A 3D structure model of the melibiose permease of Escherichia coli represents a distinctive fold for Na+ symporters

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 36, 2009, Pages 15291-15296

  Yousef, Mohammad S ^a,b,c   Guan, Lan ^a,b  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c CAIRO UNIVERSITY   (Egypt)

Author keywords

Bioenergetics; Ligand binding; MelB; Protein threading; Sugar cation symporter

Indexed keywords

CATION; COTRANSPORTER; LACTOSE PERMEASE; MELIBIOSE; MEMBRANE PROTEIN; PERMEASE; SODIUM ION; SUGAR;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; CHROMATOGRAPHY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; DNA TEMPLATE; ESCHERICHIA COLI; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT;

CRYSTALLIZATION; ESCHERICHIA COLI; MODELS, MOLECULAR; PROTEIN CONFORMATION; SODIUM; SYMPORTERS;

ESCHERICHIA COLI;

EID: 70349317512     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905516106     Document Type: Article

References (54)

1. Yazyu H, et al. (1984) Nucleotide sequence of the melB gene and characteristics of deduced amino acid sequence of the melibiose carrier in Escherichia coli. J Biol Chem 259:4320-4326. (Pubitemid 14127794)
2. Saier MH, Jr (2000) Families of transmembrane sugar transport proteins. Mol Microbiol 35:699-710.
3. Tokuda H, Kaback HR (1977) Sodium-dependent methyl 1-thio-β-D- galactopyranoside transport in membrane vesicles isolated from Salmonella typhimurium. Biochemistry 16:2130-2136.
4. + and methul-beta-D-thiogalactopyranoside mediated by the melibiose transport system of Escherichia coli. Biochem Biophys Res Commun 76:26-31.
5. Bassilana M, Pourcher T, Leblanc G (1987) Facilitated diffusion properties of melibiose permease in Escherichia coli membrane vesicles. Release of co-substrates is rate limiting for permease cycling. J Biol Chem 262:16865-16870.
6. Wilson DM, Wilson TH (1987) Cation specificity for sugar substrates of the melibiose carrier in Escherichia coli. Biochim Biophys Acta 904:191-200.
7. Tsuchiya T, Wilson TH (1978) Cation-sugar cotransport in the melibiose transport system of Escherichia coli. Membr Biochem 2:63-79. (Pubitemid 9063696)
8. Bassilana M, Pourcher T, Leblanc G (1988) Melibiose permease of Escherichia coli. Characteristics of co-substrates release during facilitated diffusion reactions. J Biol Chem 263:9663-9667. (Pubitemid 18193422)
9. Kaback HR, Sahin-Toth M, Weinglass AB (2001) The kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2:610-620.
10. Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67-91.
11. Pourcher T, Bibi E, Kaback HR, Leblanc G (1996) Membrane topology of the melibiose permease of Escherichia coli studied by melB-phoA fusion analysis. Biochemistry 35:4161-4168. (Pubitemid 26113474)
12. + sugar symport is catalyzed by a single polypeptide. Biochemistry 34:4412-4420.
13. Botfield MC, Naguchi K, Tsuchiya T, Wilson TH (1992) Membrane topology of the melibiose carrier of Escherichia coli. J Biol Chem 267:1818-1822.
14. Gwizdek C, Leblanc G, Bassilana M (1997) Proteolytic mapping and substrate protection of the Escherichia coli melibiose permease. Biochemistry 36:8522-8529. (Pubitemid 27305135)
15. Hacksell I, et al. (2002) Projection structure at 8 Å resolution of the melibiose permease, an Na-sugar co-transporter from Escherichia coli. EMBO J 21:3569-3574. (Pubitemid 34787030)
16. Purhonen P, Lundback AK, Lemonnier R, Leblanc G, Hebert H (2005) Three-dimensional structure of the sugar symporter melibiose permease from cryo-electron microscopy. J Struct Biol 152:76-83. (Pubitemid 41384179)
17. Guan L, Mirza O, Verner G, Iwata S, Kaback HR (2007) Structural determination of wild-type lactose permease. Proc Natl Acad Sci USA 104:15294-15298. (Pubitemid 47502911)
18. Abramson J, et al. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610-615. (Pubitemid 36927939)
19. + symport in LacY. EMBO J 25:1177-1183.
20. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:616-620. (Pubitemid 36927940)
21. Yin Y, He X, Szewczyk P, Nguyen T, Chang G (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741-744.
22. Shi J, Blundell TL, Mizuguchi K (2001) FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310:243-257. (Pubitemid 32619966)
23. Teodorescu O, Galor T, Pillardy J, Elber R (2004) Enriching the sequence substitution matrix by structural information. Proteins 54:41-48.
24. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat Protoc 4:363-371.
25. von Heijne G (1989) Control of topology and mode of assembly of a polytopic membrane protein by positively charged residue. Nature 341:456-458.
26. +-coupled sugar translocation. J Biol Chem 278:1518-1524.
27. Meyer-Lipp K, et al. (2006) The inner interhelix loop 4-5 of the melibiose permease from Escherichia coli takes part in conformational changes after sugar binding. J Biol Chem 281:25882-25892. (Pubitemid 44401794)
28. Ding PZ (2004) Loop X/XI, the largest cytoplasmic loop in the membrane-bound melibiose carrier of Escherichia coli, is a functional re-entrant loop. Biochim Biophys Acta 1660:106-117.
29. Kaback HR (2005) Structure and mechanism of the lactose permease. C R Biol 328:557-567.
30. Smirnova I, et al. (2007) Sugar binding induces an outward facing conformation of LacY. Proc Natl Acad Sci USA 104:16504-16509. (Pubitemid 350211048)
31. Kaback HR, et al. (2007) Site-directed alkylation and the alternating access model for LacY. Proc Natl Acad Sci USA 104:491-494. (Pubitemid 46123053)
32. Matsuzaki S, Weissborn AC, Tamai E, Tsuchiya T, Wilson TH (1999) Melibiose carrier of Escherichia coli: Use of cysteine mutagenesis to identify the amino acids on the hydrophilic face of transmembrane helix 2. Biochim Biophys Acta 1420:63-72.
33. Pourcher T, Deckert M, Bassilana M, Leblanc G (1991) Melibiose permease of Escherichia coli: Mutation of aspartic acid 55 in putative helix II abolishes activation of sugar binding by Na+ ions. Biochem Biophys Res Commun 178:1176-1181.
34. Hama H, Wilson TH (1994) Replacement of alanine 58 by asparagine enables the melibiose carrier of Klebsiella pneumoniae to couple sugar transport to Na+. J Biol Chem 269:1063-1067. (Pubitemid 24981980)
35. Pourcher T, Zani ML, Leblanc G (1993) Mutagenesis of acidic residues in putative membrane-spanning segments of the melibiose permease of Escherichia coli. I. Effect on Na(+)-dependent transport and binding properties. J Biol Chem 268:3209-3215. (Pubitemid 23070946)
36. Zani ML, Pourcher T, Leblanc G (1994) Mutation of polar and charged residues in the hydrophobic NH2-terminal domains of the melibiose permease of Escherichia coli. J Biol Chem 269:24883-24889.
37. Zani ML, Pourcher T, Leblanc G (1993) Mutagenesis of acidic residues in putative membrane-spanning segments of the melibiose permease of Escherichia coli. II. Effect on cationic selectivity and coupling properties. J Biol Chem 268:3216-3221. (Pubitemid 23070947)
38. Leon X, Lemonnier R, Leblanc G, Padros E (2006) Changes in secondary structures and acidic side chains of melibiose permease upon cosubstrates binding. Biophys J 91:4440-4449. (Pubitemid 44904230)
39. Cordat E, Leblanc G, Mus-Veteau I (2000) Evidence for a role of helix IV in connecting cation- and sugar-binding sites of Escherichia coli melibiose permease. Biochemistry 39:4493-4499. (Pubitemid 30212665)
40. --dependent neurotransmitter transporters. Nature 437:215-223.
41. +/sugar symport. Science 321:810-814.
42. Weyand S, et al. (2008) Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322:709-713.
43. Boudker O, Ryan RM, Yernool D, Shimamoto K, Gouaux E (2007) Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445:387-393. (Pubitemid 46160902)
44. Franco PJ, Wilson TH (1999) Arg-52 in the melibiose carrier of Escherichia coli is important for cation-coupled sugar transport and participates in an intrahelical salt bridge. J Bacteriol 181:6377-6386. (Pubitemid 29512948)
45. Franco PJ, Jena AB, Wilson TH (2001) Physiological evidence for an interaction between helices II and XI in the melibiose carrier of Escherichia coli. Biochim Biophys Acta 1510:231-242.
46. Guan L, Hu Y, Kaback HR (2003) Aromatic stacking in the sugar binding site of the lactose permease. Biochemistry 42:1377-1382. (Pubitemid 36205943)
47. Kasho VN, Smirnova IN, Kaback HR (2006) Sequence alignment and homology threading reveals prokaryotic and eukaryotic proteins similar to lactose permease. J Mol Biol 358:1060-1070.
48. Ambroise Y, Leblanc G, Rousseau B (2000) Active-site-directed photolabeling of the melibiose permease of Escherichia coli. Biochemistry 39:1338-1345. (Pubitemid 30090702)
49. Mus-Veteau I, Leblanc G (1996) Melibiose permease of Escherichia coli: Structural organization of cosubstrate binding sites as deduced from tryptophan fluorescence analyses. Biochemistry 35:12053-12060. (Pubitemid 26313676)
50. Meyer-Lipp K, Ganea C, Pourcher T, Leblanc G, Fendler K (2004) Sugar binding induced charge translocation in the melibiose permease from Escherichia coli. Biochemistry 43:12606-12613. (Pubitemid 39314722)
51. + antiporter and insights into mechanism of action and regulation by pH. Nature 435:1197-1202.
52. Collaborative Computational Project N (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D 50:760-763.
53. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037-10041. (Pubitemid 32802969)
54. Landau M, et al. (2005) ConSurf 2005: The projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33:W299-W302. (Pubitemid 44529930)