A salt-bridge motif involved in ligand binding and large-scale domain motions of the maltose-binding protein

Biophysical Journal

Volumn 89, Issue 5, 2005, Pages 3362-3371

  Stockner, Thomas ^a   Vogel, Hans J ^a   Tieleman, D Peter ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; GLUTAMIC ACID; LYSINE; MALTOSE; MALTOSE BINDING PROTEIN; MALTOTRIOSE; OLIGOSACCHARIDE; PROTEIN MALFGK2; SUGAR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL SURVIVAL; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CHEMOTAXIS; CYTOPLASM; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; SIMULATION;

BACTERIA (MICROORGANISMS);

EID: 27744606438     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.069443     Document Type: Article

References (69)

1. Higgins, C. F. 1992. ABC transporters-from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
2. Stock, J. B., and M. G. Surette. 1996. Chemotaxis. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. F. C. Neidhardt, editor. ASM Press, Washington, D.C. 1103-1129.
3. Quiocho, F. A., and P. S. Ledvina. 1996. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 20:17-25.
4. Sugiyama, S., Y. Matsuo, K. Maenaka, D. G. Vassylyev, M. Matsushima, K. Kashiwagi, K. Igarashi, and K. Morikawa. 1996. The 1.8-Å x-ray structure of the Escherichia coli PotD protein complexed with spermidine and the mechanism of polyamine binding. Protein Sci. 5:1984-1990.
5. Krewulak, K. D., R. S. Peacock, and H. J. Vogel. 2004. Periplasmic binding proteins involved in bacterial iron uptake. In Iron Transport in Bacteria. J. H. Corsa, A. R. Mey, and S. M. Payne, editors. ASM Press, Washington, D.C. 118-129.
6. Spurlino, J. C., G. Y. Lu, and F. A. Quiocho. 1991. The 2.3-Å resolution structure of the maltose-binding or maltodextrin-binding protein, a primary receptor of bacterial active-transport and chemotaxis. J. Biol. Chem. 266:5202-5219.
7. Fukami-Kobayashi, K., Y. Tateno, and K. Nishikawa. 1999. Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J. Mol. Biol. 286:279-290.
8. Sharff, A. J., L. E. Rodseth, J. C. Spurlino, and F. A. Quiocho. 1992. Crystallographic evidence of a large ligand-induced hinge-twist motion between the 2 domains of the maltodextrin binding-protein involved in active-transport and chemotaxis. Biochemistry. 31:10657-10663.
9. Boos, W., and J. M. Lucht. 1996. Periplasmic Binding Protein-Dependent ABC Transporters, in Escherichia coli and Salmonella: Cellular And Molecular Biology, 2nd ed. F. C. Neidhardt, editor. ASM Press, Washington, D.C. 1149-1209.
10. Boos, W., and H. Shuman. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol. Mol. Biol. Rev. 62:204-229.
11. Quiocho, F. A., J. C. Spurlino, and L. E. Rodseth. 1997. Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor. Structure. 5:997-1015.
12. Kellermann, O., and S. Szmelcman. 1974. Active transportation of maltose in Escherichia coli K-12. Involvement of a perplasmic maltose-binding protein. Eur. J. Biochem. 47:139-149.
13. Szmelcman, S., M. Schwartz, T. J. Silhavy, and W. Boos. 1976. Maltose transport in Escherichia coli-K12-Comparison of transport kinetics in wild-type and lambda-resistant mutants with dissociation-constants of maltose-binding protein as measured by fluorescence quenching. Eur. J. Biochem. 65:13-19.
14. Treptow, N. A., and H. A. Shuman. 1985. Genetic-evidence for substrate and periplasmic-binding-protein recognition by the malf and malg proteins, cytoplasmic membrane-components of the Escherichia coli maltose transport-system. J. Bacteriol. 163:654-660.
15. Treptow, N. A., and H. A. Shuman. 1988. Allele-specific male mutations that restore interactions between maltose-binding protein and the inner-membrane components of the maltose transport-system. J. Mol. Biol. 202:809-822.
16. Hor, L. I., and H. A. Shuman. 1993. Genetic-analysis of periplasmic binding-protein dependent transport in Escherichia coli-each lobe of maltose-binding protein interacts with a different subunit of the MalFGK(2) membrane-transport complex. J. Mol. Biol. 233: 659-670.
17. Pang, A., Y. Arinaminpathy, M. S. P. Sansom, and P. C. Biggin. 2003. Interdomain dynamics and ligand binding: molecular dynamics simulations of glutamine binding protein. FEBS Lett. 550:168-174.
18. Arinaminpathy, Y., M. S. Sansom, and P. C. Biggin. 2002. Molecular dynamics simulations of the ligand-binding domain of the ionotropic glutamate receptor GluR2. Biophys. J. 82:676-683.
19. Roccatano, D., A. E. Mark, and S. Hayward. 2001. Investigation of the mechanism of domain closure in citrate synthase by molecular dynamics simulation. J. Mol. Biol. 310:1039-1053.
20. Daidone, I., D. Roccatano, and S. Hayward. 2004. Investigating the accessibility of the closed domain conformation of citrate synthase using essential dynamics sampling. J. Mol. Biol. 339:515-525.
21. Tirion, M. M. 1996. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 77:1905-1908.
22. Tama, F., and Y. H. Sanejouand. 2001. Conformational change of proteins arising from normal mode calculations. Protein Eng. 14:1-6.
23. Kitao, A., and N. Go. 1991. Conformational dynamics of polypeptides and proteins in the dihedral angle space and in the cartesian coordinate space-normal mode analysis of deca-alanine. J. Comput. Chem. 12: 359-368.
24. Echols, N., D. Milburn, and M. Gerstein. 2003. MolMovDB: analysis and visualization of conformational change and structural flexibility. Nucleic Acids Res. 31:478-482.
25. Miller, D. M., J. S. Olson, J. W. Pflugrath, and F. A. Quiocho. 1983. Rates of ligand-binding to periplasmic proteins involved in bacterial transport and chemotaxis. J. Biol. Chem. 258:3665-3672.
26. Rubin, S. M., S. Y. Lee, E. J. Ruiz, A. Pines, and D. E. Wemmer. 2002. Detection and characterization of xenon-binding sites in proteins by 129Xe NMR spectroscopy. J. Mol. Biol. 322:425-440.
27. Biotech Validation Suite for Protein Structures, http://biotech.ebi. ac.uk:8400.
28. Duan, X., and F. A. Quiocho. 2002. Structural evidence for a dominant role of nonpolar interactions in the binding of a transport/chemosensory receptor to its highly polar ligands. Biochemistry. 41:706-712.
29. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. (Online). 7:306-317.
30. Berendsen, H. J. C., D. Vanderspoel, and R. Vandrunen. 1995. GROMACS-a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 91:43-56.
31. Scott, W. R. P., P. H. Hunenberger, I. G. Tironi, A. E. Mark, S. R. Billeter, J. Fennen, A. E. Torda, T. Huber, P. Kruger, and W. F. van Gunsteren. 1999. The GROMOS biomolecular simulation program package. J. Phys. Chem. A. 103:3596-3607.
32. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. Reidel, Dordrecht, The Netherlands. 331-342.
33. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3689.
34. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
35. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald-an N.Log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
36. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
37. Miyamoto, S., and P. A. Kollman. 1992. SETTLE. J. Comput. Chem. 13:952-962.
38. Feenstra, K. A., B. Hess, and H. J. C. Berendsen. 1999. Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J. Comput. Chem. 20:786-798.
39. Amadei, A., A. B. M. Linssen, and H. J. C. Berendsen. 1993. Essential dynamics of proteins. Proteins. 17:412-425.
40. Hayward, S., and H. J. C. Berendsen. 1998. Systematic analysis of domain motions in proteins from conformational change: New results on citrate synthase and T4 lysozyme. Proteins. 30:144-154.
41. Hayward, S., and R. A. Lee. 2002. Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50. J. Mol. Graph. Model. 21:181-183.
42. Shilton, B. H., M. M. Flocco, M. Nilsson, and S. L. Mowbray. 1996. Conformational changes of three periplasmic receptors for bacterial chemotaxis and transport: The maltose-, glucose/galactose- and ribose-binding proteins. J. Mol. Biol. 264:350-363.
43. Merzel, F., and J. C. Smith. 2002. Is the first hydration shell of lysozyme of higher density than bulk water? Proc. Natl. Acad. Sci. USA. 99:5378-5383.
44. Svergun, D. I., S. Richard, M. H. J. Koch, Z. Sayers, S. Kuprin, and G. Zaccai. 1998. Protein hydration in solution: experimental observation by x-ray and neutron scattering. Proc. Natl. Acad. Sci. USA. 95:2267-2272.
45. Clarke, T. E., S. Y. Ku, D. R. Dougan, H. J. Vogel, and L. W. Tari. 2000. The structure of the ferric siderophore binding protein FhuD complexed with gallichrome. Nat. Struct. Biol. 7:287-291.
46. Borths, E. L., K. P. Locher, A. T. Lee, and D. C. Rees. 2002. The structure of Escherichia coll BtuF and binding to its cognate ATP binding cassette transporter. Proc. Natl. Acad. Sci. USA. 99:16642-16647.
47. Karpowich, N. K., H. H. Huang, P. C. Smith, and J. F. Hunt. 2003. 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. 278:8429-8434.
48. Krewulak, K. D., C. M. Shepherd, and H. J. Vogel. 2005. Molecular dynamics simulations of the periplasmic ferric-hydroxamate binding protein FhuD. Biometals. 8:375-386.
49. Bjorkman, A. J., and S. L. Mowbray. 1998. Multiple open forms of ribose-binding protein trace the path of its conformational change. J. Mol. Biol. 279:651-664.
50. Sun, Y. J., J. Rose, B. C. Wang, and C. D. Hsiao. 1998. The structure of glutamine-binding protein complexed with glutamine at 1.94 angstrom resolution: comparisons with other amino acid binding proteins. J. Mol. Biol. 278:219-229.
51. Austermuhle, M. I., J. A. Hall, C. S. Klug, and A. L. Davidson. 2004. Maltose-binding protein is open in the catalytic transition state for ATP hydrolysis during maltose transport. J. Biol. Chem. 279:28243-28250.
52. Zhang, Y. H., D. E. Mannering, A. L. Davidson, N. H. Yao, and M. D. Manson. 1996. Maltose-binding protein containing an interdomain disulfide bridge confers a dominant-negative phenotype for transport and chemotaxis. J. Biol. Chem. 271:17881-17889.
53. Koiwai, O., and H. Hayashi. 1979. Studies on bacterial chemotaxis.4. Interaction of maltose receptor with a membrane-bound chemosensing component. J. Biochem. (Tokyo). 86:27-34.
54. Manson, M. D., and M. Kossmann. 1986. Mutations in tar suppress defects in maltose chemotaxis caused by specific male mutations. J. Bacteriol. 165:34-40.
55. Kossmann, M., C. Wolff, and M. D. Manson. 1988. Maltose chemoreceptor of Escherichia coli-interaction of maltose-binding protein and the tar signal transducer. J. Bacteriol. 170:4516-4521.
56. Gardina, P., C. Conway, M. Kossman, and M. Manson. 1992. Aspartate and maltose-binding protein interact with adjacent sites in the tar chemotactic signal transducer of Escherichia coli. J. Bacteriol. 174:1528-1536.
57. Zhang, Y. H., P. J. Gardina, A. S. Kuebler, H. S. Kang, J. A. Christopher, and M. D. Manson. 1999. Model of maltose-binding protein/chemoreceptor complex supports intrasubunit signaling mechanism. Proc. Natl. Acad. Sci. USA. 96:939-944.
58. Milburn, M. V., G. G. Prive, D. L. Milligan, W. G. Scott, J. Yeh, J. Jancarik, D. E. Koshland, and S. H. Kim. 1991. 3-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science. 254:1342-1347.
59. Flocco, M. M., and S. L. Mowbray. 1994. The 1.9 Angstrom x-ray structure of a closed unliganded form of the periplasmic glucose/ galactose receptor from Salmonella typhimurium. J. Biol. Chem. 269: 8931-8936.
60. Wolf, A., E. W. Shaw, K. Nikaido, and G. F. L. Ames. 1994. The histidine-binding protein undergoes conformational-changes in the absence of ligand as analyzed with conformation-specific monoclonal-antibodies. J. Biol. Chem. 269:23051-23058.
61. Monod, J., J. Wyman, and J. P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88-118.
62. Koshland, D. E., Jr., G. Nemethy, and D. Filmer. 1966. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry. 5:365-385.
63. Evenas, J., V. Tugarinov, N. R. Skrynnikov, N. K. Goto, R. Muhandiram, and L. E. Kay. 2001. Ligand-induced structural changes to maltodextrin-binding protein as studied by solution NMR spectroscopy. J. Mol. Biol. 309:961-974.
64. Millet, O., R. P. Hudson, and L. E. Kay. 2003. The energetic cost of domain reorientation in maltose-binding protein as studied by NMR and fluorescence spectroscopy. Proc. Natl. Acad. Sci. USA. 100: 12700-12705.
65. Eisenhaber, F., P. Lijnzaad, P. Argos, C. Sander, and M. Scharf. 1995. The double cubic lattice method-efficient approaches to numerical-integration of surface-area and volume and to dot surface contouring of molecular assemblies. J. Comput. Chem. 16:273-284.
66. Eisenberg, D., and A. D. Mclachlan. 1986. Solvation energy in protein folding and binding. Nature. 319:199-203.
67. Kraulis, P. J. 1991. MolScript-a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
68. Merritt, E. A., and D. J. Bacon. 1997. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:505-524.
69. PyMOL. DeLano Scientific, http://pymol.sourceforge.net