecting duct, Proc. Natl. Acad. Sci. USA, 106, 2441, 10.1073/pnas.0813002106

Zhang, 1991, Evidence from oocyte expression that the erythrocyte water channel is distinct from band 3 and the glucose transporter, J. Clin. Invest., 88, 1553, 10.1172/JCI115466