Three-dimensional organization of the aquaporin water channel: What can structure tell us about function?

Vitamins and Hormones

Volumn 62, Issue , 2001, Pages 133-166

  Mitra, Alok K ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN;

AMINO ACID SEQUENCE; ANIMAL; BODY WATER; CHEMISTRY; CRYSTALLIZATION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; REVIEW; STRUCTURE ACTIVITY RELATION; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; ANIMALS; AQUAPORINS; BIOLOGICAL TRANSPORT; BODY WATER; CRYSTALLIZATION; HUMANS; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0035222461     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0083-6729(01)62003-x     Document Type: Review

References (125)

1. L Abrami V Berthonaud Glycerol permeability of mutant aquaporin 1 and other AQP-MIP proteins: Inhibition studies Pflugers Arch. 431 3 1996 408 414
2. P Agre Aquaporin nomenclature workshop: Mammalian aquaporins Biol. Cell. 89 1997 255 257
3. P Agre D Brown S Nielsen Aquaporin water channels: Unanswered questions and unresolved controversies Curr. Opin. Cell Biol. 7 1995 472 483
4. P Agre M.D Lee S Devidas W.B Guggino Aquaporins and ion conductance Science 275 1997 1490 [letter; comment]
5. P Agre G.M Preston Aquaporin CHIP: The archetypal molecular water channel Am. J. Physiol. 265 4/2 1993 F463 F476
6. L.A Amos R Henderson P.N.T Unwin Three-dimensional structure determination by electron microscopy of two-dimensional crystals Prog. Biophys. Mol. Biol. 39 1982 183 231
7. J.P Andersen B Vilsen Structure-function relationships of cation translocation by Ca(2+)- and Na+,K(+)-ATPases studied by site-directed mutagenesis FEBS Lett. 359 2/3 1995 101 106
8. +-ATPase in the open conformation Nature 392 1998 840 843
9. L Bai K Fushimi S Sasaki F Marumo Structure of aquaporin-2 vasopressin water channel J. Biol. Chem. 271 1996 5171 5176
10. S.P Balashov R Govindjee Effect of the arginine-82 to alanine mutation in bacteriorhodopsin on dark adaptation, proton release, and the photochemical cycle Biochemistry 32 39 1993 10331 10343
11. J Berriman N Unwin Analysis of transient structures by cryomicroscopy combined with rapid mixing of spray droplets Ultramicroscopy 56 1994 241 252
12. E Bibi The role of the ribosome-translocon complex in translation and assembly of polytopic membrane proteins Trend. Biol. Sci. 23 1998 51 55
13. M.J Borgnia D Kozono P Maloney P Agre Purification and functional reconstitution of bacterial aquaporins Biophys. Soc. Abstr 76 1999 W-Pos204
14. M.S Braiman T Mogi Vibrational spectroscopy of bacteriorhodopsin mutants. I. Tyrosine-185 protonates and deprotonates during the photocycle Proteins 3 4 1988 219 229
15. P Bron V Lagree A Froger J.-P Rolland J.-F Hubert C Delamarche S Deschamps I Pellerin D Thomas W Haase Oligomerization state of MIP proteins expressed in Xenopus Oocytes as revealed by freeze-fracture electronmicroscopy analysis J. Struct. Biol. 128 1999 287 296
16. D Brown T Katsura Cellular distribution of the aquaporins: A family of water channel proteins Histochem. Cell Biol. 104 1 1995 1 9
17. S.K Buchanan B.S Smith L Venkatramani D Xia L Esser M Palnitkar R Chakraborty D van der Helm J Deisenhofer Crystal structure of the outer membrane active transporter FepA from Escherichia coli Nat. Struct. Biol. 6 1999 56 63 [see comments]
18. V Cabiaux K.A Oberg P Pancoska T Walz P Agre A Engel Secondary structure comparison of aquaporin-1 and bacteriorhodopsin: A Fourier transform infrared spectroscopy study of two-dimensional membrane crystals Biophys. J. 73 1997 406 417
19. K.L Cahalan J.E Hall pH and calcium regulate the water permeability of aquaporin O J. Biol. Chem. 2000 (in press)
20. G Chang R.H Spencer A.T Lee M.T Barclay D.C Rees Structure of the MscL homolog from Mycobacterium tuberculosis : A gated mechanosensitive ion channel Science 282 1998 2220 2226
21. P Charnet C Labarca An open-channel blocker interacts with adjacent turns of alpha-helices in the nicotinic acetylcholine receptor Neuron 4 1 1990 87 95
22. A Cheng A.N van Hoek M Yeager A.S Verkman A.K Mitra Three-dimensional organization of a human water channel Nature 387 1997 627 630
23. L.A Coury J.C Mathai G.V Prasad J.L Brodsky P Agre M.L Zeidel Reconstitution of water channel function of aquaporins 1 and 2 by expression in yeast secretory vesicles Am. J. Physiol. 274 1998 F34 F42
24. M.J Daniels M.J Chrispeels M Yeager Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography J. Mol. Biol. 294 1999 1337 1349
25. P.M Deen M.A Verdijk N.V Knoers B Wieringa L.A Monnens C.H van Os B.A van Cost Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine Science 264 1994 92 95
26. B.M Denker B.L Smith F.P Kühajda P Agre Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules J. Biol. Chem. 263 1988 15634 15642
27. D.A Doyle J.M Cabral R.A Pfuetzner A Kuo J.M Gulbis S.L Cohen B.T Chait R MacKinnon The structure of the potassium channel: Molecular basis of K+ conduction and selectivity Science 280 1998 69 77
28. J Dubochet M Adrian J.J Chang J.C Homo J Lepault A.W McDowall P Schultz Cryo-electron microscopy of vitrified specimens Q. Rev. Biophys 21 1988 129 228
29. M Echevarria A.A Ilundain Aquaporins J. Physiol. Biochem. 54 1998 107 118
30. A Engel Y Fujiyoshi P Agre The importance of aquaporin water channel protein EMBO J. 19 2000 800 806
31. A Engel T Walz P Agre The aquaporin family of membrane water channels Curr. Opin. Struct. Biol. 4 1994 545 553
32. A.D Ferguson E Hofmann J.W Coulton K Diederichs W Welte Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide Science 282 1998 2215 2220
33. A Finkelstein In water movement through lipid bilayers, pores, and plasma membranes Theory and Reality 1987 Wiley New York 66 80
34. J.J Fischbarg J Li M Cheung F Czegledy P Iserovitch K Kuang Predictive evidence for a porin-type b-barrel fold in CHIP28 and other members of the MIP family: A restricted-pore model common to water channels and facilitators J. Membr. Biol. 143 1995 177 188
35. A Froger B Tallur D Thomas C Delamarche Prediction of functional residues in water channels and related proteins Prot. Sci. 7 1998 1458 1468
36. D.A Goldstein A.K Solomon Determination of equivalent pore radius of human red cells by osmotic pressure measurements J. Gen. Physiol. 44 1960 1 17
37. M.B Gorin S.B Yancey J Cline J.P Revel J Horwitz The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning Cell 39 1984 49 59
38. W.N Green N.S Millar Ion-channel assembly Trends Neurosci. 18 1995 280 287
39. N Grigorieff T.A Ceska K.H Downing J.M Baldwin R Henderson Electron-crystallographic refinement of the structure of bacteriorhodopsin J. Mol. Biol. 259 1996 393 421
40. P.I Haris D Chapman G Benga A Fourier-transform infrared spectroscopic investigation of the hydrogen-deuterium exchange and secondary structure of the 28-kDa channel-forming integral membrane protein (CHIP28) Eur. J. Biochem. 233 1995 649 654
41. L Hasler J.B Heymann A Engel J Kistler T Walz 2D crystallization of membrane proteins: Rationales and examples J. Struct. Biol. 121 1998 162 171
42. L Hasler T Walz P Tittmann H Gross J Kistler A Engel Purified lens major intrinsic protein forms highly ordered tetragonal two-dimensional arrays by reconstitution J. Mol. Biol. 279 1998 855 864
43. R Henderson J.M Baldwin T.A Ceska F Zemlin E Beckmann K.H Downing Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy J. Mol. Biol. 213 1990 899 929
44. J.B Heymann A Engel Structural clues in the sequences of the aquaporins J. Mol. Biol. 295 2000 1039 1053
45. J.B Heymann P Agre A Engel Progress on structure and function of aquaporin 1 J. Struct. Biol. 121 1998 191 206
46. J.P Hosler J.P Shapleigh Polar residues in helix VIII of subunit I of cytochrome c oxidase influence the activity and the structure of the active site Biochemistry 35 33 1996 10776 10783
47. K Imoto C Busch Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance Nature 335 6191 1988 645 648
48. S Iwata C Ostermeier B Ludwig H Michel Structure at 2.8 Å resolution of cytochrome c oxidase from Paracocus dentrificans Nature 376 1995 660 669
49. B.K Jap M Zulauf T Scheybani A Hefti W Baumeister U Aebi A Engel 2D crystallization: From art to science Ultramicroscopy 46 1992 45 84
50. B.K Jap H Li Structure of the osmo-regulated H2O-channel, AQP-CHIP, in projection at 3.5 Å resolution J. Mol. Biol. 251 1995 413 420
51. I Johansson M Karlsson V.K Shukla M.J Chrispeels C Larsson P Kjelbom Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation Plant Cell 10 1998 451 459
52. J.S Jung G.M Preston B.L Smith W.B Guggino P Agre Molecular structure of the water channel through aquaporin CHIP. The hourglass model J. Biol. Chem. 269 1994 14648 14654
53. E.J Kamsteeg T.A Wormhoudt J.P Rijss C.H van Os P.M Deen An impaired routing of wild-type aquaporin-2 after tetramerization with an aquaporin-2 mutant explains dominant nephrogenic diabetes insipidus EMBO J. 18 1999 2394 2400
54. Y Kimura D.G Vassylyev A Miyazawa A Kidera M Matsushima K Mitsuoka K Murata T Hirai Y Fujiyoshi Surface of bacteriorhodopsin revealed by high-resolution electron crystallography Nature 389 6647 1997 206 211
55. L.S King P Agre Pathophysiology of the aquaporin water channels Annu. Rev. Physiol. 58 1996 619 648
56. W Kühlbrandt Two-dimensional crystallization of membrane proteins Q. Rev. Biophys. 25 1992 1 49
57. W Kühlbrandt D.N Wang Y Fujiyoshi Atomic model of plant light-harvesting complex by electron crystallography Nature 367 1994 614 621
58. C Kushmerick K Varadaraj Effects of lens major intrinsic protein on glycerol permeability and metabolism J. Membr. Biol. 161 1 1998 9 19
59. M Kuwahara Y Gu Mercury-sensitive residues and pore site in AQP3 water channel Biochemistry 36 46 1997 13973 13978
60. V Lagree A Froger S Deschamps I Pellerin C Delamarche G Bonnec J Gouranton D Thomas J.F Hubert Oligomerization state of water channels and glycerol facilitators. Involvement of loop E J. Biol. Chem. 273 1999 33949 33953
61. V Lagree I Pellerin J.F Hubert F Tacnet F Le Caherec N Roudier D Thomas J Gouranton S Deschamps A yeast recombinant aquaporin mutant that is not expressed or mistargeted in Xenopus oocyte can be functionally analyzed in reconstituted proteoliposomes J. Biol. Chem. 273 1998 12422 12426
62. V Lagree A Froger S Deschamps J.E Hubert C Delamarche G Bonnec D Thomas J Gouranton I Pellerin Switch from an aquaporin to a glycerol channel by two amino acids substitution J. Biol. Chem. 274 1999 6817 6819
63. V Laize G Rousselet J.M Verbavatz V Berthonaud R Gobin N Roudier L Abrami P Ripoche F Tacnet Functional expression of the human CHIP28 water channel in a yeast secretory mutant FEBS Lett. 373 1995 269 274
64. V Laize P Ripoche F Tacnet Purification and functional reconstitution of the human CHIP28 water channel expressed in Saccharomyces cerevisiae Prot. Expr. Purif. 11 1997 284 288
65. M.B Lande I Jo M.L Zeidel M Somers H.W Harris Jr. Phosphorylation of aquaporin-2 does not alter the membrane water permeability of rat papillary water channel-containing vesicles J. Biol. Chem. 272 1996 5552 5557
66. H Li S Lee B.K Jap Molecular design of aquaporin-1 water channel as revealed by electron crystallography Nat. Struct. Biol. 4 1997 263 265 [letter]
67. T Ma B Yang A.M Gillespie E.J Carlson C.J Epstein A.S Verkman Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels J. Biol. Chem. 273 1997 4296 4299
68. R.I Macey Transport of water and urea in red blood cells Am. J. Physiol. 246 1984 C195 C203
69. R.I Macey R.E Farmer Inhibition of water and solute permeability in human red blood cells Biochim. Biophys. Acta 211 1 1970 104 106
70. J.C Mathai P Agre Hourglass pore-forming domains restrict aquaporin-1 assembly Biochemistry 38 1999 923 928
71. C Maurel R.T Kado J Guern M.J Chrispeels Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP EMBO J. 14 1995 3028 3035
72. A.K Meinild D.A Klaerke T Zeuthen Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporin 0–5 J. Biol. Chem. 273 1998 32446 32451
73. A.K Mitra A.N van Hoek M.C Wiener A.S Verkman M Yeager The CHIP28 water channel visualized in ice by electron crystallography Nat. Struct. Biol. 2 1995 726 729 [letter]
74. K Mitsuoka K Murata T Walz T Hirai P Agre J.B Heymann A Engel Y Fujiyoshi The structure of aquaporin-1 at 4.5-Å resolution reveals short α-helices in the center of the monomer J. Struct. Biol. 128 1999 34 43
75. A Miyazawa Y Fujiyoshi M Stowell N Unwin Nicotinic acetylcholine receptor at 4.6 Å resolution: Transverse tunnels in the channel wall J. Mol. Biol. 288 1999 765 786
76. 2 permeability of Xenopus oocytes Am. J. Physiol. 274 1998 C543 C548
77. S Nielsen B.L Smith E.L Christensen M.A Knepper P Agre CHIP28 water channels are localized in constitutively water-permeable segments of the nephron J. Cell. Biol. 120 1993 371 383
78. E Nogales S.G Wolf K.H Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 1999 2003
79. M.Y Okamura G Feher Proton transfer in reaction centers for photosynthetic bacteria Annu. Rev. Biochem. 61 1992 861 896
80. K.M Page C.A Curtis The functional role of the binding site aspartate in muscarinic acetylcholine receptors, probed by site-directed mutagenesis Eur. J. Pharmacol. 289 3 1995 429 437
81. G.M Pao L.-F Wu K.D Johnson M.J Höfte Chrispeels G Sweet N.N Sandal M.H Saier Jr. Evolution of the MIP family of integral membrane transport proteins Mol. Microbiol. 5 1991 33 37
82. G.V Prasad L.A Coury F Finn M.L Zeidel Reconstituted aquaporin 1 water channels transport C02 across membranes J. Biol. Chem. 273 1998 33123 33126
83. G.M Preston P Agre Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family Proc. Natl. Acad. Sci. USA 88 1991 11110 11114
84. G.M Preston T.P Carroll Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein Science 256 5055 1992 385 387
85. G.M Preston J.S Jung W.B Guggino P Agre The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel J. Biol. Chem. 268 1993 17 20
86. G.M Preston B.L Smith M.L Zeidel J.J Moulds P Agre Mutations in aquaporin-1 in phenotypically normal humans without functional CHIP water channels Science 265 1994 1585 1587
87. J Reizer A Reizer 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
88. G Ren A Cheng P Melnyk A.K Mitra Polymorphism in the packing of aquaporin-1 tetramers in 2-D crystals J. Struct. Biol. 135 2000 45 53
89. G Ren P Melnyk A.K Mitra Structural analysis of the binding of a mercurial reagent to AQP1 by electron cryo-crystallography Biophys. Soc. Abstr 76 1999 M-AM-A5
90. P Ringler M.J Borgnia H Stahlberg P.C Maloney P Agre A Engel Structure of the water channel AQPZ from Escherichia coli revealed by electron crystallography J. Mol. Biol. 291 1999 1181 1190
91. L.B Shi A.S Verkman Selected cysteine point mutations confer mercurial sensitivity to the mercurial-insensitive water channel MIWC/AQP-4 Biochemistry 35 2 1996 538 544
92. L.B Shi W.R Skach Distinct biogenesis mechanisms for the water channels MIWC and CHIP28 at the endoplasmic reticulum Biochemistry 34 26 1995 8250 8256
93. L.B Shi W.R Skach A.S Verkman Functional independence of monomeric CHIP28 water channels revealed by expression of wild-type mutant heterodimers J. Biol. Chem. 269 1994 10417 10422
94. B.L Smith P Agre Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins J. Biol. Chem. 266 1991 6407 6415
95. B.L Smith G.M Preston F.A Spring D.J Anstee P Agre Human red cell aquaporin CHIP I. Molecular characterization of ABH and colton blood group antigens J. Clin. Invest. 94 1994 1043 1049
96. H Tsukaguchi C Shayakul B Berger B Mackenzie S Devidas W.B Guggino A.N van Hoek M.A Hediger Molecular characterization of a broad selectivity neutral solute channel J. Biol. Chem. 273 1998 24737 24743
97. N Unwin Acetylcholine receptor channel imaged in the open state Nature 373 1995 37 43
98. N Unwin The nicotinic acetylcholine receptor of the Torpedo electric ray J. Struct. Biol. 121 1998 181 190
99. A.N van Hoek M.L Hom L.H Luthjens M.D de Jong J.A Dempster C.H van Os Functional unit of 30 kDa for proximal tubule water channels as revealed by radiation inactivation J. Biol Chem. 266 1991 16633 16635
100. A.N van Hoek L.H Luthjens A 30-kDa functional size for the erythrocyte water channel determined in situ by radiation inactivation Biochem. Biophys. Res. Commun. 184 3 1992 1331 1338
101. A.N van Hoek M Wiener S Bicknese L Miercke J Biwersi A.S Verkman Secondary structure analysis of purified functional CHIP28 water channels by CD and FTIR spectroscopy Biochemistry 32 1993 11847 11856
102. A.N van Hoek M.C Wiener J.M Verbavatz D Brown P.H Lipniunas P.R Townsend A.S Verkman Purification and structure-function analysis of native, PNGase F-treated, and endo-beta-galactosidase-treated CHIP28 water channels Biochemistry 34 1995 2212 2222
103. J.M Verbavatz D Brown L Sabolic G Valenti D.A Ausiello A.N Van Hoek T Ma A.S Verkman Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: A freeze-fracture study J. Cell. Biol. 123 1993 605 618
104. A.S Verkman A.N van Hoek T Ma A Frigeri W.R Skach A Mitra B.K Tamarappoo J Farinas Water transport across mammalian cell membranes Am. J. Physiol. 270 1996 C12 C30
105. A.S Verkman A.K Mitra Structure and function of aquaporin water channels Am. J. Physiol. 278 2000 F13 F28
106. T Walz B.L Smith P Agre A Engel The three-dimensional structure of human erythrocyte aquaporin CHIP EMBO J. 13 1994 2985 2993
107. T Walz B.L Smith M.L Zeidel A Engel P Agre Biologically active two-dimensional crystals of aquaporin CHIP J. Biol. Chem. 269 1994 1583 1586
108. T Walz D Typke B.L Smith P Agre A Engel Projection map of aquaporin-1 determined by electron crystallography Nat. Struct. Biol. 2 1995 730 732 [letter]
109. T Walz P Tittmann K.H Fuchs D.J Muller B.L Smith P Agre H Gross A Engel Surface topographies at subnanometer-resolution reveal asymmetry and sidedness of aquaporin-1 J. Mol. Biol. 264 1996 907 918
110. T Walz T Hirai K Murata J.B Heymann K Mitsuoka Y Fujiyoshi B.L Smith P Agre A Engel The three-dimensional structure of aquaporin-1 Nature 387 1997 624 662
111. D.J Welling P.A Welling L.W Welling Filled pore approximation: A theoretical framework for solute-solvent coupling in narrow water channels Am. J. Physiol. 270 1996 C1246 C1254
112. G.J Wistow M.M Pisano A.B Chepelinsky Tandem sequence repeats in transmembrane channel proteins Trends Biochem. Sci. 16 1991 170 171
113. J Yang Y.N Jan L.Y Jan Determination of the subunit stoichiometry of an inwardly rectifying potassium channel Neuron 15 1995 1441 1447
114. B Yang A.N van Hoek A.S Verkman Very high single channel water permeability of aquaporin-4 in baculovirus-infected insect cells and liposomes reconstituted with purified aquaporin-4 Biochemistry 36 1997 7625 7632
115. B Yang A.S Verkman 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 1997 16140 16146
116. B Yang N Fukuda A van Hoek M.A Matthay T Ma A.S Verkman Carbon dioxide permeability of aquaporin-1 measured in erythrocytes and lung of aquaporin-1 null mice and in reconstituted proteoliposomes J. Biol. Chem. 275 4 2000 2686 2692
117. M Yasui A Nazama T.-H Kwon S Nielsen W Guggino P Agre Rapid gating of an intracellular aquaporin Nature 402 1999 184 187
118. A.J Yool W.D Stamer J.W Regan Forskolin stimulation of water and cation permeability in aquaporin 1 water channels Science 273 1996 1216 1218
119. M.L Zeidel S.V Ambudkar B.L Smith P Agre Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein] Biochemistry 31 1992 7436 7440
120. M.L Zeidel S Nielsen B.L Smith S.V Ambudkar A.B Maunsbach P Agre Ultrastructure, pharmacologic inhibition, and transport selectivity of aquaporin channel-forming integral protein in proteoliposomes Biochemistry 33 1994 1606 1615
121. + J. Biol. Chem. 274 1999 21631 21636
122. P Zhang C Toyoshima K Yonekura N.M Green D.L Stokes Structure of the calcium pump from sarcoplasmic reticulum at 8-Å resolution Nature 392 1998 835 839
123. R Zhang S.L Alper Evidence from oocyte expression that the erythrocyte water channel is distinct from band 3 and the glucose transporter J. Clin Invest. 88 5 1991 1553 1558
124. R.B Zhang K.A Logee Expression of mRNA coding for kidney and red cell water channels in Xenopus oocytes J. Biol. Chem. 265 26 1990 15375 15378
125. R Zhang A.N van Hoek A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k Biochemistry 32 12 1993 2938 2941