Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

Crossref logo

Fol. Biol. 2006, 52, 173-180

https://doi.org/10.14712/fb2006052050173

Regulation of Selectivity and Translocation of Aquaporins: an Update

Miloš M. Petrović1, K. Valeš2, G. Stojan3, G. Basta-Jovanović3, D. M. Mitrović1

1Institute of Physiology, School of Medicine, Belgrade University, Serbia
2Institute of Physiology, Academy of Sciences of the Czech Republic, Prague, Czech Republic
3Institute of Pathology, School of Medicine, Belgrade University, Serbia

Received September 2006
Accepted October 2006

References

1. Agre, P., King, L. S., Yasui, M., Guggino, W. B., Ottersen, O. P., Fujiyoshi, Y., Engel, A., Nielsen, S. (2002) Aquaporin water channels – from atomic structure to clinical medicine. J. Physiol. (Lond.) 542, 3-16. <https://doi.org/10.1113/jphysiol.2002.020818>
2. Bacallao, R., Antony, C., Dotti, C., Karsenti, E., Stelzer, E., Simons, K. (1989) The subcellular organization of MadinDarby canine kidney cells during the formation of a polarized epithelium J. Cell Biol. 109, 2817-2832. <https://doi.org/10.1083/jcb.109.6.2817>
3. Barth, H., Hofmann, F., Olenik, C., Just, I., Aktories, K. (1998) The N-terminal part of the enzyme component (C2I) of the binary Clostridium botulinum C2 toxin interacts with the binding component C2II and functions as a carrier system for a Rho ADP-ribosylating C3-like fusion toxin. Infect. Immun. 66, 1364-1369. <https://doi.org/10.1128/IAI.66.4.1364-1369.1998>
4. Beitz, E., Wu, B., Holm, L. M., Schultz, J. E., Zeuthen, T. (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc. Natl. Acad. Sci. USA 103, 269-274. <https://doi.org/10.1073/pnas.0507225103>
5. Birnbaumer, M., Seibold, A., Gilbert, S., Ishido, M., Barberis, C., Antaramian, A., Brabet, P., Rosenthal, W. (1992) Molecular cloning of the receptor for human antidiuretic hormone. Nature 357, 333-335. <https://doi.org/10.1038/357333a0>
6. Buendia, B., Bre, M., Griffiths, G., Karsenti, E. (1990) Cytoskeletal control of centrioles movement during the establishment of polarity in Madin-Darby canine kidney cells. J. Cell Biol. 110, 1123-1135. <https://doi.org/10.1083/jcb.110.4.1123>
7. Chakrabarti, N., Tajkhorshid, E., Roux, B., Pomes, R. (2004) Molecular basis of proton blockage in aquaporins. Structure 12, 65-74. <https://doi.org/10.1016/j.str.2003.11.017>
8. Champigneulle, A., Siga, E., Vassent, G., Imbert-Teboul, M. (1993)V2-like vasopressin receptor mobilizes intracellular Ca2+ in rat medullary collecting tubules. Am. J. Physiol. Renal Physiol. 265, F35-45. <https://doi.org/10.1152/ajprenal.1993.265.1.F35>
9. Chou, C.-L., Rapko, S. I., Knepper, M. A. (1998) Phosphoinositide signaling in rat inner medullary collecting duct. Am. J. Physiol. Renal Physiol. 274, F564-572. <https://doi.org/10.1152/ajprenal.1998.274.3.F564>
10. Chou, C.-L., Yip, K.-P., Michea, L., Kador, K., Ferraris, J. D., Wade, J. B., Knepper, M. A. (2000) Regulation of aquaporin-2 trafficking by vasopressin in the renal collecting duct. Roles of ryanodine-sensitive Ca2+ stores and calmodulin. J. Biol. Chem. 275, 36839-36846. <https://doi.org/10.1074/jbc.M005552200>
11. Chou, C.-L., Christensen, B. M., Frische, S., Vorum, H., Desai, R. A., Hoffert, J. D., de Lanerolle, P., Nielsen, S., Knepper, M. A. (2004) Non-muscle myosin II and myosin light chain kinase are downstream targets for vasopressin signaling in the renal collecting duct. J. Biol. Chem. 279, 49026-49035. <https://doi.org/10.1074/jbc.M408565200>
12. Christensen, B. M., Zelenina, M., Aperia, A., Nielsen, S. (2000) Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am. J. Physiol. Renal Physiol. 278, F29-42. <https://doi.org/10.1152/ajprenal.2000.278.1.F29>
13. de Groot, B. L., Engel, A., Grubmuller, H. (2001) A refined structure of human aquaporin-1. FEBS Lett. 504, 206-211. <https://doi.org/10.1016/S0014-5793(01)02743-0>
14. de Groot, B. L., Frigato, T., Helms, V., Grubmuller, H. (2003) The mechanism of proton exclusion in the aquaporin-1 water channel. J. Mol. Biol. 333, 279-293. <https://doi.org/10.1016/j.jmb.2003.08.003>
15. Denker, B., Smith, B., Kuhajda, F., Agre, P. (1988) Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263, 15634-15642. <https://doi.org/10.1016/S0021-9258(19)37635-5>
16. Dong, J.-M., Leung, T., Manser, E., Lim, L. (1998) cAMPinduced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKα. J. Biol. Chem. 273, 22554-22562. <https://doi.org/10.1074/jbc.273.35.22554>
17. Dransart, E., Olofsson, B., Cherfils, J. (2005) RhoGDIs revisited: novel roles in Rho regulation. Traffic 6, 957-966. <https://doi.org/10.1111/j.1600-0854.2005.00335.x>
18. Fujiyoshi, Y., Mitsuoka, K., de Groot, B. L., Philippsen, A., Grubmuller, H., Agre, P., Engel, A. (2002) Structure and function of water channels. Curr. Opin. Struct. Biol. 12, 509-515. <https://doi.org/10.1016/S0959-440X(02)00355-X>
19. 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. <https://doi.org/10.1074/jbc.272.23.14800>
20. Gao, T., Yatani, A., Dell’Acqua, M. L., Sako, H., Green, S. A., Dascal, N., Scott, J. D., Hosey, M. M. (1997) cAMPdependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19, 185-196. <https://doi.org/10.1016/S0896-6273(00)80358-X>
21. Gary, R., Bretscher, A. (1995) Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 6, 1061-1075. <https://doi.org/10.1091/mbc.6.8.1061>
22. Gautreau, A., Louvard, D., Arpin, M. (2000) Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J. Cell Biol. 150, 193-204. <https://doi.org/10.1083/jcb.150.1.193>
23. Goldsmith, S. R. (2006) Is there a cardiovascular rationale for the use of combined vasopressin V1a/V2 receptor antagonists? Am. J. Med. 119, S93-S96. <https://doi.org/10.1016/j.amjmed.2006.05.015>
24. Gorelick, D. A., Praetorius, J., Tsunenari, T., Nielsen, S., Agre, P. (2006) Aquaporin-11: a channel protein lacking apparent transport function expressed in brain. BMC Biochem. 7, 14. <https://doi.org/10.1186/1471-2091-7-14>
25. 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. <https://doi.org/10.1242/jcs.00053>
26. Hara-Chikuma, M., Sohara, E., Rai, T., Ikawa, M., Okabe, M., Sasaki, S., Uchida, S., Verkman, A.S. (2005) Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: adipocyte glycerol permeability as a novel regulator of fat accumulation. J. Biol. Chem. 280, 15493-15496. <https://doi.org/10.1074/jbc.C500028200>
27. Hasler, U., Mordasini, D., Bens, M., Bianchi, M., Cluzeaud, F., Rousselot, M.,. Vandewalle, A, Feraille, E., Martin, P.Y. (2002) Long term regulation of aquaporin-2 expression in vasopressin-responsive renal collecting duct principal cells. J. Biol. Chem. 277, 10379-10386. <https://doi.org/10.1074/jbc.M111880200>
28. Hedfalk, K., Tornroth-Horsefield, S., Nyblom, M., Johanson, U., Kjellbom, P., Neutze, R. (2006) Aquaporin gating. Curr. Opin. Struct. Biol. Memb. Eng. Des. 16, 447-456. <https://doi.org/10.1016/j.sbi.2006.06.009>
29. Henn, V., Edemir, B., Stefan, E., Wiesner, B., Lorenz, D., Theilig, F., Schmitt, R., Vossebein, L., Tamma, G., Beyermann, M., Krause, E., Herberg, F. W., Valenti, G., Bachmann, S., Rosenthal, W., Klussmann, E. (2004) Identification of a novel A-kinase anchoring protein 18 isoform and evidence for its role in the vasopressininduced aquaporin-2 shuttle in renal principal cells. J. Biol. Chem. 279, 26654-26665. <https://doi.org/10.1074/jbc.M312835200>
30. Hunter, T. (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225-236. <https://doi.org/10.1016/0092-8674(95)90405-0>
31. Inoue, T., Nielsen, S., Mandon, B., Terris, J., Kishore, B. K., M. A. Knepper, M. A., (1998) SNAP-23 in rat kidney: colocalization with aquaporin-2 in collecting duct vesicles. Am. J. Physiol. Renal Physiol. 275, F752-760. <https://doi.org/10.1152/ajprenal.1998.275.5.F752>
32. Ishibashi, K. (2006) Aquaporin subfamily with unusual NPA boxes. Biochim. Biophys. Acta 1758, 989-993. <https://doi.org/10.1016/j.bbamem.2006.02.024>
33. Johnson, B. D., Scheuer, T., Catterall, W. A. (1994) Voltagedependent potentiation of L-type Ca2+ channels in skeletal muscle cells requires anchored cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 91, 11492-11496. <https://doi.org/10.1073/pnas.91.24.11492>
34. Jung, J., Preston, G., Smith, B., Guggino, W., Agre, P. (1994) Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 269, 14648-14654. <https://doi.org/10.1016/S0021-9258(17)36674-7>
35. Kamsteeg, E. J., Heijnen, I., van Os, C. H., Deen, P. M. T. (2000) The subcellular localization of an aquaporin-2 tetramer depends on the stoichiometry of phosphorylated and nonphosphorylated monomers. J. Cell Biol. 151, 919-930. <https://doi.org/10.1083/jcb.151.4.919>
36. Kang, D.-Y., Park, J.-I., Cho, W.-S., Jeong, M.-H., Cho, G.W., Park, H.-T., Bae, H.-R. (2004) Identification of vasopressin-induced genes in AQP2-transfected MDCK cells by suppression subtractive hybridization. Biochem. Biophys. Res. Commun. 324, 1234-1241. <https://doi.org/10.1016/j.bbrc.2004.09.185>
37. King, L. S., Kozono, D., Agre, P. (2004) From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell Biol. 5, 687-698. <https://doi.org/10.1038/nrm1469>
38. Kishida, K., Shimomura, I., Kondo, H., Kuriyama, H., Makino, Y., Nishizawa, H., Maeda, N., Matsuda, M., Ouchi, N., Kihara, S., Kurachi, Y., Funahashi, T., Matsuzawa, Y. (2001) Genomic structure and insulinmediated repression of the aquaporin adipose (AQPap), adipose-specific glycerol channel. J. Biol. Chem. 276, 36251-36260. <https://doi.org/10.1074/jbc.M106040200>
39. Klussmann, E., Tamma, G., Lorenz, D.,. Wiesner, B., Maric, K., Hofmann, F., Aktories, K., Valenti, G., Rosenthal, W. (2001) An inhibitory role of Rho in the vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 276, 20451-20457. <https://doi.org/10.1074/jbc.M010270200>
40. Kong, Y., Ma J. (2001) Dynamic mechanisms of the membrane water channel aquaporin-1 (AQP1). Proc. Natl. Acad. Sci. USA 98, 14345-14349. <https://doi.org/10.1073/pnas.251507998>
41. Kozono, D., Yasui, M., King, L. S., Agre, P. (2002) Aquaporin water channels: atomic structure molecular dynamics meet clinical medicine. J. Clin. Invest. 109, 1395-1399. <https://doi.org/10.1172/JCI0215851>
42. Lang, P., Gesbert, F., Delespine-Carmagnat, M., Stancou, R., Pouchelet, M., Bertoglio, J. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15, 510-519. <https://doi.org/10.1002/j.1460-2075.1996.tb00383.x>
43. Lin, S.-H., D. Bichet, G., Sasaki, S., Kuwahara, M., Arthus, M.F., Lonergan, M., Lin, Y.F. (2002) Two novel aquaporin-2 mutations responsible for congenital nephrogenic diabetes insipidus in Chinese families. J. Clin. Endocrinol. Metab. 87, 2694-2700. <https://doi.org/10.1210/jcem.87.6.8617>
44. Lu, Y., Turnbull, I. R, Bragin, A., Carveth, K., Verkman, A. S., Skach, W. R. (2000) Reorientation of aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol. Biol. Cell 11, 2973-2985. <https://doi.org/10.1091/mbc.11.9.2973>
45. Mandon, B., Chou, C.-L., Nielsen, S., Knepper, M. A. (1996) Syntaxin-4 is localized to the apical plasma membrane of rat renal collecting duct cells: possible role in aquaporin-2 trafficking. J. Clin. Invest. 98, 906-913. <https://doi.org/10.1172/JCI118873>
46. Marples, D., Schroer, T. A., Ahrens, N., Taylor, A., Knepper, M. A., Nielsen, S. (1998) Dynein and dynactin colocalize with AQP2 water channels in intracellular vesicles from kidney collecting duct. Am. J. Physiol. Renal Physiol. 274, F384-394. <https://doi.org/10.1152/ajprenal.1998.274.2.F384>
47. Marples, D., Frokiaer, J., Nielsen, S. (1999) Long-term regulation of aquaporins in the kidney. Am. J. Physiol. Renal Physiol. 276, F331-339. <https://doi.org/10.1152/ajprenal.1999.276.3.F331>
48. Musch, A. (2004) Microtubule organization and function in epithelial cells. Traffic 5, 1-9. <https://doi.org/10.1111/j.1600-0854.2003.00149.x>
49. Nielsen, S., Marples, D., Birn, H., Mohtashami, M., Dalby, N. O., 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. <https://doi.org/10.1172/JCI118229>
50. Noda, Y., Sasaki, S. (2005) Trafficking mechanism of water channel aquaporin-2. Biol. Cell 97, 885-892. <https://doi.org/10.1042/BC20040120>
51. Pasel, K., Schulz, A., Timmermann, K., Linnemann, K., Hoeltzenbein, M., Jaaskelainen, J., Gruters, A., Filler, G., Schoneberg, T. (2000) Functional characterization of the molecular defects causing nephrogenic diabetes insipidus in eight families. J. Clin. Endocrinol. Metab. 85, 1703-1710.
52. Pfeffer, S. R. (1999) Transport-vesicle targeting: tethers before SNAREs. Nat. Cell. Biol. 1, E17-22. <https://doi.org/10.1038/8967>
53. Pomes, R., Roux, B. (1996) Structure and dynamics of a proton wire: a theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel. Biophys. J. 71, 19-39. <https://doi.org/10.1016/S0006-3495(96)79211-1>
54. Preston, G., 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. USA 88, 11110-11114. <https://doi.org/10.1073/pnas.88.24.11110>
55. Ren, G., Reddy, V. S., Cheng, A., Melnyk, P., Mitra, A. K. (2001) Visualization of a water-selective pore by electron crystallography in vitreous ice. Proc. Natl. Acad. Sci. USA 98, 1398-1403. <https://doi.org/10.1073/pnas.98.4.1398>
56. Shi, L., Skach, W., Verkman, A. (1994) Functional independence of monomeric CHIP28 water channels revealed by expression of wild-type mutant heterodimers. J. Biol. Chem. 269, 10417-10422. <https://doi.org/10.1016/S0021-9258(17)34076-0>
57. Simon, H., Gao, Y., Franki, N., Hays, R. M. (1993) Vasopressin depolymerizes apical F-actin in rat inner medullary collecting duct. Am. J. Physiol. Cell Physiol. 265, C757-762. <https://doi.org/10.1152/ajpcell.1993.265.3.C757>
58. Tajkhorshid, E., Nollert, P., Jensen, M. O., Miercke, L. J., O’Connell, J., Stroud, R.M., Schulten, K. (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296, 525-530. <https://doi.org/10.1126/science.1067778>
59. Tamarappoo, B. K., A. S. Verkman (1998) Defective aquaporin-2 trafficking in nephrogenic diabetes insipidus and correction by chemical chaperones. J. Clin. Invest. 101, 2257-2267. <https://doi.org/10.1172/JCI2303>
60. Tamma, G., Klussmann, E., Maric, K., Aktories, K., Svelto, M., Rosenthal, W., Valenti, G. (2001) Rho inhibits cAMPinduced translocation of aquaporin-2 into the apical membrane of renal cells. Am. J. Physiol. Renal Physiol. 281, F1092-1101. <https://doi.org/10.1152/ajprenal.0091.2001>
61. 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. <https://doi.org/10.1242/jcs.02495>
62. Terris, J., Ecelbarger, C. A., Nielsen, S., Knepper, M. A. (1996) Long-term regulation of four renal aquaporins in rats. Am. J. Physiol. Renal Physiol. 271, F414-422. <https://doi.org/10.1152/ajprenal.1996.271.2.F414>
63. Tsukita, S., Yonemura, S., Tsukita, S. (1997) ERM (ezrin/radixin/moesin) family: from cytoskeleton to signal transduction. Curr. Opin. Cell Biol. 9, 70-75. <https://doi.org/10.1016/S0955-0674(97)80154-8>
64. Valenti, G., Procino, G., Carmosino, M., Frigeri, A., Mannucci, R., Nicoletti, I., Svelto, M. (2000) The phosphatase inhibitor okadaic acid induces AQP2 translocation independently from AQP2 phosphorylation in renal collecting duct cells. J. Cell Sci. 113, 1985-1992. <https://doi.org/10.1242/jcs.113.11.1985>
65. Van Aelst, L., D’Souza-Schorey, C. (1997) Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322. <https://doi.org/10.1101/gad.11.18.2295>
66. van Balkom, B. W. M., Savelkoul, P. J. M., Markovich, D., Hofman, E., Nielsen, S., van der Sluijs, P., Deen, P. M. T. (2002) The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J. Biol. Chem. 277, 41473-41479. <https://doi.org/10.1074/jbc.M207525200>
67. van Balkom, B. W. M., Hoffert, J. D., Chou, C.-L., Knepper, M. A. (2004) Proteomic analysis of long-term vasopressin action in the inner medullary collecting duct of the Brattleboro rat. Am. J. Physiol. Renal Physiol. 286, F216-224. <https://doi.org/10.1152/ajprenal.00307.2003>
68. Voth, D. E., Ballard, J. D. (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 18, 247-263. <https://doi.org/10.1128/CMR.18.2.247-263.2005>
69. Yonemura, S., Matsui, T., Tsukita, S., Tsukita, S. (2002) Rhodependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580. <https://doi.org/10.1242/jcs.115.12.2569>
70. Zardoya, R. (2005) Phylogeny and evolution of the major intrinsic protein family. Biol. Cell 97, 397-414. <https://doi.org/10.1042/BC20040134>
71. Zelenina, M., Christensen, B. M., Palmer, J., Nairn, A. C., Nielsen, S., Aperia, A. (2000) Prostaglandin E2 interaction with AVP: effects on AQP2 phosphorylation and distribution. Am. J. Physiol. Renal Physiol. 278, F388-394. <https://doi.org/10.1152/ajprenal.2000.278.3.F388>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive