The Subcellular Localization of an Aquaporin-2 Tetramer Depends on the Stoichiometry of Phosphorylated and Nonphosphorylated Monomers
Tóm tắt
In renal principal cells, vasopressin regulates the shuttling of the aquaporin (AQP)2 water channel between intracellular vesicles and the apical plasma membrane. Vasopressin-induced phosphorylation of AQP2 at serine 256 (S256) by protein kinase A (PKA) is essential for its localization in the membrane. However, phosphorylated AQP2 (p-AQP2) has also been detected in intracellular vesicles of noninduced principal cells. As AQP2 is expressed as homotetramers, we hypothesized that the number of p-AQP2 monomers in a tetramer might be critical for the its steady state distribution. Expressed in oocytes, AQP2-S256D and AQP2-S256A mimicked p-AQP2 and non–p-AQP2, respectively, as routing and function of AQP2-S256D and wild-type AQP2 (wt-AQP2) were identical, whereas AQP2-S256A was retained intracellularly. In coinjection experiments, AQP2-S256A and AQP2-S256D formed heterotetramers. Coinjection of different ratios of AQP2-S256A and AQP2-S256D cRNAs revealed that minimally three AQP2-S256D monomers in an AQP2 tetramer were essential for its plasma membrane localization. Therefore, our results suggest that in principal cells, minimally three monomers per AQP2 tetramer have to be phosphorylated for its steady state localization in the apical membrane. As other multisubunit channels are also regulated by phosphorylation, it is anticipated that the stoichiometry of their phosphorylated and nonphosphorylated subunits may fine-tune the activity or subcellular localization of these complexes.
Từ khóa
Tài liệu tham khảo
Bao, 2000, Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome, J. Biol. Chem., 275, 26178, 10.1074/jbc.M002367200
Brown, 1989, Membrane recycling and epithelial cell function, Am. J. Physiol., 256, F1
Brown, 1996, Protein trafficking and polarity in kidney epitheliumfrom cell biology to physiology, Physiol. Rev., 76, 245, 10.1152/physrev.1996.76.1.245
Brown, 1988, Vasopressin stimulates endocytosis in kidney collecting duct principal cells, Eur. J. Cell Biol., 46, 336
Cheng, 1998, Assembly of the epithelial Na+ channel evaluated using sucrose gradient sedimentation analysis, J. Biol. Chem., 273, 22693, 10.1074/jbc.273.35.22693
Christensen, 2000, Localization and regulation of PKA-phosphorylated AQP2 in response to V(2)-receptor agonist/antagonist treatment, Am. J. Physiol. Renal Physiol., 278, F29, 10.1152/ajprenal.2000.278.1.F29
Deen, 1998, Physiology and pathophysiology of the aquaporin-2 water channel, Curr. Opin. Nephrol. Hypertens., 7, 37, 10.1097/00041552-199801000-00007
Deen, 1994, Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine, Science., 264, 92, 10.1126/science.8140421
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, 1997, Aquaporin-2 transfection of Madin-Darby canine kidney cells reconstitutes vasopressin-regulated transcellular osmotic water transport, J. Am. Soc. Nephrol., 8, 1493, 10.1681/ASN.V8101493
Deen, 1997, Apical and basolateral expression of aquaporin-1 in transfected MDCK and LLC-PK cells and functional evaluation of their transcellular osmotic water permeabilities, Pflugers Arch., 433, 780, 10.1007/s004240050345
Ecelbarger, 1995, Aquaporin-3 water channel localization and regulation in rat kidney, Am. J. Physiol. Renal Physiol., 38, F663, 10.1152/ajprenal.1995.269.5.F663
Eskandari, 1998, Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy, Proc. Natl. Acad. Sci. USA., 95, 11235, 10.1073/pnas.95.19.11235
Fushimi, 1993, Cloning and expression of apical membrane water channel of rat kidney collecting tubule, Nature., 361, 549, 10.1038/361549a0
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
Ghosh, 1998, An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells, J. Cell Biol., 142, 923, 10.1083/jcb.142.4.923
Glowatzki, 1995, Subunit-dependent assembly of inward-rectifier K+ channels, Proc. R. Soc. Lond. B. Biol. Sci., 261, 251, 10.1098/rspb.1995.0145
Harris, 1991, Current understanding of the cellular biology and molecular structure of the antidiuretic hormone-stimulated water transport pathway, J. Clin. Invest., 88, 1, 10.1172/JCI115263
Hasler, 1998, Purified lens major intrinsic protein (MIP) forms highly ordered tetragonal two-dimensional arrays by reconstitution, J. Mol. Biol., 279, 855, 10.1006/jmbi.1998.1796
Hoffman, 1994, Role of phosphorylation in desensitization of acetylcholine receptors expressed in Xenopus oocytes, J. Neurosci., 14, 4185, 10.1523/JNEUROSCI.14-07-04185.1994
Huang, 1994, Constitutive activation of Mek1 by mutation of serine phosphorylation sites, Proc. Natl. Acad. Sci. USA., 91, 8960, 10.1073/pnas.91.19.8960
Inoue, 1998, SNAP-23 in rat kidneycolocalization with aquaporin-2 in collecting duct vesicles, Am. J. Physiol., 275, F752
Jessus, 1998, Ras family proteinsnew players involved in the diplotene arrest of Xenopus oocytes, Biol. Cell., 90, 573, 10.1111/j.1768-322X.1998.tb01066.x
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
Kamsteeg, 1999, An impaired routing of wild-type aquaporin-2 after tetramerization with an aquaporin-2 mutant explains dominant nephrogenic diabetes insipidus, EMBO (Eur. Mol. Biol. Organ.) J., 18, 2394, 10.1093/emboj/18.9.2394
Katsura, 1996, Direct demonstration of aquaporin-2 water channel recycling in stably transfected LLC-PK1 epithelial cells, Am. J. Physiol., 39, F548
Katsura, 1997, Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells, Am. J. Physiol., 41, F816
Klussmann, 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, 10.1074/jbc.274.8.4934
Kowlessur, 1995, Further studies of the role of Ser-16 in the regulation of the activity of phenylalanine hydroxylase, Proc. Natl. Acad. Sci. USA., 92, 4743, 10.1073/pnas.92.11.4743
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
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
Liebenhoff, 1995, Identification of Rab3-, Rab5a- and synaptobrevin II-like proteins in a preparation of rat kidney vesicles containing the vasopressin-regulated water channel, FEBS Lett., 365, 209, 10.1016/0014-5793(95)00476-P
Lukacs, 1997, Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation, Biochem. J., 328, 353, 10.1042/bj3280353
Mandon, 1996, Syntaxin-4 is localized to the apical plasma membrane of rat renal collecting duct cellspossible role in aquaporin-2 trafficking, J. Clin. Invest., 98, 906, 10.1172/JCI118873
Marples, 1995, Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct, Am. J. Physiol., 38, C655, 10.1152/ajpcell.1995.269.3.C655
Marples, 1998, Dynein and dynactin colocalize with aqp2 water channels in intracellular vesicles from kidney collecting duct, Am. J. Physiol., 43, F384
Martin, 1998, Role of aquaporin-2 water channels in urinary concentration and dilution defects, Kidney Int. Suppl., 65, S57
Martinez, 1997, Dual phosphorylation of the T-loop in cdk7its role in controlling cyclin H binding and CAK activity, EMBO (Eur. Mol. Biol. Organ.) J., 16, 343, 10.1093/emboj/16.2.343
McDonald, 1998, Adjacent phosphorylation sites on GABAA receptor beta subunits determine regulation by cAMP-dependent protein kinase, Nat. Neurosci., 1, 23, 10.1038/223
McLean, 1974, Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy, J. Histochem. Cytochem., 22, 1077, 10.1177/22.12.1077
McNicholas, 1994, Regulation of ROMK1 K+ channel activity involves phosphorylation processes, Proc. Natl. Acad. Sci. USA., 91, 8077, 10.1073/pnas.91.17.8077
Molloy, 1999, Bi-cycling the furin pathwayfrom TGN localization to pathogen activation and embryogenesis, Trends Cell Biol., 9, 28, 10.1016/S0962-8924(98)01382-8
Morrill, 1984, Endocytosis in the amphibian oocyte. Effect of insulin and progesterone on membrane and fluid internalization during the meiotic divisions, Biochim. Biophys. Acta., 803, 71, 10.1016/0167-4889(84)90056-9
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
Neely, 1999, Heterotetrameric composition of aquaporin-4 water channels, Biochemistry., 38, 11156, 10.1021/bi990941s
Nielsen, 1993, CHIP28 water channels are localized in constitutively water-permeable segments of the nephron, J. Cell Biol., 120, 371, 10.1083/jcb.120.2.371
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, 1995, Expression of VAMP2-like protein in kidney collecting duct intracellular vesicles. Colocalization with aquaporin-2 water channels, J. Clin. Invest., 96, 1834, 10.1172/JCI118229
Nielsen, 1998, Renal aquaporinskey roles in water balance and water balance disorders, Curr. Opin. Nephrol. Hypertens., 7, 509, 10.1097/00041552-199809000-00005
Nielsen, 1999, Physiology and pathophysiology of renal aquaporins, J. Am. Soc. Nephrol., 10, 647, 10.1681/ASN.V103647
Nishimoto, 1999, Arginine vasopressin stimulates phosphorylation of aquaporin-2 in rat renal tissue, Am. J. Physiol., 276, F254
Oh, 1998, Isolation and subfractionation of plasma membranes to purify caveolae separately from glycosyl-phosphatidylinositol-anchored protein microdomains, Cell Biology, A Laboratory Handbook, 34
Quick, 1997, Second messengers, trafficking-related proteins, and amino acid residues that contribute to the functional regulation of the rat brain GABA transporter GAT1, J. Neurosci., 17, 2967, 10.1523/JNEUROSCI.17-09-02967.1997
Rich, 1993, Regulation of the cystic fibrosis transmembrane conductance regulator Cl− channel by negative charge in the R domain, J. Biol. Chem., 268, 20259, 10.1016/S0021-9258(20)80723-6
Rohn, 2000, Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system, J. Cell Sci., 113, 2093, 10.1242/jcs.113.12.2093
Sabolic, 1995, The AQP2 water channeleffect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats, J. Membr. Biol., 143, 165, 10.1007/BF00233445
Schnermann, 1998, Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice, Proc. Natl. Acad. Sci. USA., 95, 9660, 10.1073/pnas.95.16.9660
Shimkets, 1998, In vivo phosphorylation of the epithelial sodium channel, Proc. Natl. Acad. Sci. USA., 95, 3301, 10.1073/pnas.95.6.3301
Sonnichsen, 2000, Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11, J. Cell Biol., 149, 901, 10.1083/jcb.149.4.901
Strange, 1988, Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule, J. Membr. Biol., 103, 17, 10.1007/BF01871929
Staub, 1997, Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination, EMBO (Eur. Mol. Biol. Organ.) J., 16, 6325, 10.1093/emboj/16.21.6325
Terris, 1995, Distribution of aquaporin-4 water channel expression within rat kidney, Am. J. Physiol. Renal Physiol., 38, F775, 10.1152/ajprenal.1995.269.6.F775
Valenti, 1998, A heterotrimeric G protein of the Gi family is required for cAMP-triggered trafficking of aquaporin 2 in kidney epithelial cells, J. Biol. Chem., 273, 22627, 10.1074/jbc.273.35.22627
Valenti, 2000, The phosphatase inhibitor okadaic acid induces AQP2 translocation independently from AQP2 phosphorylation in renal collecting duct cells, J. Cell Sci., 113, 1985, 10.1242/jcs.113.11.1985
Wade, 1981, ADH actionevidence for a membrane shuttle mechanism, Ann. NY Acad. Sci., 372, 106, 10.1111/j.1749-6632.1981.tb15464.x
Xu, 1996, Phosphorylation of the ATP-sensitive, inwardly rectifying K+ channel, ROMK, by cyclic AMP-dependent protein kinase, J. Biol. Chem., 271, 9313, 10.1074/jbc.271.16.9313
Yang, 1997, Water and glycerol permeabilities of aquaporins 1–5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes, J. Biol. Chem., 272, 16140, 10.1074/jbc.272.26.16140
Zehavi-Feferman, 1995, Control of p62 binding to TGN38/41 by phosphorylation, FEBS Lett., 368, 122, 10.1016/0014-5793(95)00613-E