Mechanism of Gating and Ion Conductivity of a Possible Tetrameric Pore in Aquaporin-1

Structure

Volumn 14, Issue 9, 2006, Pages 1411-1423

  Yu, Jin ^a   Yool, Andrea J ^b   Schulten, Klaus ^a   Tajkhorshid, Emad ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Program in Neuroscience   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AQUAPORIN 1; ARGININE; CYCLIC GMP; WATER;

ARTICLE; BINDING SITE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COW; CRYSTAL STRUCTURE; HYDRATION; ION CONDUCTANCE; ION TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIMULATION;

AMINO ACID SEQUENCE; AQUAPORIN 1; CYCLIC GMP; CYTOPLASM; ION CHANNEL GATING; ION TRANSPORT; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 33748196115     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.07.006     Document Type: Article

References (72)

1. Abu-Hamdah R., Cho W.J., Cho S.J., Jeremic A., Kelly M., Ilie A.E., and Jena B.P. Regulation of the water channel aquaporin-1: isolation and reconstitution of the regulatory complex. Cell Biol. Int. 28 (2004) 7-17
2. Agre P. Aquaporin water channels (nobel lecture). Angew. Chem. Int. Ed. Engl. 43 (2004) 4278-4290
3. Agre P., Bonhivers M., and Borgnia M.J. The aquaporins, blueprints for cellular plumbing systems. J. Biol. Chem. 273 (1998) 14659-14662
4. Agre P., King L.S., Yasui M., Guggino W.B., Ottersen O.P., Fujiyoshi Y., Engel A., and Nielsen S. Aquaporin water channels-from atomic structure to clinical medicine. J. Physiol. 542 (2002) 3-16
5. Allen R., Melchionna S., and Hansen J. Intermittent permeation of cylindrical nanopores by water. Phys. Rev. Lett. 89 (2002) 175502
6. Anthony T., Brooks H., Boassa D., Leonov S., Yanochko G., Regan J., and Yool A. Cloned human aquaporin-1 is a cyclic GMP-gated ion channel. Mol. Pharmacol. 57 (2000) 576-588
7. Beckstein O., and Sansom M.S.P. Liquid-vapor oscillations of water in hydrophobic nanopores. Proc. Natl. Acad. Sci. USA 100 (2003) 7063-7068
8. Beckstein O., and Sansom M.S. The influence of geometry, surface character, and flexibility on the permeation of ions and water through biological pores. Phys. Biol. 1 (2004) 42-52
9. Beckstein O., Tai K., and Sansom M.S.P. Not ions alone: barriers to ion permeation in nanopores and channels. J. Am. Chem. Soc. 126 (2004) 14694-14695
10. Boassa D., and Yool A. A fascinating tail: cGMP activation of aquaporin-1 ion channels. Trends Pharmacol. Sci. 23 (2002) 558-562
11. Boassa D., and Yool A. Single amino acids in the carboxyl terminal domain of aquaporin-1 ion channels contribute to cGMP-dependent activation. BMC Physiol. 3 (2003) 12
12. Boassa D., Stamer W.D., and Yool A.J. Ion channel function of aquaporin-1 natively expressed in choroid plexus. J. Neurosci. (2006) 7811-7819
13. Bok D., Dockstader J., and Horwitz J. Immunocytochemical localization of the lens main intrinsic polypeptide (MIP26) in communicating junctions. J. Cell Biol. 92 (1982) 213-220
14. Borgnia M., Nielsen S., Engel A., and Agre P. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68 (1999) 425-458
15. Brünger A.T. X-PLOR, Version 3.1: A System for X-Ray Crystallography and NMR (1992), Yale University Press, New Haven, CT
16. Chakrabarti N., Tajkhorshid E., Roux B., and Pomès R. Molecular basis of proton blockage in aquaporins. Structure 12 (2004) 65-74
17. de Groot B.L., and Grubmüller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294 (2001) 2353-2357
18. de Groot B.L., Engel A., and Grubmüller H. A refined structure of human aquaporin-1. FEBS Lett. 504 (2001) 206-211
19. de Groot B.L., Frigato T., Helms V., and Grubmüller H. The mechanism of proton exclusion in the aquaporin-1 water channel. J. Mol. Biol. 333 (2003) 279-293
20. Echtay K., Bienengraeber M., and Klingenberg M. Role of intrahelical arginine residues in functional properties of uncoupling protein (ucp1). Biochemistry 40 (2001) 5243-5248
21. Essmann U., Perera L., Berkowitz M.L., Darden T., Lee H., and Pedersen L.G. A smooth particle mesh Ewald method. J. Chem. Phys. 103 (1995) 8577-8593
22. Feller S.E., Zhang Y.H., Pastor R.W., and Brooks B.R. Constant pressure molecular dynamics simulation-the Langevin piston method. J. Chem. Phys. 103 (1995) 4613-4621
23. Fidyk N., and Cerione R. Understanding the catalytic mechanism of GTPase-activating proteins: demonstration of the importance of switch domain stabilization in the stimulation of GTP hydrolysis. Biochemistry 41 (2002) 15644-15653
24. Fu D., Libson A., Miercke L.J.W., Weitzman C., Nollert P., Krucinski J., and Stroud R.M. Structure of a glycerol conducting channel and the basis for its selectivity. Science 290 (2000) 481-486
25. Gonen T., Sliz P., Kistler J., Cheng Y., and Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429 (2004) 193-197
26. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., and Walz T. Lipidprotein interactions in double-layered two-dimensional AQP0 crystals. Nature 438 (2005) 633-638
27. Grayson P., Tajkhorshid E., and Schulten K. Mechanisms of selectivity in channels and enzymes studied with interactive molecular dynamics. Biophys. J. 85 (2003) 36-48
28. Harries W.E.C., Akhavan D., Miercke L.J.W., Khademi S., and Stroud R. The channel architecture of aquaporin 0 at a 2.2-angstrom resolution. Proc. Natl. Acad. Sci. USA 101 (2004) 14045-14050
29. Heymann J.B., and Engel A. Aquaporins: phylogeny, structure, and physiology of water channels. News Physiol. Sci. 14 (1999) 187-193
30. Heymann J.B., Agre P., and Engel A. Progress on the structure and function of aquaporin 1. J. Struct. Biol. 121 (1998) 191-206
31. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38
32. Ilan B., Tajkhorshid E., Schulten K., and Voth G.A. The mechanism of proton exclusion in aquaporin channels. Proteins 55 (2004) 223-228
33. Isralewitz B., Gao M., and Schulten K. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 11 (2001) 224-230
34. + channel functions. Annu. Rev. Physiol. 54 (1992) 537-555
35. Jensen M.Ø., Tajkhorshid E., and Schulten K. The mechanism of glycerol conduction in aquaglyceroporins. Structure 9 (2001) 1083-1093
36. Jensen M.Ø., Park S., Tajkhorshid E., and Schulten K. Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc. Natl. Acad. Sci. USA 99 (2002) 6731-6736
37. Jensen M.Ø., Tajkhorshid E., and Schulten K. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85 (2003) 2884-2899
38. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
39. King L., and Arge P. Pathophysiology of the aquaporin water channels. Annu. Rev. Physiol. 58 (1996) 619-648
40. Lee J.K., Kozono D., Remis J., Kitagawa Y., Agre P., and Stroud R. Structural basis for water conductance by the archaeal aquaporin AqpM. Proc. Natl. Acad. Sci. USA 102 (2005) 18932-18937
41. Liu K., Kozono D., Kato Y., Agre P., and Yasui A.H.M. 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 (2005) 2192-2197
42. MacKerell Jr. A.D., Bashford D., Bellott M., Dunbrack Jr. R.L., Evanseck J., Field M.J., Fischer S., Gao J., Guo H., Ha S., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
43. Martyna G.J., Tobias D.J., and Klein M.L. Constant pressure molecular dynamics algorithms. J. Chem. Phys. 101 (1994) 4177-4189
44. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., and Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 407 (2000) 599-605
45. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kale L., and Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26 (2005) 1781-1802
46. Pohl P., Saparov S.M., Borgnia M.J., and Agre P. Highly selective water channel activity measured by voltage clamp: analysis of planar lipid bilayers reconstituted with purified AqpZ. Proc. Natl. Acad. Sci. USA 98 (2001) 9624-9629
47. Preston G.M., and Agre P. Isolation of the cDNA for erythrocyte integral membraneprotein of 28 kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. USA 88 (1991) 11110-11114
48. Preston G.M., Carroll T.P., Guggino W.B., and Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256 (1992) 385-387
49. Saparov S.M., Kozono D., Rothe U., Agre P., and Pohl P. Water and ion permeation of aquaporin-1 in planar lipid bilayers. J. Biol. Chem. 276 (2001) 31515-31520
50. Saparov S., Tsunoda S., and Pohl P. Proton exclusion by an aquaglyceroprotein: a voltage clamp study. Biol. Cell. 97 (2005) 545-550
51. Savage D.F., Egea P.F., Robles-Colmenares Y., O'Connell III J.D., and Stroud R.M. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. PLoS Biol. 1 (2003) 334-340
52. Smart O.S., Neduvelil J.G., Wang X., Wallace B.A., and Sansom M.S.P. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14 (1996) 354-360
53. Sotomayor M., and Schulten K. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87 (2004) 3050-3065
54. Sui H., Han B.-G., Lee J.K., Walian P., and Jap B.K. Structural basis of waterspecific transport through the AQP1 water channel. Nature 414 (2001) 872-878
55. Tajkhorshid E., Nollert P., Jensen M.Ø., Miercke L.J.W., O'Connell J., Stroud R.M., and Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296 (2002) 525-530
56. Tibbs G., Liu D., Leypold B., and Siegelbaum S. A state-independent interaction between ligand and a conserved arginine residue in cyclic nucleotide-gated channels reveals a functional polarity of the cyclic nucleotide binding site. Biol. Chem. 273 (1998) 4497-4505
57. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., and Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 439 (2006) 688-694
58. Tsunoda S., Wiesner B., Lorenz D., Rosenthal W., and Pohl P. Aquaporin-1, nothing but a water channel. J. Biol. Chem. 279 (2004) 11364-11367
59. Vitale N., Moss J., and Vaughan M. Molecular characterization of the GTPase-activating domain of ADP-ribosylation factor domain protein 1 (ard1). J. Biol. Chem. 273 (1998) 2553-2560
60. Wang Y., Schulten K., and Tajkhorshid E. What makes an aquaporin a glycerol channel: a comparative study of AqpZ and GlpF. Structure 13 (2005) 1107-1118
61. Yanochko G., and Yool A. Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain. J. Neurosci. 22 (2002) 2530-2540
62. Yanochko G., and Yool A. Block by extracellular divalent cations of Drosophila big brain channels expressed in Xenopus oocytes. Biophys. J. 86 (2004) 1470-1478
63. Yasui M., Hazama A., Kwon T.-H., Nielsen S., Guggino W.B., and Agre P. Rapid gating and anion permeability of an intracellular aquaporin. Nature 402 (1999) 184-187
64. Yool A., and Stamer W. Novel roles for aquaporins as gated ion channels. In: Bittar E.E., and Maue R.A. (Eds). Molecular Insights into Ion Channel Biology in Health and Disease Volume 32 (2002), Elsevier Science, Amsterdam, The Netherlands 351-379
65. Yool A.J., and Weinstein A.M. New roles for old holes: ion channel function in aquaporin-1. News Physiol. Sci. 17 (2002) 68-72
66. Yool A., Stamer W., and Regan J. Forskolin simulation of water and cation permeability in aquaporin 1 water channels. Science 273 (1996) 1216-1218
67. Yool A., Brokl O.H., Pannabecker T.L., Dantzler W.H., and Stamer W.D. 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
68. Zagotta W., and Siegelbaum S. Structure and function of cyclic nucleotide gate channels. Annu. Rev. Neurosci. 58 (1996) 619-648
69. Zagotta W., Olivier N., Black K., Young E., Olson R., and Gouaux J. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425 (2003) 200-205
70. Zeidel M.L., Nielsen S., Smith B.L., Ambudkar S.V., Maunsbach A.B., and Agre P. Ultrastructure, pharmacological inhibition, and transport selectivity of aquaporin channel-forming integral protein in proteoliposomes. Biochemistry 33 (1994) 1606-1615
71. Zhu F., Tajkhorshid E., and Schulten K. Molecular dynamics study of aquaporin-water channel in a lipid bilayer. FEBS Lett. 504 (2001) 212-218
72. Zhu F., Tajkhorshid E., and Schulten K. Theory and simulation of water permeation in aquaporin-1. Biophys. J. 86 (2004) 50-57