Structural comparison of lactose permease and the glycerol-3-phosphate antiporter: Members of the major facilitator superfamily

Current Opinion in Structural Biology

Volumn 14, Issue 4, 2004, Pages 413-419

  Abramson, Jeff ^a   Kaback, H Ronald ^b   Iwata, So ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCEROPHOSPHATE; LACTOSE PERMEASE; MEMBRANE PROTEIN; PHOSPHATE TRANSPORTER; PROTEIN DERIVATIVE;

AMINO TERMINAL SEQUENCE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; ESCHERICHIA COLI; GENE TRANSLOCATION; HYDROGEN BOND; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MONOSACCHARIDE TRANSPORT PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; SYMPORTERS;

EID: 4143061717     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.07.005     Document Type: Review

References (36)

1. I.T. Paulsen, L. Nguyen, M.K. Sliwinski, R. Rabus, and M.H. Saier Jr. Microbial genome analyses: comparative transport capabilities in eighteen prokaryotes J Mol Biol 301 2000 75 100
2. International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome Nature 409 2001 860 921
3. J.C. Venter, M.D. Adams, E.W. Myers, P.W. Li, R.J. Mural, G.G. Sutton, H.O. Smith, M. Yandell, C.A. Evans, and R.A. Holt The sequence of the human genome Science 291 2001 1304 1351
4. M.H. Saier Jr. Families of transmembrane transporters selective for amino acids and their derivatives Microbiology 146 2000 1775 1795
5. M.H. Saier Jr. A functional-phylogenetic classification system for transmembrane solute transporters Microbiol Mol Biol Rev 64 2000 354 411
6. Widdas WF Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer J Physiol 118 1952 23 39
7. I.C. West Ligand conduction and the gated-pore mechanism of transmembrane transport Biochim Biophys Acta 1331 1997 213 234
8. Heymann JAW, R. Sarker, T. Hirai, D. Shi, J.L.S. Milne, P.C. Maloney, and S. Subramaniam Projection structure and molecular architecture of OxlT, a bacterial membrane transporter EMBO J 20 2001 4408 4413
9. T. Hirai, J.A. Heymann, D. Shi, R. Sarker, P.C. Maloney, and S. Subramaniam Three-dimensional structure of a bacterial oxalate transporter Nat Struct Biol 9 2002 597 600 This paper presents the three-dimensional structure of OxlT at 6.5 Å derived from an electron crystallographic analysis of two-dimensional crystals. This is the first three-dimensional structure of an MFS transporter. The structure reveals that the 12 helices are symmetrically arranged around a central hydrophilic cavity.
10. J. Abramson, I. Smirnova, V. Kasho, G. Verner, H.R. Kaback, and S. Iwata Structure and mechanism of the lactose permease of Escherichia coli Science 301 2003 610 615 This paper reports the crystal structure at 3.5 Å of E. coli LacY. The N- and C-terminal domains of the molecule, each with six transmembrane helices, are symmetrically positioned. A large hydrophilic cavity open to the cytoplasmic side represents the inward-facing conformation of the transporter. The structure with a bound lactose homologue reveals the residues that play major roles in substrate recognition and proton translocation.
11. Y. Huang, M.J. Lemieux, J. Song, M. Auer, and D.N. Wang Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli Science 301 2003 616 620 This paper reports the 3.3 Å resolution structure of GlpT from E. coli. The N- and C-terminal halves of the protein exhibit pseudo-twofold symmetry. Closed off to the periplasm, a centrally located substrate translocation pore contains two arginines at its closed end, which comprise the possible substrate-binding site.
12. H.R. Kaback, M. Sahin-Tóth, and A.B. Weinglass The kamikaze approach to membrane transport Nat Rev Mol Cell Biol 2 2001 610 622
13. P.L. Sorgen, Y. Hu, L. Guan, H.R. Kaback, and M.E. Girvin An approach to membrane protein structure without crystals Proc Natl Acad Sci USA 99 2002 14037 14040 This paper presents a three-dimensional structural model of LacY from E. coli, calculated based on various restraints, including measured distances from cross-linking experiments.
14. S. Hayashi, J.P. Koch, and E.C. Lin Active transport of L-alpha-glycerophosphate in Escherichia coli J Biol Chem 239 1964 3098 3105
15. S.V. Ambudkar, T.J. Larson, and P.C. Maloney Reconstitution of sugar phosphate transport systems of Escherichia coli J Biol Chem 261 1986 9083 9086
16. H.R. Kaback, and J. Wu The lactose permease of Escherichia coli: what to do while awaiting crystals of a membrane transport protein Acc Chem Res 32 1999 805 813
17. I.N. Smirnova, and H.R. Kaback A mutation in the lactose permease of Escherichia coli that decreases conformational flexibility and increases protein stability Biochemistry 42 2003 3025 3031 LacY with a Cys154Gly mutation binds substrate with high affinity, but catalyses little transport. The purified mutant protein exhibits much greater thermal stability than the wild type and little tendency to aggregate. The Cys154Gly mutation also significantly increased the expression level of an unstable mutant of LacY. The authors concluded that the Cys154Gly mutation causes a more compact structure and decreased conformational flexibility.
18. M.J. Lemieux, J. Song, M.J. Kim, Y. Huang, A. Villa, M. Auer, X.D. Li, and D.N. Wang Three-dimensional crystallization of the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily Protein Sci 12 2003 2748 2756 This paper reports the successful three-dimensional crystallisation of GlpT, the glycerol-3-phosphate transporter from E. coli inner membrane. Limited proteolysis and crystallisation using a detergent mixture significantly improve the quality of the crystals.
19. G. Chang, R.H. Spencer, A.T. Lee, M.T. Barclay, and D.C. Rees Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel Science 282 1998 2220 2226
20. D.A. Doyle, J. Morais Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon The structure of the potassium channel: molecular basis of K+ conduction and selectivity Science 280 1998 69 77
21. G. Chang, and C.B. Roth Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters Science 293 2001 1793 1800
22. P.J. Henderson Proton-linked sugar transport systems in bacteria J Bioenerg Biomembr 22 1990 525 569
23. L. Guan, F.D. Murphy, and H.R. Kaback Surface-exposed positions in the transmembrane helices of the lactose permease of Escherichia coli determined by intermolecular thiol cross-linking Proc Natl Acad Sci USA 99 2002 3475 3480
24. N. Ermolova, L. Guan, and H.R. Kaback Intermolecular thiol cross-linking via loops in the lactose permease of Escherichia coli Proc Natl Acad Sci USA 100 2003 10187 10192
25. K.R. MacKenzie, and D.M. Engelman Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A dimerization Proc Natl Acad Sci USA 95 1998 3583 3590
26. J. le Coutre, L.R. Narasimhan, C.K. Patel, and H.R. Kaback The lipid bilayer determines helical tilt angle and function in lactose permease of Escherichia coli Proc Natl Acad Sci USA 94 1997 10167 10171
27. E.A. Merritt, S. Sarfaty, I.K. Feil, and W.G. Hol Structural foundation for the design of receptor antagonists targeting Escherichia coli heat-labile enterotoxin Structure 5 1997 1485 1499
28. D.D. Mitchell, J.C. Pickens, K. Korotkov, E. Fan, and W.G. Hol 3,5-substituted phenyl galactosides as leads in designing effective cholera toxin antagonists; synthesis and crystallographic studies Bioorg Med Chem 12 2004 907 920
29. M.L. Ujwal, M. Sahin-Tóth, B. Persson, and H.R. Kaback Role of glutamate-269 in the lactose permease of Escherichia coli Mol Membr Biol 11 1994 9 16
30. P.J. Franco, and R.J. Brooker Functional roles of Glu-269 and Glu-325 within the lactose permease of Escherichia coli J Biol Chem 269 1994 7379 7386
31. A.B. Weinglass, M. Sondej, and H.R. Kaback Manipulating conformational equilibria in the lactose permease of Escherichia coli J Mol Biol 315 2002 561 571
32. M. Sahin-Tóth, K.M. Akhoon, J. Runner, and H.R. Kaback Ligand recognition by the lactose permease of Escherichia coli: specificity and affinity are defined by distinct structural elements of galactopyranosides Biochemistry 39 2000 5097 5103
33. M. Sahin-Tóth, M.C. Lawrence, T. Nishio, and H.R. Kaback The C-4 hydroxyl group of galactopyranosides is the major determinant for ligand recognition by the lactose permease of Escherichia coli Biochemistry 40 2001 13015 13019
34. J.F. Riordan Arginyl residues and anion binding sites in proteins Mol Cell Biochem 26 1979 71 92
35. M.C. Fann, and P.C. Maloney Functional symmetry of UhpT, the sugar phosphate transporter of Escherichia coli J Biol Chem 273 1998 33735 33740
36. M. Fann, A.H. Davies, A. Varadhachary, T. Kuroda, C. Sevier, T. Tsuchiya, and P.C. Maloney Identification of two essential arginine residues in UhpT, the sugar phosphate antiporter of Escherichia coli J Membr Biol 164 1998 187 195