Abstract
Membrane water channel aquaporin-2 (AQP2) and glucose transporter 4 (GLUT4) exhibit a common feature in that they are stored in intracellular storage compartments and undergo translocation to the plasma membrane upon hormonal stimulation. We compared the intracellular localization and trafficking of AQP2 and GLUT4 in polarized Madin-Darby canine kidney cells stably transfected with human AQP2 (MDCK-hAQP2) by immunofluorescence microscopy. When expressed in MDCK-hAQP2 cells, GLUT4 and GLUT4—EGFP were predominantly localized in the perinuclear region close to and within the Golgi apparatus, similar to endogenous GLUT4 in adipocytes and myocytes. In addition, GLUT4 was occasionally seen in EEA1-positive early endosomes. AQP2, on the other hand, was sequestered in subapical Rab11-positive vesicles. In the basal state, the intracellular storage site of GLUT4 was distinct from that of AQP2. Forskolin induced translocation of AQP2 from the subapical storage vesicles to the apical plasma membrane, which did not affect GLUT4 localization. When forskolin was washed out, AQP2 was first retrieved to early endosomes from the apical plasma membrane, where it was partly colocalized with GLUT4. AQP2 was then transferred to Rab11-positive storage vesicles. These results show that AQP2 and GLUT4 share a common compartment after retrieval from the plasma membrane, but their storage compartments are distinct from each other in polarized MDCK-hAQP2 cells.
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References
Asai T, Kuwahara M, Kurihara H, Sakai T, Terada Y, Marumo F, Sasaki S (2003) Pathogenesis of nephrogenic diabetes insipidus by aquaporin-2 C-terminus mutations. Kidney Int 64:2–10
Asano T, Takata K, Katagiri H, Ishihara H, Inukai K, Anai M, Hirano H, Yazaki Y, Oka Y (1993) The role of N-glycosylation in the targeting and stability of GLUT1 glucose transporter. FEBS Lett 324:258–261
Blok J, Gibbs EM, Lienhard GE, Slot JW, Geuze HJ (1988) Insulin-induced translocation of glucose transporters from post-Golgi compartments to the plasma membrane of 3T3-L1 adipocytes. J Cell Biol 106:69–76
Duman JG, Forte JG (2003) What is the role of SNARE proteins in membrane fusion? Am J Physiol Cell Physiol 285:C237–C249
Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S (1993) Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361:549–552
Fushimi K, Sasaki S, Marumo F (1997) Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272:14800–14804
Gouraud S, Laera A, Calamita G, Carmosino M, Procino G, Rossetto O, Mannucci R, Rosenthal W, Svelto M, Valenti G (2002) Functional involvement of VAMP/synaptobrevin-2 in cAMP-stimulated aquaporin 2 translocation in renal collecting duct cells. J Cell Sci 115:3667–3674
Itoh T, Rai T, Kuwahara M, Ko SB, Uchida S, Sasaki S, Ishibashi K (2005) Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem Biophys Res Commun 330:832–838
Jhun BH, Rampal AL, Liu H, Lachaal M, Jung CY (1992) Effects of insulin on steady state kinetics of GLUT4 subcellular distribution in rat adipocytes. Evidence of constitutive GLUT4 recycling. J Biol Chem 267:17710–17715
Kamsteeg EJ, Bichet DG, Konings IB, Nivet H, Lonergan M, Arthus MF, van Os CH, Deen PM (2003) Reversed polarized delivery of an aquaporin-2 mutant causes dominant nephrogenic diabetes insipidus. J Cell Biol 163:1099–1109
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
Lafont F, Verkade P, Galli T, Wimmer C, Louvard D, Simons K (1999) Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc Natl Acad Sci USA 96:3734–3738
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 Renal Physiol 286:F233–F243
Martin S, Tellam J, Livingstone C, Slot JW, Gould GW, James DE (1996) The glucose transporter (GLUT-4) and vesicle-associated membrane protein-2 (VAMP-2) are segregated from recycling endosomes in insulin-sensitive cells. J Cell Biol 134:625–635
Molloy SS, Thomas L, VanSlyke JK, Stenberg PE, Thomas G (1994) Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J 13:18–33
Morishita Y, Matsuzaki T, Hara chikuma M, Andoo A, Shimono M, Matsuki A, Kobayashi K, Ikeda M, Yamamoto T, Verkman A, Kusano E, Ookawara S, Takata K, Sasaki S, Ishibashi K (2005) Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol Cell Biol 25:7770–7779
Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW (1993) Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90:11663–11667
Nielsen S, Marples D, Birn H, Mohtashami M, Dalby NO, Trimble M, Knepper M (1995a) 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, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995b) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013–1017
Nielsen S, Frokiaer 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 (2006) Regulation of aquaporin-2 trafficking and its binding protein complex. Biochim Biophys Acta 1758:1117–1125
Pascoe WS, Inukai K, Oka Y, Slot JW, James DE (1996) Differential targeting of facilitative glucose transporters in polarized epithelial cells. Am J Physiol 271:C547–C554
Procino G, Caces DB, Valenti G, Pessin JE (2006) Adipocytes support cAMP-dependent translocation of aquaporin-2 from intracellular sites distinct from the insulin-responsive GLUT4 storage compartment. Am J Physiol Renal Physiol 290:F985–F994
Ramm G, Slot JW, James DE, Stoorvogel W (2000) Insulin recruits GLUT4 from specialized VAMP2-carrying vesicles as well as from the dynamic endosomal/trans-Golgi network in rat adipocytes. Mol Biol Cell 11:4079–4091
Robben JH, Knoers NV, Deen PM (2006) Cell biological aspects of the vasopressin type-2 receptor and aquaporin 2 water channel in nephrogenic diabetes insipidus. Am J Physiol Renal Physiol 291:F257–F270
Satoh S, Nishimura H, Clark AE, Kozka IJ, Vannucci SJ, Simpson IA, Quon MJ, Cushman SW, Holman GD (1993) Use of bismannose photolabel to elucidate insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. Evidence that exocytosis is a critical site of hormone action. J Biol Chem 268:17820–17829
Shinoda Y, Suzuki T, Sugawara-Yokoo M, Nagamatsu S, Kuwano H, Takata K (2001) Expression of sugar transporters by in vivo electroporation and particle gun methods in the rat liver: localization to specific membrane domains. Acta Histochem Cytochem 34: 15–24
Shinoda Y, Matsuzaki T, Yokoo-Sugawara M, Suzuki T, Aoki T, Hagiwara H, Kuwano H, Takata K (2003) Introduction and expression of glucose transporters in pancreatic acinar cells by in vivo electroporation. Acta Histochem Cytochem 36:77–82
Slot JW, Geuze HJ, Gigengack S, Lienhard GE, James DE (1991) Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113:123–135
Steegmaier M, Lee KC, Prekeris R, Scheller RH (2000) SNARE protein trafficking in polarized MDCK cells. Traffic 1:553–560
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
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
Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83
Takata K, Matsuzaki T, Tajika Y, Ablimit A, Suzuki T, Aoki T, Hagiwara H (2005) Aquaporin water channels in the kidney. Acta Histochem Cytochem 38:199–207
Voorhees P, Deignan E, van Donselaar E, Humphrey J, Marks MS, Peters PJ, Bonifacino JS (1995) An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J 14:4961–4975
Watson RT, Kanzaki M, Pessin JE (2004) Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr Rev 25:177–204
Acknowledgments
We wish to thank Sachiko Fukushima for secretarial assistance. This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Hasegawa, T., Matsuzaki, T., Tajika, Y. et al. Differential localization of aquaporin-2 and glucose transporter 4 in polarized MDCK cells. Histochem Cell Biol 127, 233–241 (2007). https://doi.org/10.1007/s00418-006-0264-4
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DOI: https://doi.org/10.1007/s00418-006-0264-4