Structural insights into the activation mechanism of melibiose permease by sodium binding

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

Volumn 107, Issue 51, 2010, Pages 22078-22083

  Granell, Meritxell ^a   León, Xavier ^a   Leblanc, Gérard ^b   Padrós, Esteve ^a   Lórenz Fonfría, Víctor A ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

Infrared spectroscopy; Ligand binding; Membrane proteins; Sugar cation symporter

Indexed keywords

ASPARTIC ACID; CATION; CYSTEINE; LIGAND; MELIBIOSE; PERMEASE; SODIUM; SODIUM ION;

ACIDITY; ARTICLE; BINDING SITE; COMPARATIVE STUDY; CONFORMATION; ENZYME BINDING; ENZYME STRUCTURE; FLUORESCENCE SPECTROSCOPY; INFRARED SPECTROSCOPY; MUTANT; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS;

ESCHERICHIA COLI; MELIBIOSE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SODIUM; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STRUCTURE-ACTIVITY RELATIONSHIP; SYMPORTERS;

ESCHERICHIA COLI;

EID: 78650649169     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1008649107     Document Type: Article

References (51)

1. Mitchell P (1972) Chemiosmotic coupling in energy transduction: a logical development of biochemical knowledge. J Bioenerg 3:5-24.
2. Jardetsky O (1966) Simple allosteric model for membrane pumps. Nature 211:969-970.
3. Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67-91.
4. Krishnamurthy H, Piscitelli CL, Gouaux E (2009) Unlocking the molecular secrets of sodium-coupled transporters. Nature 459:347-355.
5. +-symporters with inverted repeats. Curr Opin Struct Biol 19:425-432.
6. + antiporter. Trends Biochem Sci 33:435-443.
7. Law CJ, Maloney PC, Wang DN (2008) Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 62:289-305.
8. Forrest LR, Rudnick G (2009) The rocking bundle: A mechanism for ion-coupled solute flux by symmetrical transporters. Physiology 24:377-386.
9. Poolman B, et al. (1996) Cation and sugar selectivity determinants in a novel family of transport proteins. Mol Microbiol 19:911-922.
10. Tsuchiya T, Wilson DM, Wilson TH (1985) Melibiose-cation cotransport system of Escherichia coli. Ann NY Acad Sci 456:342-349. (Pubitemid 16110689)
11. + sugar symport is catalyzed by a single polypeptide. Biochemistry 34:4412-4420.
12. + symporter of Escherichia coli: Kinetic and molecular properties. Philos Trans R Soc Lond B Biol Sci 326:411-423.
13. Mus-Veteau I, Pourcher T, Leblanc G (1995) Melibiose permease of Escherichia coli Substrate-induced conformational changes monitored by tryptophan fluorescence spectroscopy. Biochemistry 34:6775-6783.
14. 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.
15. Maehrel C, Cordat E, Mus-Veteau I, Leblanc G (1998) Structural studies of the melibiose permease of Escherichia coliby fluorescence resonanceenergy transfer. I. Evidence for ion-induced conformational change. J Biol Chem 273:33192-33197.
16. +-coupled transport in site-directed mutants of the melibiose carrier of Escherichia coli. Biochim Biophys Acta 1282:240-248.
17. + concentrations. J Biol Chem 261:6893-6899.
18. 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.
19. 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.
20. 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.
21. Dave N, et al. (2000) Secondary structure components and properties of the melibiose permease from Escherichia coli: A fourier transform infrared spectroscopy analysis. Biophys J 79:747-755.
22. Gwizdek C, Leblanc G, Bassilana M (1997) Proteolytic mapping and substrate protection of the Escherichia coli melibiose permease. Biochemistry 36:8522-8529.
23. Botfield MC, Naguchi K, Tsuchiya T, Wilson TH (1992) Membrane topology of the melibiose carrier of Escherichia coli. J Biol Chem 267:1818-1822.
24. + symporters. Proc Natl Acad Sci USA 106:15291-15296.
25. Abramson J, et al. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610-615.
26. 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.
27. Hirai T, et al. (2002) Three-dimensional structure of abacterial oxalate transporter. Nat Struct Biol 9:597-600.
28. Abramson J, Kaback HR, Iwata S (2004) Structural comparis on of lactose permease and the glycerol-3-phosphate antiporter: Members of the major facilitator superfamily. Curr Opin Struct Biol 14:413-419.
29. Wilson TH, Ding PZ (2001) Sodium-substrate cotransport in bacteria. Biochim Biophys Acta 1505(1):121-130.
30. Meyer-Lipp K, et al. (2006) The inner interhelix loop 4-5 of the melibiose permease from Escherichia colitakes part in conformational changes after sugar binding. J Biol Chem 281:25882-25892.
31. 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.
32. León X, Lórenz-Fonfría VA, Lemonnier R, Leblanc G, Padrós E (2005) Substrate-induced conformational changes of melibiose permease from Escherichia coli studied by infrared difference spectroscopy. Biochemistry 44:3506-3514.
33. León X, Lemonnier R, Leblanc G, Padrós E (2006) Changes in secondary structures and acidic side chains of melibiose permease upon cosubstrates binding. Biophys J 91:4440-4449.
34. Ganea C, Pourcher T, Leblanc G, Fendler K (2001) Evidence for intraprotein charge transfer during the transport activity of the melibiose permease from Escherichia coli. Biochemistry 40:13744-13752.
35. + ions. Biochem Biophys Res Commun 178:1176-1181.
36. +-dependent transport and binding properties. J Biol Chem 268:3209-3215. (Pubitemid 23070946)
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. Wilson DM, Wilson TH (1992) Asp-51 and Asp-120 are important for the transport function of the Escherichia coli melibiose carrier. J Bacteriol 174:3083-3086.
39. León X, Leblanc G, Padrós E (2009) Alteration of sugar-induced conformational changes of the melibiose permease by mutating Arg141 in loop 4-5. Biophys J 96:4877-4886.
40. Kotting C, Gerwert K (2005) Proteins in action monitored by time-resolved FTIR spectroscopy. Chem Phys Chem 6:881-888.
41. +-coupled sugar translocation. J Biol Chem 278:1518-1524.
42. Ding PZ, Wilson TH (2001) The effect of modifications of the charged residues in the transmembrane helices on the transport activity of the melibiose carrier of Escherichia coli. Biochem Biophys Res Commun 285:348-354.
43. Matsuzaki S, Weissborn AC, Tamai E, Tsuchiya T, Wilson TH (1999) Melibiose carrier of Escherichia coin Use of cysteine mutagenesis to identify the amino acids on the hydrophilic face of transmembrane helix 2. Biochim Biophys Acta 1420:63-72.
44. Ding PZ, Wilson TH (2001) Cysteine mutagenesis of the amino acid residues of transmembrane helix I in the melibiose carrier of Escherichia coli. Biochemistry 40:5506-5510.
45. Singh SK, Piscitelli CL, Yamashita A, Gouaux E (2008) A competitive inhibitor traps LeuT in an open-to-out conformation. Science 322:1655-1661.
46. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protoc 5:725-738.
47. Dave N, Lórenz-Fonfria VA, Leblanc G, Padrós E (2008) FTIR spectroscopy of secondary- structure reorientation of melibiose permease modulated by substrate binding. Biophys J 94:3659-3670.
48. Lórenz-Fonfria VA, Granell M, León X, Leblanc G, Padrós E (2009) In-plane and out- of-plane infrared difference spectroscopy unravels tilting of helices and structural changes in a membrane protein upon substrate binding. J Am Chem Soc 131:15094-15095.
49. 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.
50. Vardy E, Arkin IT, Gottschalk KE, Kaback HR, Schuldiner S (2004) Structural conservation in the major facilitator superfamily as revealed by comparative modeling. Protein Sci 13:1832-1840.
51. Lemieux MJ (2007) Eukaryotic major facilitator superfamily transporter modeling based on the prokaryotic GlpT crystal structure. Mol Membr Biol 24:333-341.