Structure, function and translational relevance of aquaporin dual water and ion channels

Molecular Aspects of Medicine

Volumn 33, Issue 5-6, 2012, Pages 553-561

  Yool, Andrea J ^a   Campbell, Ewan M ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

AQP; Arylsulfonamide; Cyclic GMP; Fluid transport; MIP; Nonselective cation channel

Indexed keywords

AMINO ACID; AQUAPORIN; AQUAPORIN 0; AQUAPORIN 1; AQUAPORIN 6; GLYCEROL; ION CHANNEL; NODULIN; NODULIN 26 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; HUMAN; ION CONDUCTANCE; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; WATER PERMEABILITY;

AMINO ACID SEQUENCE; ANIMALS; AQUAGLYCEROPORINS; AQUAPORINS; BIOLOGICAL TRANSPORT; GLYCEROL; HUMANS; MOLECULAR SEQUENCE DATA; PLANTS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; WATER; WATER-ELECTROLYTE BALANCE;

EID: 84865527559     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2012.02.001     Document Type: Review

References (81)

1. T.L. Anthony, H.L. Brooks, D. Boassa, S. Leonov, G.M. Yanochko, J.W. Regan, and A.J. Yool Cloned human aquaporin-1 is a cyclic GMP-gated ion channel Mol. Pharmacol. 57 3 2000 576 588
2. M.B. Arciszewski, M. Stefaniak, A. Zacharko-Siembida, and J. Calka Aquaporin 1 water channel is expressed on submucosal but not myenteric neurons from the ovine duodenum Ann. Anat. 193 2 2010 81 85
3. I. Arnaoutova, N.X. Cawley, N. Patel, T. Kim, T. Rathod, and Y.P. Loh Aquaporin 1 is important for maintaining secretory granule biogenesis in endocrine cells Mol. Endocrinol. 22 8 2008 1924 1934
4. N.W. Baetz, E.A. Hoffman, A.J. Yool, and W.D. Stamer Role of aquaporin-1 in trabecular meshwork cell homeostasis during mechanical strain Exp. Eye Res. 89 1 2009 95 100
5. G. Benga, O. Popescu, V. Borza, V.I. Pop, A. Muresan, I. Mocsy, A. Brain, and J.M. Wrigglesworth Water permeability in human erythrocytes: identification of membrane proteins involved in water transport Eur. J. Cell Biol. 41 2 1986 252 262
6. G. Benga, O. Popescu, V.I. Pop, and R.P. Holmes P-(Chloromercuri) benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes Biochemistry 25 7 1986 1535 1538
7. D. Boassa, W.D. Stamer, and A.J. Yool Ion channel function of aquaporin-1 natively expressed in choroid plexus J. Neurosci. 26 30 2006 7811 7819
8. D. Boassa, and A.J. Yool A fascinating tail: cGMP activation of aquaporin-1 ion channels Trends Pharmacol. Sci. 23 12 2002 558 562
9. D. Boassa, and A.J. Yool Single amino acids in the carboxyl terminal domain of aquaporin-1 contribute to cGMP-dependent ion channel activation BMC Physiol. 3 2003 12
10. D. Boassa, and A.J. Yool Physiological roles of aquaporins in the choroid plexus Curr. Top. Dev. Biol. 67 2005 181 206
11. C. Bondy, E. Chin, B.L. Smith, G.M. Preston, and P. Agre Developmental gene expression and tissue distribution of the CHIP28 water-channel protein Proc. Natl. Acad. Sci. USA 90 10 1993 4500 4504
12. H.L. Brooks, J.W. Regan, and A.J. Yool Inhibition of aquaporin-1 water permeability by tetraethylammonium: involvement of the loop E pore region Mol. Pharmacol. 57 5 2000 1021 1026
13. B. Burghardt, M.L. Elkaer, T.H. Kwon, G.Z. Racz, G. Varga, M.C. Steward, and S. Nielsen Distribution of aquaporin water channels AQP1 and AQP5 in the ductal system of the human pancreas Gut 52 7 2003 1008 1016
14. E.M. Campbell, D.N. Birdsell, and A.J. Yool The activity of human aquaporin 1 as a cGMP-gated cation channel is regulated by tyrosine phosphorylation in the carboxyl terminal domain Mol. Pharmacol. 81 2012 1 9
15. G. Chandy, G.A. Zampighi, M. Kreman, and J.E. Hall Comparison of the water transporting properties of MIP and AQP1 J. Membr. Biol. 159 1 1997 29 39
16. C.A. Cowan, N. Yokoyama, L.M. Bianchi, M. Henkemeyer, and B. Fritzsch EphB2 guides axons at the midline and is necessary for normal vestibular function Neuron 26 2 2000 417 430
17. D. Doherty, L.Y. Jan, and Y.N. Jan The Drosophila neurogenic gene big brain, which encodes a membrane-associated protein, acts cell autonomously and can act synergistically with Notch and Delta Development 124 19 1997 3881 3893
18. M. Endo, R.K. Jain, B. Witwer, and D. Brown Water channel (aquaporin 1) expression and distribution in mammary carcinomas and glioblastomas Microvasc. Res. 58 2 1999 89 98
19. A. Frigeri, G.P. Nicchia, and M. Svelto Aquaporins as targets for drug discovery Curr. Pharm. Des. 13 23 2007 2421 2427
20. D. Gomes, A. Agasse, P. Thiebaud, S. Delrot, H. Geros, and F. Chaumont Aquaporins are multifunctional water and solute transporters highly divergent in living organisms Biochim. Biophys. Acta 1788 6 2009 1213 1228
21. C. Hachez, and F. Chaumont Aquaporins: a family of highly regulated multifunctional channels Adv. Exp. Med. Biol. 679 2010 1 17
22. Y. Hayashi, N.A. Edwards, M.A. Proescholdt, E.H. Oldfield, and M.J. Merrill Regulation and function of aquaporin-1 in glioma cells Neoplasia 9 9 2007 777 787
23. 2+ activation J. Biol. Chem. 277 32 2002 29224 29230
24. V.J. Huber, M. Tsujita, I.L. Kwee, and T. Nakada Inhibition of aquaporin 4 by antiepileptic drugs Bioorg. Med. Chem. 17 1 2009 418 424
25. V.J. Huber, M. Tsujita, M. Yamazaki, K. Sakimura, and T. Nakada Identification of arylsulfonamides as Aquaporin 4 inhibitors Bioorg. Med. Chem. Lett. 17 5 2007 1270 1273
26. J.H. Hwang, S.R. Ellingson, and D.M. Roberts Ammonia permeability of the soybean nodulin 26 channel FEBS Lett. 584 20 2010 4339 4343
27. I. Iandiev, T. Pannicke, M.B. Reichel, P. Wiedemann, A. Reichenbach, and A. Bringmann Expression of aquaporin-1 immunoreactivity by photoreceptor cells in the mouse retina Neurosci. Lett. 388 2 2005 96 99
28. M. Ikeda, E. Beitz, D. Kozono, W.B. Guggino, P. Agre, and M. Yasui Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63 J. Biol. Chem. 277 42 2002 39873 39879
29. P.A. Johansson, K.M. Dziegielewska, C.J. Ek, M.D. Habgood, K. Mollgard, A. Potter, M. Schuliga, and N.R. Saunders Aquaporin-1 in the choroid plexuses of developing mammalian brain Cell Tissue Res. 322 3 2005 353 364
30. J.S. Jung, G.M. Preston, B.L. Smith, W.B. Guggino, and P. Agre Molecular structure of the water channel through aquaporin CHIP. The hourglass model J. Biol. Chem. 269 20 1994 14648 14654
31. K. Jurkat-Rott, H. Lerche, Y. Weber, and F. Lehmann-Horn Hereditary channelopathies in neurology Adv. Exp. Med. Biol. 686 2010 305 334
32. L.S. King, D. Kozono, and P. Agre From structure to disease: the evolving tale of aquaporin biology Nat. Rev. Mol. Cell Biol. 5 9 2004 687 698
33. C. Kushmerick, S.J. Rice, G.J. Baldo, H.C. Haspel, and R.T. Mathias Ion, water and neutral solute transport in Xenopus oocytes expressing frog lens MIP Exp. Eye Res. 61 3 1995 351 362
34. J.W. Lee, Y. Zhang, C.D. Weaver, N.H. Shomer, C.F. Louis, and D.M. Roberts Phosphorylation of nodulin 26 on serine 262 affects its voltage-sensitive channel activity in planar lipid bilayers J. Biol. Chem. 270 45 1995 27051 27057
35. M.H. Levin, and A.S. Verkman Aquaporins and CFTR in ocular epithelial fluid transport J. Membr. Biol. 210 2 2006 105 115
36. K. Liu, D. Kozono, Y. Kato, P. Agre, A. Hazama, and M. Yasui Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution Proc. Natl. Acad. Sci. USA 102 6 2005 2192 2197
37. T. Ma, B. Yang, A. Gillespie, E.J. Carlson, C.J. Epstein, and A.S. Verkman Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels J. Biol. Chem. 273 8 1998 4296 4299
38. J.M. Markert, C.M. Fuller, G.Y. Gillespie, J.K. Bubien, L.A. McLean, R.L. Hong, K. Lee, S.R. Gullans, T.B. Mapstone, and D.J. Benos Differential gene expression profiling in human brain tumors Physiol. Genomics 5 1 2001 21 33
39. E. McCoy, and H. Sontheimer Expression and function of water channels (aquaporins) in migrating malignant astrocytes Glia 55 10 2007 1034 1043
40. E. Migliati, N. Meurice, P. DuBois, J.S. Fang, S. Somasekharan, E. Beckett, G. Flynn, and A.J. Yool Inhibition of aquaporin-1 and aquaporin-4 water permeability by a derivative of the loop diuretic bumetanide acting at an internal pore-occluding binding site Mol. Pharmacol. 76 1 2009 105 112
41. E. Modesto, L. Barcellos, and A.C. Campos-de-Carvalho MIP 28 forms channels in planar lipid bilayers Braz. J. Med. Biol. Res. 23 10 1990 1029 1032
42. E. Modesto, P.D. Lampe, M.C. Ribeiro, D.C. Spray, and A.C. Campos de Carvalho Properties of chicken lens MIP channels reconstituted into planar lipid bilayers J. Membr. Biol. 154 3 1996 239 249
43. S.M. Mulders, G.M. Preston, P.M. Deen, W.B. Guggino, C.H. van Os, and P. Agre Water channel properties of major intrinsic protein of lens J. Biol. Chem. 270 15 1995 9010 9016
44. M. Nagahama, N. Ma, R. Semba, and S. Naruse Aquaporin 1 immunoreactive enteric neurons in the rat ileum Neurosci. Lett. 395 3 2006 206 210
45. K.L. Nemeth-Cahalan, and J.E. Hall PH and calcium regulate the water permeability of aquaporin 0 J. Biol. Chem. 275 10 2000 6777 6782
46. J.M. Nerbonne, C.G. Nichols, T.L. Schwarz, and D. Escande Genetic manipulation of cardiac K(+) channel function in mice. what have we learned, and where do we go from here? Circ. Res. 89 11 2001 944 956
47. S. Nielsen, B.L. Smith, E.I. Christensen, and P. Agre Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia Proc. Natl. Acad. Sci. USA 90 15 1993 7275 7279
48. C.M. Niemietz, and S.D. Tyerman Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules FEBS Lett. 465 2-3 2000 110 114
49. Oshio, K.; Binder, D.K.; Liang, Y.; Bollen, A.; Feuerstein, B.; Berger, M.S.; Manley, G.T.; 2005. Expression of the aquaporin-1 water channel in human glial tumors. Neurosurgery 56 (2),375-381 (discussion 375-381).
50. K. Oshio, H. Watanabe, D. Yan, A.S. Verkman, and G.T. Manley Impaired pain sensation in mice lacking Aquaporin-1 water channels Biochem. Biophys. Res. Commun. 341 4 2006 1022 1028
51. E. Page, J. Winterfield, G. Goings, A. Bastawrous, and J. Upshaw-Earley Water channel proteins in rat cardiac myocyte caveolae: osmolarity-dependent reversible internalization Am. J. Physiol. 274 6 Pt 2 1998 H1988 H2000
52. T.L. Pannabecker, A. Dahlmann, O.H. Brokl, and W.H. Dantzler Mixed descending- and ascending-type thin limbs of Henle's loop in mammalian renal inner medulla Am. J. Physiol. Renal. Physiol. 278 2 2000 F202 F208
53. G.M. Preston, T.P. Carroll, W.B. Guggino, and P. Agre Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein Science 256 5055 1992 385 387
54. G.M. Preston, J.S. Jung, W.B. Guggino, and P. Agre Membrane topology of aquaporin CHIP. Analysis of functional epitope-scanning mutants by vectorial proteolysis J. Biol. Chem. 269 3 1994 1668 1673
55. Y. Rao, R. Bodmer, L.Y. Jan, and Y.N. Jan The big brain gene of Drosophila functions to control the number of neuronal precursors in the peripheral nervous system Development 116 1 1992 31 40
56. J. Reizer, A. Reizer, and M.H. Saier Jr. The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins Crit. Rev. Biochem. Mol. Biol. 28 3 1993 235 257
57. S.M. Saparov, D. Kozono, U. Rothe, P. Agre, and P. Pohl Water and ion permeation of aquaporin-1 in planar lipid bilayers. Major differences in structural determinants and stoichiometry J. Biol. Chem. 276 34 2001 31515 31520
58. L. Shen, P. Shrager, S.J. Girsch, P.J. Donaldson, and C. Peracchia Channel reconstitution in liposomes and planar bilayers with HPLC-purified MIP26 of bovine lens J. Membr. Biol. 124 1 1991 21 32
59. Stamer, W.; Baetz, N.; Yool, A.; 2008. Ocular aquaporins and aqueous humor dynamics. In: Civan, M. (Ed.), Current Topics in Membranes: The Eye's Aqueous Humor. Elsevier Inc.
60. W.D. Stamer, Y. Huang, R.E. Seftor, S.S. Svensson, R.W. Snyder, and J.W. Regan Cultured human trabecular meshwork cells express functional alpha 2A adrenergic receptors Invest. Ophthalmol. Vis. Sci. 37 12 1996 2426 2433
61. K. Tatsumi, S. Tsuji, H. Miwa, T. Morisaku, M. Nuriya, M. Orihara, K. Kaneko, H. Okano, and M. Yasui Drosophila big brain does not act as a water channel, but mediates cell adhesion FEBS Lett. 583 12 2009 2077 2082
62. S. Tornroth-Horsefield, Y. Wang, K. Hedfalk, U. Johanson, M. Karlsson, E. Tajkhorshid, R. Neutze, and P. Kjellbom Structural mechanism of plant aquaporin gating Nature 439 7077 2006 688 694
63. S.P. Tsunoda, B. Wiesner, D. Lorenz, W. Rosenthal, and P. Pohl Aquaporin-1, nothing but a water channel J. Biol. Chem. 279 12 2004 11364 11367
64. K. Varadaraj, C. Kushmerick, G.J. Baldo, S. Bassnett, A. Shiels, and R.T. Mathias The role of MIP in lens fiber cell membrane transport J. Membr. Biol. 170 3 1999 191 203
65. C.D. Weaver, N.H. Shomer, C.F. Louis, and D.M. Roberts Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel J. Biol. Chem. 269 27 1994 17858 17862
66. B. Yang, T. Ma, and A.S. Verkman Erythrocyte water permeability and renal function in double knockout mice lacking aquaporin-1 and aquaporin-3 J. Biol. Chem. 276 1 2001 624 628
67. G.M. Yanochko, and A.J. Yool Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain J. Neurosci. 22 7 2002 2530 2540
68. G.M. Yanochko, and A.J. Yool Block by extracellular divalent cations of Drosophila big brain channels expressed in Xenopus oocytes Biophys. J. 86 3 2004 1470 1478
69. M. Yasui, A. Hazama, T.H. Kwon, S. Nielsen, W.B. Guggino, and P. Agre Rapid gating and anion permeability of an intracellular aquaporin Nature 402 6758 1999 184 187
70. A. Yool, O. Brokl, T. Pannabecker, W. Dantzler, and W. Stamer Tetraethylammonium block of water flux in Aquaporin-1 channels expressed in kidney thin limbs of Henle's loop and a kidney-derived cell line BMC Physiol. 2 2002 4
71. A.J. Yool Aquaporins: multiple roles in the central nervous system Neuroscientist 13 5 2007 470 485
72. A.J. Yool Dominant-negative suppression of big brain ion channel activity by mutation of a conserved glutamate in the first transmembrane domain Gene. Expr. 13 6 2007 329 337
73. A.J. Yool Functional domains of aquaporin-1: keys to physiology, and targets for drug discovery Curr. Pharm. Des. 13 31 2007 3212 3221
74. A.J. Yool, E.A. Brown, and G.A. Flynn Roles for novel pharmacological blockers of aquaporins in the treatment of brain oedema and cancer Clin. Exp. Pharmacol. Physiol 37 2010 403 409
75. A.J. Yool, and W.D. Stamer Novel roles for aquaporins as gated ion channels R.A. Maui, Molecular and Cellular Insights to Ion Channel Biology 2004 Elsevier Amsterdam 351 357
76. A.J. Yool, W.D. Stamer, and J.W. Regan Forskolin stimulation of water and cation permeability in aquaporin 1 water channels Science 273 5279 1996 1216 1218
77. A.J. Yool, and A.M. Weinstein New roles for old holes: Ion channel function in aquaporin-1 News Physiol. Sci. 17 2002 68 72
78. J. Yu, A.J. Yool, K. Schulten, and E. Tajkhorshid Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1 Structure 14 9 2006 1411 1423
79. G.A. Zampighi, J.E. Hall, and M. Kreman Purified lens junctional protein forms channels in planar lipid films Proc. Natl. Acad. Sci. USA 82 24 1985 8468 8472
80. M. Zelenina, S. Zelenin, A.A. Bondar, H. Brismar, and A. Aperia Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine Am. J. Physiol. Renal. Physiol. 283 2 2002 F309 F318
81. W. Zhang, E. Zitron, M. Homme, L. Kihm, C. Morath, D. Scherer, S. Hegge, D. Thomas, C.P. Schmitt, M. Zeier, H. Katus, C. Karle, and V. Schwenger Aquaporin-1 channel function is positively regulated by protein kinase C J. Biol. Chem. 282 29 2007 20933 20940