Crystal structure of Bordetella pertussis BugD solute receptor unveils the basis of ligand binding in a new family of periplasmic binding proteins

Journal of Molecular Biology

Volumn 356, Issue 4, 2006, Pages 1014-1026

  Huvent, Isabelle ^a   Belrhali, Hassan ^b   Antoine, Rudy ^a   Bompard, Coralie ^a   Locht, Camille ^a   Jacob Dubuisson, Françoise ^a   Villeret, Vincent ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

Aspartate; Bordetella; Carboxylate binding; Crystal structure; Periplasmic binding protein

Indexed keywords

AMIDE; ASPARTIC ACID; BACTERIAL PROTEIN; CARBOXYLIC ACID; OXYGEN; PERIPLASMIC BINDING PROTEIN; PROTEIN BUG; PROTEIN BUGD; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BORDETELLA PERTUSSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON; HYDROGEN BOND; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE;

BACTERIA (MICROORGANISMS); BORDETELLA; BORDETELLA PERTUSSIS; DIONAEA;

EID: 31344463251     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.096     Document Type: Article

References (50)

1. J.S. Lolkema, B. Poolman, and W.N. Konings Bacterial solute uptake and efflux systems Curr. Opin. Microbiol. 1 1998 248 253
2. A.J. Driessen, B.P. Rosen, and W.N. Konings Diversity of transport mechanisms: common structural principles Trends Biochem. Sci. 25 2000 397 401
3. K.A. Widenhorn, W. Boos, J.M. Somers, and W.W. Kay Cloning and properties of the Salmonella typhimurium tricarboxylate transport operon in Escherichia coli J. Bacteriol. 170 1988 883 888
4. J.A. Forward, M.C. Behrendt, N.R. Wyborn, R. Cross, and D.J. Kelly TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse gram-negative bacteria J. Bacteriol. 179 1997 5482 5493
5. B. Winnen, R.N. Hvorup, and M.H. Saier Jr The tripartite tricarboxylate transporter (TTT) family Res. Microbiol. 154 2003 457 465
6. R. Rabus, D.L. Jack, D.J. Kelly, and M.H. Saier Jr TRAP transporters: an ancient family of extracytoplasmic solute- receptor-dependent secondary active transporters Microbiology 145 1999 3431 3445
7. R. Antoine, F. Jacob-Dubuisson, H. Drobecq, E. Willery, S. Lesjean, and C. Locht Overrepresentation of a gene family encoding extracytoplasmic solute receptors in Bordetella J. Bacteriol. 185 2003 1470 1474
8. H. Nikaido, and J.A. Hall Overview of bacterial ABC transporters Methods Enzymol. 292 1998 3 20
9. R. Tam, and M.H. Saier Jr Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria Microbiol. Rev. 57 1993 320 346
10. J.W. Pflugrath, and F.A. Quiocho The 2 Å resolution structure of the sulfate-binding protein involved in active transport in Salmonella typhimurium J. Mol. Biol. 200 1988 163 180
11. J.S. Sack, M.A. Saper, and F.A. Quiocho 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. 206 1989 171 191
12. J.Y. Zou, M.M. Flocco, and S.L. Mowbray The 1.7 Å refined X-ray structure of the periplasmic glucose/galactose receptor from Salmonella typhimurium J. Mol. Biol. 233 1993 739 752
13. J.C. Spurlino, G.Y. Lu, and F.A. Quiocho The 2.3-Å resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis J. Biol. Chem. 266 1991 5202 5219
14. N. Yao, S. Trakhanov, and F.A. Quiocho Refined 1.89-Å structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins Biochemistry 33 1994 4769 4779
15. A.V. Nickitenko, S. Trakhanov, and F.A. Quiocho 2 Å resolution structure of DppA, a periplasmic dipeptide transport/chemosensory receptor Biochemistry 34 1995 16585 16595
16. M.D. Adams, and D.L. Oxender Bacterial periplasmic binding protein tertiary structures J. Biol. Chem. 264 1989 15739 15742
17. F.A. Quiocho, and P.S. Ledvina Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes Mol. Microbiol. 20 1996 17 25
18. E.G. Hutchinson, and J.M. Thornton PROMOTIF-a program to identify and analyze structural motifs in proteins Protein Sci. 5 1996 212 220
19. K. Fukami-Kobayashi, Y. Tateno, and K. Nishikawa Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history J. Mol. Biol. 286 1999 279 290
20. S. Sugiyama, D.G. Vassylyev, M. Matsushima, K. Kashiwagi, K. Igarashi, and K. Morikawa Crystal structure of PotD, the primary receptor of the polyamine transport system in Escherichia coli J. Biol. Chem. 271 1996 9519 9525
21. Z. Wang, A. Choudhary, P.S. Ledvina, and F.A. Quiocho Fine tuning the specificity of the periplasmic phosphate transport receptor. Site-directed mutagenesis, ligand binding, and crystallographic studies J. Biol. Chem. 269 1994 25091 25094
22. B.H. Oh, G.F. Ames, and S.H. Kim Structural basis for multiple ligand specificity of the periplasmic lysine-, arginine-, ornithine-binding protein J. Biol. Chem. 269 1994 26323 26330
23. C.D. Hsiao, Y.J. Sun, J. Rose, and B.C. Wang The crystal structure of glutamine-binding protein from Escherichia coli J. Mol. Biol. 262 1996 225 242
24. L. Holm, and C. Sander Protein structure comparison by alignment of distances matrices J. Mol. Biol. 223 1993 123 138
25. E. Krissinel, and K. Henrick Secondary structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallog. sect. D 60 2004 2256 2268
26. B.H. Oh, J. Pandit, C.H. Kang, K. Nikaido, S. Gokcen, G.F. Ames, and S.H. Kim Three-dimensional structures of the periplasmic lysine/arginine/ornithine- binding protein with and without a ligand J. Biol. Chem. 268 1993 11348 11355
27. A.J. Bjorkman, and S.L. Mowbray Multiple open forms of ribose-binding protein trace the path of its conformational change J. Mol. Biol. 279 1998 651 664
28. U. Magnusson, B.N. Chaudhuri, J. Ko, C. Park, T.A. Jones, and S.L. Mowbray Hinge-bending motion of D-allose-binding protein from Escherichia coli: three open conformations J. Biol. Chem. 277 2002 14077 14084
29. U. Magnusson, B. Salopek-Sondi, L.A. Luck, and S.L. Mowbray X-ray structures of the leucine-binding protein illustrate conformational changes and the basis of ligand specificity J. Biol. Chem. 279 2004 8747 8752
30. A.J. Sharff, L.E. Rodseth, J.C. Spurlino, and F.A. Quiocho 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 31 1992 10657 10663
31. B.H. Oh, C.H. Kang, H. De Bondt, S.H. Kim, K. Nikaido, A.K. Joshi, and G.F. Ames The bacterial periplasmic histidine-binding protein. Structure/function analysis of the ligand-binding site and comparison with related proteins J. Biol. Chem. 269 1994 4135 4143
32. Y.J. Sun, J. Rose, B.C. Wang, and C.D. Hsiao The structure of glutamine-binding protein complexed with glutamine at 1.94 Å resolution: comparisons with other amino acid binding proteins J. Mol. Biol. 278 1998 219 229
33. J.I. Yeh, H.P. Biemann, J. Pandit, D.E. Koshland, and S.H. Kim The three-dimensional structure of the ligand-binding domain of a wild-type bacterial chemotaxis receptor. Structural comparison to the cross-linked mutant forms and conformational changes upon ligand binding J. Biol. Chem. 268 1993 9787 9792
34. M.V. Milburn, G.G. Prive, D.L. Milligan, W.G. Scott, J. Yeh, and J. Jancarik Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand Science 254 1991 1342 1347
35. F.A. Quiocho, and N.K. Vyas Novel stereospecificity of the l-arabinose-binding protein Nature 310 1984 381 386
36. S.L. Mowbray, and L.B. Cole 1.7 Å X-ray structure of the periplasmic ribose receptor from Escherichia coli J. Mol. Biol. 225 1992 155 175
37. B.N. Chaudhuri, J. Ko, C. Park, T.A. Jones, and S.L. Mowbray Structure of d-allose binding protein from Escherichia coli bound to d-allose at 1.8 Å resolution J. Mol. Biol. 286 1999 1519 1531
38. F.A. Quiocho, J.C. Spurlino, and L.E. Rodseth Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor Structure 5 1997 997 1015
39. J.R. Tame, G.N. Murshudov, E.J. Dodson, T.K. Neil, G.G. Dodson, C.F. Higgins, and A.J. Wilkinson The structural basis of sequence-independent peptide binding by OppA protein Science 264 1994 1578 1581
40. J.R. Tame, E.J. Dodson, G. Murshudov, C.F. Higgins, and A.J. Wilkinson The crystal structures of the oligopeptide-binding protein OppA complexed with tripeptide and tetrapeptide ligands Structure 3 1995 1395 1406
41. J. Parkhill, M. Sebaihia, A. Preston, L.D. Murphy, N. Thomson, and D.E. Harris Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica Nature Genet. 35 2003 32 40
42. F.D. Menozzi, R. Mutombo, G. Renauld, C. Gantiez, J.H. Hannah, and E. Leininger Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis Infect. Immun. 62 1994 769 778
43. S. Doublie Preparation of selenomethionyl proteins for phase determination Methods Enzymol. 276 1997 523 530
44. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
45. T. Schneider, and G. Sheldrick Substructure solution with SHELXD Acta Crystallog. sect. D 58 2002 1772 1779
46. G. Bricogne, C. Vonrhein, C. Flensburg, M. Schiltz, and W. Paciorek Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0 Acta Crystallog. sect. D 59 2003 2023 2030
47. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nature Struct. Biol. 6 1999 458 463
48. G.N. Murshudov, A. Lebedev, A.A. Vagin, K.S. Wilson, and E.J. Dodson Efficient anisotropic refinement of macromolecular structures using FFT Acta Crystallog. sect. D 55 1999 247 255
49. Roussel, A, Cambillau, C. (1991). Turbo-Frodo. In Silicon Graphics Geometry, Partners Directory, Silicon Graphics, Mountain View, CA.
50. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallog. 26 1993 283 291