The structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: A member of the major facilitator superfamily

Current Opinion in Structural Biology

Volumn 14, Issue 4, 2004, Pages 405-412

  Lemieux, M Joanne ^a,b   Huang, Yafei ^a   Wang, Da Neng ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCEROPHOSPHATE; PHOSPHATE TRANSPORTER; PROTEIN DERIVATIVE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BACILLUS SUBTILIS; BACTERIAL CELL; BINDING SITE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CITRIC ACID CYCLE; CONFORMATIONAL TRANSITION; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; ESCHERICHIA COLI; GENE TRANSLOCATION; MEMBRANE BIOLOGY; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN TRANSPORT; REVIEW; RNA TRANSLATION; SEQUENCE HOMOLOGY; STREPTOCOCCUS THERMOPHILUS; 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;

ESCHERICHIA COLI;

EID: 4143072800     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.06.003     Document Type: Review

References (61)

1. P. Mitchell Molecule, group and electron translocation through the natural membranes Biochem Soc Symp 22 1963 141 168
2. I.T. Paulsen, M.K. Sliwinski, and M.H. Saier Jr. Microbial genome analyses: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities J Mol Biol 277 1998 573 592
3. 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
4. J. Reizer, K. Finley, D. Kakuda, C.L. MacLeod, A. Reizer, and M.H. Saier Jr. Mammalian integral membrane receptors are homologous to facilitators and antiporters of yeast, fungi, and eubacteria Protein Sci 2 1993 20 30
5. P.J.F. Henderson The 12-transmembrane helix transporters Curr Opin Cell Biol 5 1993 708 712
6. P.C. Maloney Bacterial transporters Curr Opin Cell Biol 6 1994 571 582
7. S.S. Pao, I.T. Paulsen, and M.H. Saier Jr. Major facilitator superfamily Microbiol Mol Biol Rev 62 1998 1 34
8. Q. Ren, K.H. Kang, and I.T. Paulsen TransportDB: a relational database of cellular membrane transport systems Nucleic Acids Res 32 2004 D284 D288
9. S. Takamori, J.S. Rhee, C. Rosenmund, and R. Jahn Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons Nature 407 2000 189 194
10. S.B. Levy Active efflux, a common mechanism for biocide and antibiotic resistance J Appl Microbiol 92 2002 65S-71S
11. M.C. Maiden, E.O. Davis, S.A. Baldwin, D.C. Moore, and P.J. Henderson Mammalian and bacterial sugar transport proteins are homologous Nature 325 1987 641 643
12. W.F. Widdas 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
13. C. Patlak Contributions to the theory of active transport: II. The gate type non-carrier mechanism and generalizations concerning tracer flow, efficiency, and measurement of energy expenditure Bull Math Biophys 19 1957 209 235
14. G.A. Vidavar Inhibition of parallel flux and augmentation of counter flux shown by transport models not involving a mobile carrier J Theor Biol 10 1966 301 306
15. I.C. West Ligand conduction and the gated-pore mechanism of transmembrane transport Biochim Biophys Acta 1331 1997 213 234
16. W.P. Jencks The utilization of binding energy in coupled vectorial processes Adv Enzymol Relat Areas Mol Biol 51 1980 75 106
17. C. Tanford Mechanism of free energy coupling in active transport Annu Rev Biochem 52 1983 379 409
18. M. Auer, M.J. Kim, M.J. Lemieux, A. Villa, J. Song, X.D. Li, and D.N. Wang High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter Biochemistry 40 2001 6628 6635
19. 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
20. 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 The 3.3 ̊ resolution structure of GlpT from E. coli reveals 12 transmembrane α helices forming N- and C-terminal domains with pseudo-twofold symmetry. Between the two domains, two arginine sidechains constitute the substrate-binding site. The transporter is in its inward-facing, unliganded conformation. In combination with biochemical experiments, the structure suggests a single binding site, alternating access mechanism with a rocker-switch type of movement.
21. 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 describes the 3.5 Å crystal structure of LacY from E. coli. The twelve transmembrane α helices of the protein form two six-helix bundles. A substrate analog bound between the bundles reveals the substrate-binding site and the residues involved. The transporter is in its inward-facing conformation. The structure provides a framework to understand the vast amounts of biochemical data available on the protein.
22. 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 The 6.5 Å resolution structure of OxlT determined by cryo-electron microscopy of two-dimensional crystals grown in the presence of substrate revealed 12 transmembrane α helices surrounding a central pore. This was the first time that the transmembrane α helices of an MFS protein were visualized, proving the 12-helix topology predicted from the protein sequence.
23. T. Hirai, J.A. Heymann, P.C. Maloney, and S. Subramaniam Structural model for 12-helix transporters belonging to the major facilitator superfamily J Bacteriol 185 2003 1712 1718
24. S. Hayashi, J.P. Koch, and Lin ECC Active transport of L-α-glycerophosphate in Escherichia coli J Biol Chem 239 1964 3098 3105
25. Rock CO, Cronan JE: Lipid metabolism in prokaryotes. In Biochemistry of Lipids and Membranes. Edited by Vance DE, Vance JE. San Francisco: Benjamin/Cummings; 1985:73-115.
26. i exchange mediated by the GlpT-dependent sn-glycerol-3-phosphate transport system in Escherichia coli J Bacteriol 161 1985 1054 1058
27. 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
28. + to adenosine 5′-triphosphate stoichiometry of Escherichia coli ATP synthase using 31P NMR Biochemistry 23 1984 3667 3675
29. K. Eiglmeier, W. Boos, and S.T. Cole Nucleotide sequence and transcriptional startpoint of the glpT gene of Escherichia coli: extensive sequence homology of the glycerol-3- phosphate transport protein with components of the hexose-6-phosphate transport system Mol Microbiol 1 1987 251 258
30. L. Bartoloni, M. Wattenhofer, J. Kudoh, A. Berry, K. Shibuya, K. Kawasaki, J. Wang, S. Asakawa, I. Talior, and B. Bonne-Tamir Cloning and characterization of a putative human glycerol 3-phosphate permease gene (SLC37A1 or G3PP) on 21q22.3: mutation analysis in two candidate phenotypes, DFNB10 and a glycerol kinase deficiency Genomics 70 2000 190 200
31. P.C. Maloney, S.V. Ambudkar, V. Anatharam, L.A. Sonna, and A. Varadhachary Anion-exchange mechanisms in bacteria Microbiol Rev 54 1990 1 17
32. L.A. Sonna, S.V. Ambudkar, and P.C. Maloney The mechanism of glucose 6-phosphate transport by Escherichia coli J Biol Chem 263 1988 6625 6630
33. M.C. 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
34. R.T. Yan, and P.C. Maloney Identification of a residue in the translocation pathway of a membrane carrier Cell 75 1993 37 44
35. R.T. Yan, and P.C. Maloney Residues in the pathway through a membrane transporter Proc Natl Acad Sci USA 92 1995 5973 5976
36. M. Matos, M.C. Fann, R.T. Yan, and P.C. Maloney Enzymatic and biochemical probes of residues external to the translocation pathway of UhpT, the sugar phosphate carrier of Escherichia coli J Biol Chem 271 1996 18571 18575
37. 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
38. Y. Liu, D.M. Engelman, and M. Gerstein Genomic analysis of membrane protein families: abundance and conserved motifs Genome Biol 3 2002 54
39. T. Skarzynski, A. Mistry, A. Wonacott, S.E. Hutchinson, V.A. Kelly, and K. Duncan Structure of UDP-N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP-N-acetylglucosamine and the drug fosfomycin Structure 4 1996 1465 1474
40. M. Sato, and M. Mueckler A conserved amino acid motif (R-X-G-R-R) in the Glut1 glucose transporter is an important determinant of membrane topology J Biol Chem 274 1999 24721 24725
41. R. Dutzler, E.B. Campbell, M. Cadene, B.T. Chait, and R. MacKinnon X-ray structure of a ClC chloride channel at 3.0 ̊ reveals the molecular basis of anion selectivity Nature 415 2002 287 294
42. A. Accardi, and C. Miller Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels Nature 427 2004 803 807
43. D.N. Wang, V.E. Sarabia, A.F. Reithmeier, and W. Kühlbrandt Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, Band 3 EMBO J 13 1994 3230 3235
44. K.A. Williams Three-dimensional structure of the ion-coupled transport protein NhaA Nature 403 2000 112 115
45. S. Murakami, R. Nakashima, E. Yamashita, and A. Yamaguchi Crystal structure of bacterial multidrug efflux transporter AcrB Nature 419 2002 587 593
46. I. Hacksell, J.L. Rigaud, P. Purhonen, T. Pourcher, H. Hebert, and G. Leblanc Projection structure at 8 ̊ resolution of the melibiose permease, an Na-sugar co-transporter from Escherichia coli EMBO J 21 2002 3569 3574
47. C. Ziegler, S. Morbach, D. Schiller, R. Kramer, C. Tziatzios, D. Schubert, and W. Kühlbrandt Projection structure and oligomeric state of the osmoregulated sodium/glycine betaine symporter BetP of Corynebacterium glutamicum J Mol Biol 337 2004 1137 1147
48. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trezeguet, G.J. Lauquin, and G. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
49. I. Ubarretxena-Belandia, J.M. Baldwin, S. Schuldiner, and C.G. Tate Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer EMBO J 22 2003 6175 6181
50. C. Ma, and G. Chang Structure of the multidrug resistance efflux transporter EmrE from Escherichia coli Proc Natl Acad Sci USA 101 2004 2852 2857
51. M. Mueckler, and C. Makepeace Analysis of transmembrane segment 8 of the GLUT1 glucose transporter by cysteine-scanning mutagenesis and substituted cysteine accessibility J Biol Chem 279 2004 10494 10499
52. + antiporter J Biol Chem 276 2001 20330 20339
53. T. Kasahara, and M. Kasahara Transmembrane segments 1, 5, 7 and 8 are required for high-affinity glucose transport by Saccharomyces cerevisiae Hxt2 transporter Biochem J 372 2003 247 252
54. Verdy E, Arkin IT, Gottschalk KE, Kaback HR, Schuldiner S: Structural conservation in the major facilitator superfamily as revealed by comparative modeling. Protein Sci 2004, in press.
55. S.G. Olsen, K.M. Greene, and R.J. Brooker Lactose permease mutants which transport (malto)-oligosaccharides J Bacteriol 175 1993 6269 6275
56. J.A. Hall, M.C. Fann, and P.C. Maloney Altered substrate selectivity in a mutant of an intrahelical salt bridge in UhpT, the sugar phosphate carrier of Escherichia coli J Biol Chem 274 1999 6148 6153
57. L.M. Veenhoff, E.H. Heuberger, and B. Poolman The lactose transport protein is a cooperative dimer with two sugar translocation pathways EMBO J 20 2001 3056 3062
58. M. Safferling, H. Griffith, J. Jin, J. Sharp, M. De Jesus, C. Ng, T.A. Krulwich, and D.N. Wang The TetL tetracycline efflux protein from Bacillus subtilis is a dimer in the membrane and in detergent solution Biochemistry 42 2003 13969 13976
59. Maloney PC, Wilson TH: Ion-coupled transport and transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology, edn 2. Edited by Neidhardt FC, Curtiss RI, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE. Washington, DC: ASM Press; 1996:1130-1148.
60. M. Kasahara, and P.C. Hinkle Reconstitution of D-glucose transport catalyzed by a protein fraction from human erythrocytes in sonicated liposomes Proc Natl Acad Sci USA 73 1976 396 400
61. DeLano WL: The PyMOL User's Manual. San Carlos, CA: DeLano Scientific; 2002.