Glycerol facilitator GlpF and the associated aquaporin family of channels

Current Opinion in Structural Biology

Volumn 13, Issue 4, 2003, Pages 424-431

  Stroud, Robert M ^a   Miercke, Larry J W ^a   O'Connell, Joseph ^a   Khademi, Shahram ^a   Lee, John K ^a   Remis, Jonathan ^a   Harries, William ^a   Robles, Yaneth ^a   Akhavan, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDITOL; AQUAPORIN; CARBONYL DERIVATIVE; GLYCEROL;

CELL MEMBRANE; CELL MEMBRANE CONDUCTANCE; ELECTROCHEMISTRY; ENANTIOSELECTIVITY; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR RECOGNITION; MOLECULE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; SIMULATION; STEREOCHEMISTRY; SURFACE PROPERTY;

EID: 0042430573     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00114-3     Document Type: Review

References (34)

1. Fischer A: Vorlesungen uber Bakterien. Jena; 1903.
2. Heller K.B., Lin E.C., Wilson T.H. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol. 144:1980;274-278.
3. Fu D., Libson A., Miercke L.J., Weitzman C., Nollert P., Krucinski J., Stroud R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science. 290:2000;481-486 The 2.2 Å resolution crystal structure of GlpF, the first for an aquaporin, explains the preferential permeability of linear carbohydrates and the exclusion of charged solutes by the channel.
4. Nollert P., Harries W.E., Fu D., Miercke L.J., Stroud R.M. Atomic structure of a glycerol channel and implications for substrate permeation in aqua(glycero)porins. FEBS Lett. 504:2001;112-117 Analysis of the structure of GlpF suggests the basis of the polarization of water during passage through the channel. The unusual geometry of amino acid mainchains leads to the presentation of two sets of four successive carbonyls to the lumen of the channel.
5. Moon C., Preston G.M., Griffin C.A., Jabs E.W., Agre P. The human aquaporin-CHIP gene. Structure, organization, and chromosomal localization. J Biol Chem. 268:1993;15772-15778.
6. Preston G.M., Agre P. 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.
7. Agre P, Preston GM, Smith BL, Jung JS: Raina Sea 1993.
8. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 256:1992;385-387.
9. Maurel C., Reizer J., Schroeder J.I., Chrispeels M.J., Saier M.H. Jr. Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J Biol Chem. 269:1994;11869-11872.
10. Park J.H., Saier M.H. Jr. Phylogenetic characterization of the MIP family of transmembrane channel proteins. J Membr Biol. 153:1996;171-180.
11. Pao G.M., Wu L.F., Johnson K.D., Hofte H., Chrispeels M.J., Sweet G., Sandal N.N., Saier M.H. Jr. Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol. 5:1991;33-37.
12. Wistow G.J., Pisano M.M., Chepelinsky A.B. Tandem sequence repeats in transmembrane channel proteins. Trends Biochem Sci. 16:1991;170-171.
13. Verkman A.S., Shi L.B., Frigeri A., Hasegawa H., Farinas J., Mitra A., Skach W., Brown D., Van Hoek A.N., Ma T. Structure and function of kidney water channels. Kidney Int. 48:1995;1069-1081.
14. Heymann J.B., Engel A. Structural clues in the sequences of the aquaporins. J Mol Biol. 295:2000;1039-1053 Sequence alignments elucidate the genetic heritage of the AQP family. Gene duplication is evident, and the alignment reveals conservation of six conserved transmembrane helices and two functional loops. Bacterial glycerol and water channels indicate divergence of these traits in bacteria.
15. Mitsuoka K., Murata K., Walz T., Hirai T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. The structure of aquaporin-1 at 4.5-Å resolution reveals short alpha-helices in the center of the monomer. J Struct Biol. 128:1999;34-43.
16. Sui H., Han B.G., Lee J.K., Walian P., Jap B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature. 414:2001;872-878 The 2.2 Å X-ray structure of bovine AQP1 illustrates details of the water-specific selectivity of the channel.
17. Tajkhorshid E., Nollert P., Jensen M.O., Miercke L.J., O'Connell J., Stroud R.M., Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science. 296:2002;525-530 A 12 ns molecular dynamics simulation shows the temporal probability distribution and orientation, as well as the hydrogen-bond dynamic arrangement, of seven to nine water molecules as they pass through the GlpF channel. The simulation demonstrates remarkable robustness and reproduces observed conductances well.
18. r 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem. 266:1991;6407-6415.
19. Cheng A., van Hoek A.N., Yeager M., Verkman A.S., Mitra A.K. Three-dimensional organization of a human water channel. Nature. 387:1997;627-630.
20. Li H., Lee S., Jap B.K. Molecular design of aquaporin-1 water channel as revealed by electron crystallography. Nat Struct Biol. 4:1997;263-265.
21. Hasler L., Walz T., Tittmann P., Gross H., Kistler J., Engel A. Purified lens major intrinsic protein (MIP) forms highly ordered tetragonal two-dimensional arrays by reconstitution. J Mol Biol. 279:1998;855-864.
22. Ringler P., Borgnia M.J., Stahlberg H., Maloney P.C., Agre P., Engel A. Structure of the water channel AqpZ from Escherichia coli revealed by electron crystallography. J Mol Biol. 291:1999;1181-1190.
23. Walz T., Hirai T., Murata K., Heymann J.B., Mitsuoka K., Fujiyoshi Y., Smith B.L., Agre P., Engel A. The three-dimensional structure of aquaporin-1. Nature. 387:1997;624-627.
24. Mitra A.K., Ren G., Reddy V.S., Cheng A., Froger A. The architecture of a water-selective pore in the lipid bilayer visualized by electron crystallography in vitreous ice. Novartis Found Symp. 245:2002;33-46 AQP1 is visualized by electron microscopy as it is inserted into a native lipid-like environment.
25. Jensen M.O., Park S., Tajkhorshid E., Schulten K. Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc Natl Acad Sci USA. 99:2002;6731-6736 Molecular dynamics simulation of glycerol passage through the GlpF channel reveals the location of potential barriers through the channel and reproduces the observed conductance well.
26. Borgnia M., Nielsen S., Engel A., Agre P. Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem. 68:1999;425-458.
27. Borgnia M.J., Kozono D., Calamita G., Maloney P.C., Agre P. Functional reconstitution and characterization of AqpZ, the E. coli water channel protein. J Mol Biol. 291:1999;1169-1179.
28. Borgnia M.J., Agre P. Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc Natl Acad Sci USA. 98:2001;2888-2893 Determination of the rates of conductance of glycerol and water through GlpF and AQPZ is reported. Although both AQPZ and GlpF have similar primary amino acid sequences, including the NPA motifs, differences in the quaternary structure explain differences in their selectivity for water.
29. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature. 407:2000;599-605 The selectivity filter of GlpF is similar to that of AQP1 in that the constriction of both pores prevents the passage of ions, protons and charged solutes, but permits water passage. NPA regions in both are important in forming the surface of the aqueous pore in this regard. The mechanisms for passing water through the channel in both GlpF and AQP1 are also similar in that breakage of hydrogen bonds is involved (NPA regions are critical in this process). In GlpF, water molecules form a single-file line, becoming hydrogen-bond donors to carbonyls, with the exception of the central water molecule, which becomes a hydrogen-bond acceptor from NPA region asparagines. Another important effect of this is that interruption of these hydrogen bonds prevents proton conductance.
30. de Groot B.L., Grubmuller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 294:2001;2353-2357 Water permeation in GlpF and AQP1 occurs through a two-stage filter: the NPA region conserved selectivity-determining region and the aromatic/arginine filter, which is proposed to act as a proton filter. Also, hydrophobic regions near the NPA region are rate-limiting water barriers. The fine-tuned water dipole rotation in AQP1 during water passage is similar to how helix dipoles orient water molecules at the center of GlpF. Although GlpF contains a wider pore than AQP1, its water permeation is lower than AQP1.
31. De Grotthuss C.J.T. Sur la décomposition de l'eau et des corps qu'elle tient en dissolution á l'aide de l'électricité galvanique. Ann Chim. LVIII:1806;54-74.
32. Fu D., Libson A., Stroud R. The structure of GlpF, a glycerol conducting channel. Novartis Found Symp. 245:2002;51-61.
33. Lagree V., Froger A., Deschamps S., Hubert J.F., Delamarche C., Bonnec G., Thomas D., Gouranton J., Pellerin I. Switch from an aquaporin to a glycerol channel by two amino acids substitution. J Biol Chem. 274:1999;6817-6819.
34. Deen P.M., Croes H., van Aubel R.A., Ginsel L.A., van Os C.H. Water channels encoded by mutant aquaporin-2 genes in nephrogenic diabetes insipidus are impaired in their cellular routing. J Clin Invest. 95:1995;2291-2296.