Trapping open and closed forms of FitE - A group III periplasmic binding protein

Proteins: Structure, Function and Bioinformatics

Volumn 75, Issue 3, 2009, Pages 598-609

  Shi, Rong ^a   Proteau, Ariane ^a   Wagner, John ^b   Cui, Qizhi ^b   Purisima, Enrico O ^b   Matte, Allan ^b   Cygler, Miroslaw ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Class III PBP; Crystal structure; Interdomain flexibility; Iron transport; Periplasmic binding protein

Indexed keywords

DIMER; PERIPLASMIC BINDING PROTEIN; PERIPLASMIC BINDING PROTEIN FITE; SIDEROPHORE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIMERIZATION; ESCHERICHIA COLI; IRON TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; PERIPLASMIC BINDING PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

BACTERIA (MICROORGANISMS); DIONAEA;

EID: 66149116873     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22272     Document Type: Article

References (75)

1. Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 2007;71:413-451. (Pubitemid 47429279)
2. Faraldo-Gomez JD, Sansom MS. Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 2003;4:105-116. (Pubitemid 36172694)
3. Postle K, Larsen RA. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 2007;20:453-465. (Pubitemid 46776585)
4. Braun V, Braun M. Active transport of iron and siderophore antibiotics. Curr Opin Microbiol 2002;5:194-201. (Pubitemid 34289928)
5. Andrews SC, Robinson AK, Rodriguez-Quinones F. Bacterial iron homeostasis. FEMS Microbiol Rev 2003;27:215-237. (Pubitemid 36694657)
6. Ouyang Z, Isaacson R. Identification and characterization of a novel ABC iron transport system, fit, in Escherichia coli. Infect Immun 2006;74:6949-6956.
7. Boos W, Lucht JM. Periplasmic binding protein-dependent ABC transporters. In: Neidhardt FC, editor. Escherichia coli and Salmonella. Washington, DC: ASM Press; 1996. 1209 p
8. Dwyer MA, Hellinga HW. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr Opin Struct Biol 2004;14:495-504. (Pubitemid 39094355)
9. Hsiao CD, Sun YJ, Rose J, Wang BC. The crystal structure of glutamine- binding protein from Escherichia coli. J Mol Biol 1996;262:225-242. (Pubitemid 26326973)
10. Quiocho FA, Ledvina PS. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol Microbiol 1996;20:17-25. (Pubitemid 26126045)
11. Richarme G, Caldas TD. Chaperone properties of the bacterial periplasmic substrate-binding proteins. J Biol Chem1997;272:15607-15612. (Pubitemid 27265528)
12. Felder CB, Graul RC, Lee AY, Merkle HP, Sadee W. The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAPS PharmSci 1999;1:E2.
13. Conklin BR, Bourne HR. Homeostatic signals. Marriage of the flytrap and the serpent. Nature 1994;367:22.
14. Mao B, Pear MR, McCammon JA, Quiocho FA. Hinge-bending in L-arabinose-binding protein. The "Venus's-flytrap" model. J Biol Chem 1982;257:1131-1133.
15. Sack JS, Saper MA, Quiocho FA. Periplasmic binding protein structure and function. Refined X-ray structures of the leucine/isoleucine/ valine-binding protein and its complex with leucine. J Mol Biol 1989;206:171-191. (Pubitemid 19095548)
16. Tam R, Saier MH, Jr. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 1993;57:320-346. (Pubitemid 23170095)
17. Fukami-Kobayashi K, Tateno Y, Nishikawa K. Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J Mol Biol 1999;286:279-290. (Pubitemid 29078412)
18. Newcomer ME, Gilliland GL, Quiocho FA. L-Arabinose-binding protein-sugar complex at 2.4 Å resolution. Stereochemistry and evidence for a structural change. J Biol Chem 1981;256:13213-13217.
19. Borths EL, Locher KP, Lee AT, Rees DC. The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proc Natl Acad Sci USA 2002;99:16642-16647. (Pubitemid 36034026)
20. Lawrence MC, Pilling PA, Epa VC, Berry AM, Ogunniyi AD, Paton JC. The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 1998;6:1553-1561. (Pubitemid 29000532)
21. Rukhman V, Anati R, Melamed-Frank M, Adir N. The MntC crystal structure suggests that import of Mn2+ in cyanobacteria is redox controlled. J Mol Biol 2005;348:961-969. (Pubitemid 40552796)
22. Lee YH, Deka RK, Norgard MV, Radolf JD, Hasemann CA. Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat Struct Biol 1999;6:628-633. (Pubitemid 29318950)
23. Lee YH, Dorwart MR, Hazlett KR, Deka RK, Norgard MV, Radolf JD, Hasemann CA. The crystal structure of Zn(II)-free Treponema pallidum TroA, a periplasmic metal-binding protein, reveals a closed conformation. J Bacteriol 2002;184:2300-2304. (Pubitemid 34259681)
24. Banerjee S, Wei B, Bhattacharyya-Pakrasi M, Pakrasi HB, Smith TJ. Structural determinants of metal specificity in the zinc transport protein ZnuA from synechocystis 6803. J Mol Biol 2003;333:1061-1069. (Pubitemid 37324505)
25. Li H, Jogl G. Crystal structure of the zinc-binding transport protein ZnuA from Escherichia coli reveals an unexpected variation in metal coordination. J Mol Biol 2007;368:1358-1366. (Pubitemid 46617595)
26. Clarke TE, Ku SY, Dougan DR, Vogel HJ, Tari LW. The structure of the ferric siderophore binding protein FhuD complexed with gallichrome. Nat Struct Biol 2000;7:287-291. (Pubitemid 30194451)
27. Karpowich NK, Huang HH, Smith PC, Hunt JF. Crystal structures of the BtuF periplasmic-binding protein for vitamin B12 suggest a functionally important reduction in protein mobility upon ligand binding. J Biol Chem 2003;278:8429-8434. (Pubitemid 36800593)
28. Muller A, Wilkinson AJ, Wilson KS, Duhme-Klair AK. An [{Fe(mecam)}2]6-bridge in the crystal structure of a ferric enterobactin binding protein. Angew Chem Int Ed Engl 2006;45:5132-5136.
29. Ho WW, Li H, Eakanunkul S, Tong Y, Wilks A, Guo M, Poulos TL. Holo- and apo- structures of bacterial periplasmic heme binding proteins. J Biol Chem, in press.
30. Kandt C, Xu Z, Tieleman DP. Opening and closing motions in the periplasmic vitamin B12 binding protein BtuF. Biochemistry 2006;45:13284-13292.
31. Krewulak KD, Shepherd CM, Vogel HJ. Molecular dynamics simulations of the periplasmic ferric-hydroxamate binding protein FhuD. Biometals 2005;18:375-386. (Pubitemid 41298022)
32. Hvorup RN, Goetz BA, Niederer M, Hollenstein K, Perozo E, Locher KP. Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 2007;317:1387-1390. (Pubitemid 47417478)
33. Perna NT, Plunkett GI, Blattner FR, Mau B, Blattner FR. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 2001;409:529-533.
34. Hendrickson WA, Horton JR, LeMaster DM. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J 1990;9:1665-1672. (Pubitemid 20137025)
35. Matthews BW. Solvent content of protein crystals. J Mol Biol 1968;33:491-497.
36. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326. (Pubitemid 27085611)
37. Terwilliger TC, Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr 1999;D55:849-861.
38. Terwilliger TC. Automated structure solution, density modification and model building. Acta Crystallogr D Biol Crystallogr 2002;58:1937-1940. (Pubitemid 35337291)
39. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-2132. (Pubitemid 41742764)
40. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr D Biol Crystallogr 1999;55:247-255. (Pubitemid 29053823)
41. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Crystallogr 1997;30:1022-1025. (Pubitemid 127485985)
42. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
43. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The protein data bank. Nucleic Acids Res 2000;28:235-242. (Pubitemid 30047768)
44. Case DA, Cheatham TE, III, Darden T, Gohlke H, Luo R, Merz KM, Jr, Onufriev A, Simmerling C, Wang B, Woods RJ. The Amber biomolecular simulation programs. J Comput Chem 2005;26:1668-1688. (Pubitemid 43076180)
45. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 2003;24:1999-2012.
46. Lee MC, Duan Y. Distinguish protein decoys by using a scoring function based on a new AMBER force field, short molecular dynamics simulations, and the generalized born solvent model. Proteins 2004;55:620-634. (Pubitemid 38620087)
47. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
48. Darden T, York D, Pedersen L. Particle mesh Ewald: an N [centerdot] log(N) method for Ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
49. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23:327-341.
50. Burmeister WP. Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Crystallogr D Biol Crystallogr 2000;56:328-341. (Pubitemid 30147184)
51. Weik M, Ravelli RB, Kryger G, McSweeney S, Raves ML, Harel M, Gros P, Silman I, Kroon J, Sussman JL. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci USA 2000;97:623-628. (Pubitemid 30070359)
52. Hayward S, Berendsen HJ. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 1998;30:144-154. (Pubitemid 28080149)
53. Holm L, Sander C. Dali: a network tool for protein structure comparison. Trends Biochem Sci 1995;20:478-480.
54. Mongan J. Interactive essential dynamics. J Comput Aided Mol Des 2004;18:433-436. (Pubitemid 40069139)
55. Gonin S, Arnoux P, Pierru B, Lavergne J, Alonso B, Sabaty M, Pignol D. Crystal structures of an extracytoplasmic solute receptor from a TRAP transporter in its open and closed forms reveal a helix- swapped dimer requiring a cation for alpha-keto acid binding. BMC Struct Biol 2007;7:11. (Pubitemid 46512607)
56. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389-3402. (Pubitemid 27359211)
57. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996;14:33-38. (Pubitemid 26152973)
58. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001;98:10037-10041. (Pubitemid 32802969)
59. Clarke TE, Braun V, Winkelmann G, Tari LW, Vogel HJ. X-ray crystallographic structures of the Escherichia coli periplasmic protein FhuD bound to hydroxamate-type siderophores and the antibiotic albomycin. J Biol Chem 2002;277:13966-13972.
60. Sharff AJ, Rodseth LE, Spurlino JC, Quiocho FA. Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. Biochemistry 1992;31:10657-10663.
61. Bjorkman AJ, Mowbray SL. Multiple open forms of ribose-binding protein trace the path of its conformational change. J Mol Biol 1998;279:651-664. (Pubitemid 28279471)
62. Trakhanov S, Vyas NK, Luecke H, Kristensen DM, Ma J, Quiocho FA. Ligand-free and -bound structures of the binding protein (LivJ) of the Escherichia coli ABC leucine/isoleucine/valine transport system: trajectory and dynamics of the interdomain rotation and ligand specificity. Biochemistry 2005;44:6597-6608. (Pubitemid 40593810)
63. Vyas NK, Vyas MN, Quiocho FA. Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science 1988;242:1290-1295. (Pubitemid 19008057)
64. Zou JY, Flocco MM, Mowbray SL. The 1.7 Å refined X-ray structure of the periplasmic glucose/galactose receptor from Salmonella typhimurium. J Mol Biol 1993;233:739-752. (Pubitemid 23314783)
65. Flocco MM, Mowbray SL. The 1.9 Å X-ray structure of a closed unliganded form of the periplasmic glucose/galactose receptor from Salmonella typhimurium. J Biol Chem 1994;269:8931-8936. (Pubitemid 24982070)
66. Ledvina PS, Tsai AL, Wang Z, Koehl E, Quiocho FA. Dominant role of local dipolar interactions in phosphate binding to a receptor cleft with an electronegative charge surface: equilibrium, kinetic, and crystallographic studies. Protein Sci 1998;7:2550-2559. (Pubitemid 28565696)
67. Walmsley AR, Shaw JG, Kelly DJ. Perturbation of the equilibrium between open and closed conformations of the periplasmic C4-dicarboxylate binding protein from Rhodobacter capsulatus. Biochemistry 1992;31:11175-11181.
68. Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007;450:515-521. (Pubitemid 350190241)
69. Braun V, Herrmann C. Docking of the periplasmic FecB binding protein to the FecCD transmembrane proteins in the ferric citrate transport system of Escherichia coli. J Bacteriol 2007;189:6913-6918. (Pubitemid 47525435)
70. Mademidis A, Killmann H, Kraas W, Flechsler I, Jung G, Braun V. ATP-dependent ferric hydroxamate transport system in Escherichia coli: periplasmic FhuD interacts with a periplasmic and with a transmembrane/ cytoplasmic region of the integral membrane protein FhuB, as revealed by competitive peptide mapping. Mol Microbiol 1997;26:1109-1123. (Pubitemid 27507893)
71. Sebulsky MT, Shilton BH, Speziali CD, Heinrichs DE. The role of FhuD2 in iron(III)-hydroxamate transport in Staphylococcus aureus. Demonstration that FhuD2 binds iron(III)-hydroxamates but with minimal conformational change and implication of mutations on transport. J Biol Chem 2003;278:49890-49900. (Pubitemid 37548824)
72. Kleywegt GJ. Experimental assessment of differences between related protein crystal structures. Acta Crystallogr D Biol Crystallogr 1999;55:1878-1884.
73. Olah GA, Trakhanov S, Trewhella J, Quiocho FA. Leucine/isoleucine/ valine-binding protein contracts upon binding of ligand. J Biol Chem 1993;268:16241-16247. (Pubitemid 23229921)
74. Oh BH, Pandit J, Kang CH, Nikaido K, Gokcen S, Ames GF, Kim SH. Three-dimensional structures of the periplasmic lysine/arginine/ ornithine-binding protein with and without a ligand. J Biol Chem 1993;268:11348-11355. (Pubitemid 23979949)
75. van der Heide T, Poolman B. ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep 2002;3:938-943.