The structure of the aquaporin-1 water channel: A comparison between cryo-electron microscopy and X-ray crystallography

Journal of Molecular Biology

Volumn 325, Issue 3, 2003, Pages 485-493

  De Groot, Bert L ^a   Engel, Andreas ^b   Grubmüller, Helmut ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Cryo electron microscopy; GlpF; Structure refinement; Water channel; X ray crystallography

Indexed keywords

AQUAPORIN 1;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DATA BASE; HUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); BOVINAE;

EID: 0037227425     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01233-0     Document Type: Article

References (44)

1. Agre, P., Bonhivers, M. & Borgnia, M. J. (1998). The Aquaporins, blueprints for cellular plumbing systems. J. Biol. Chem. 273, 14659-14662.
2. Borgnia, M., Nielsen, S., Engel, A. & Agre, P. (1999). Cellular and molecular biology of the Aquaporin water channels. Annu. Rev. Biochem. 68, 425-458.
3. Engel, A. & Stahlberg, H. (2002). Aquaglyceroporins: Channel proteins with a conserved core, multiple functions and variable surfaces. Int. Rev. Cytol. 215, 75-104.
4. Deen, P. M. T. & van Os, C. H. (1998). Epithelial Aquaporins. Curr. Opin. Cell. Biol. 10, 435-442.
5. Li, J. & Verkman, A. S. (2001). Impaired hearing in mice lacking Aquaporin-4 water channels. J. Biol. Chem. 276, 31233-31237.
6. Preston, G. M., Carroll, T. P., Guggino, W. B. & Agre, P. (1992). Appearance of water channels in Xenopus oocytes expressing red-cell CHIP28 protein. Science, 256, 385-387.
7. Reizer, J., Reizer, A. & Saier, M. H. (1993). The MIP family of integral membrane channel proteins - Sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional-differentiation of the 2 repeated halves of the proteins. Crit. Rev. Biochem. Mol. Biol. 28, 235-257.
8. Park, J. H. & Saier, M. H. (1996). Phylogenetic characterization of the MIP family of transmembrane channel proteins. J. Membr. Biol. 153, 171-180.
9. Froger, A., Tallur, B., Thomas, D. & Delamarche, C. (1998). Prediction of functional residues in water channels and related proteins. Protein Sci. 7, 1458-1468.
10. Heymann, J. B. & Engel, A. (1999). Aquaporins: Phylogeny, structure, and physiology of water channels. News Physiol. Sci. 14, 187-193.
11. Heymann, J. B. & Engel, A. (2000). Structural clues in the sequences of the Aquaporins. J. Mol. Biol. 295, 1039-1053.
12. Heller, K. B., Lin, E. C. & Wilson, T. H. (1980). Substrate-specificity and transport-properties of the glycerol facilitator of Eschericia coli. J. Bacteriol. 144, 274-278.
13. Maurel, C., Reizer, J., Schroeder, J. I., Chrispeels, M. J. & Saier, M. H. (1994). Functional characterization of the Eschericia coli glycerol facilitator GlpF, in Xenopus oocytes. J. Biol. Chem. 269, 11869-11872.
14. Zeidel, M. L., Ambudkar, S. V., Smith, B. L. & Agre, P. (1992). Reconstitution of functional water channels in liposomes containing purified red-cell CHIP28 protein. Biochemistry, 31, 7436-7440.
15. Van Hoek, A. N. & Verkman, A. S. (1992). Functional reconstitution of the isolated erythrocyte water channel CHIP28. J. Biol. Chem. 267, 18267-18269.
16. Zeidel, M. L., Nielsen, S., Smith, B. L., Ambudkar, S. V., Maunsbach, A. B. & Agre, P. (1994). Ultra-structure, pharmacological inhibition, and transport selectivity of Aquaporin channel-forming integral protein in proteoliposomes. Biochemistry, 33, 1606-1615.
17. Fu, D., Libson, A., Miercke, L. J., Weitzman, C., Nollert, P., Krucinski, J. & Stroud, R. M. (2000). Structure of a glycerol-conducting channel and the basis for its selectivity. Science, 290, 481-486.
18. Borgnia, M. J. & Agre, P. (2001). Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Eschericia coli. Proc. Natl. Acad. Sci. USA, 98, 2888-2893.
19. Smith, B. L. & Agre, P. (1991). Erythrocyte Mr-28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J. Biol. Chem. 266, 6407-6415.
20. Verbavatz, J. M., Brown, D., Sabolic, I., Valenti, G., Siello, D. A., Van Hoek, A. N. et al. (1993). Tetrameric assembly of CHIP28 water channels in liposomes and cell-membranes - A freeze-fracture study. J. Cell Biol. 123, 605-618.
21. Jung, J. S., Preston, G. M., Smith, B. L., Guggino, W. B. & Agre, P. (1994). Molecular structure of the water channel through Aquaporin CHIP - The hourglass model. J. Biol. Chem. 269, 14648-14654.
22. Braun, T., Philippsen, A., Wirtz, S., Borgnia, M. J., Agre, P., Kühlbrandt, W. et al. (2000). The 3.7 Ångstrom projection map of the glycerol facilitator GlpF: A variant of the Aquaporin tetramer. EMBO Rep. 1, 183-189.
23. Walz, T., Hirai, T., Murata, K., Heymann, J. B., Mitsuoka, K., Fujiyoshi, Y. et al. (1997). The three-dimensional structure of Aquaporin-1. Nature, 387, 624-627.
24. Cheng, A. C., Van Hoek, A. N., Yeager, M., Verkman, A. S. & Mitra, A. K. (1997). Three-dimensional organization of a human water channel. Nature, 387, 627-630.
25. Li, H. L., Lee, S. & Jap, B. K. (1997). Molecular design of Aquaporin-1 water channel as revealed by electron crystallography. Nature Struct. Biol. 4, 263-265.
26. Mitsuoka, K., Murata, K., Walz, T., Hirai, T., Agre, P., Heymann, J. B. et al. (1999). The structure of Aquaporin-1 at 4.5 Å resolution reveals short α-helices in the center of the monomer. J. Struct. Biol. 128, 34-43.
27. de Groot, B. L., Heymann, J. B., Engel, A., Mitsuoka, K., Fujiyoshi, Y. & Grubmüller, H. (2000). The fold of human Aquaporin 1. J. Mol. Biol. 300, 987-994.
28. Ren, G., Cheng, A., Reddy, V., Melnyk, P. & Mitra, A. K. (2000). Three-dimensional fold of the human AQP1 water channel determined at 4 Ångstrom resolution by electron crystallography of two-dimensional crystals embedded in ice. J. Mol. Biol. 301, 369-387.
29. Murata, K., Mitsuoka, K., Walz, T., Agre, P., Heymann, J., Engel, A. & Fujiyoshi, Y. (2000). Structural determinants of water permeation through Aquaporin-1. Nature, 407, 509-605.
30. 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.
31. Zhu, F., Tajkhorshid, E. & Schulten, K. (2001). Molecular dynamics study of aquaporin-1 water channel in a lipid bilayer. FEBS Letters, 504, 212-218.
32. Kong, Y. & Ma, J. (2001). Dynamic mechanisms of the membrane water channel aquaporin-1 (AQP1). Proc. Natl. Acad. Sci. USA, 98, 14345-14349.
33. de Groot, B. L., Engel, A. & Grubmüller, H. (2001). A refined structure of human Aquaporin-1. FEBS Letters, 504, 206-211.
34. de Groot, B. L. & Grubmüller, H. (2001). Water permeation across biological membranes: Mechanism and dynamics of Aquaporin-1 and GlpF. Science, 294, 2353-2357.
35. Sui, H., Han, B.-G., Lee, J. K., Walian, P. & Jap, B. K. (2001). Structural basis of water-specific transport through the AQP1 water channel. Nature, 414, 872-878.
36. Hooft, R. W. W., Vriend, G., Sander, C. & Abola, E. E. (1996). Errors in protein structures. Nature, 381, 272.
37. Preston, G. M., Jung, J. S., Guggino, W. B. & Agre, P. (1993). The mercury-sensitive residue at cysteine-189 in the CHIP28 water channel. J. Biol. Chem. 268, 17-20.
38. Vriend, G. (1990). WHAT IF: A molecular modeling and drug design program. J. Mol. Graphics, 8, 52-56.
39. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W. et al. (1998). Crystallography and NMR system (cns): A new software system for macromolecular structure determination. Acta Crystallog. Sect. D, 54, 905-921.
40. Lindahl, E. & Van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. J. Mol. Modell. 7, 306-317.
41. Kraulis, P. J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
42. Esnouf, R. M. (1997). An extensively modified version of MOLSCRIPT that includes greatly enhanced coloring capabilities. J. Mol. Graphics Model. 15, 132-134.
43. Merritt, E. A. & Bacon, D. J. (1997). Raster3D: Photo-realistic molecular graphics. Methods Enzymol. 277, 505-524.
44. Smart, O. S., Neduvelil, J. G., Wang, X., Wallace, B. A. & Sansom, M. S. P. (1996). HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graphics, 14, 354-360.