Crystal Structures of two Bordetella pertussis Periplasmic Receptors Contribute to Defining a Novel Pyroglutamic Acid Binding DctP Subfamily

Journal of Molecular Biology

Volumn 370, Issue 1, 2007, Pages 93-106

  Rucktooa, Prakash ^a   Antoine, Rudy ^b   Herrou, Julien ^b   Huvent, Isabelle ^a   Locht, Camille ^b   Jacob Dubuisson, Françoise ^b   Villeret, Vincent ^a   Bompard, Coralie ^a  

^a INSTITUT DE BIOLOGIE DE LILLE   (France)

^b INSTITUT PASTEUR DE LILLE   (France)

Author keywords

crystal structure; extracytoplasmic solute receptor; ligand binding; pyroglutamic acid; tripartite ATP independent periplasmic transport

Indexed keywords

ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; EXTRACYTOPLASMIC SOLUTE RECEPTOR DCTP; EXTRACYTOPLASMIC SOLUTE RECEPTOR DCTP6; LIGAND; PERMEASE; PYROGLUTAMIC ACID; RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL MEMBRANE; BINDING SITE; BORDETELLA PERTUSSIS; CELL TRANSPORT; CRYSTAL STRUCTURE; CYTOPLASM; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURE ANALYSIS; TRIPARTITE ATP INDEPENDENT PERIPLASMIC TRANSPORT SYSTEM;

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

EID: 34249288692     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.047     Document Type: Article

References (54)

1. Ames G.F., Mimura C.S., and Shyamala V. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: traffic ATPases. FEMS Microbiol. Rev. 6 (1990) 429-446
2. Tam R., and Saier Jr. M.H. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57 (1993) 320-346
3. Nikaido H., and Saier Jr. M.H. Transport proteins in bacteria: common themes in their design. Science 258 (1992) 936-942
4. Winnen B., Hvorup R.N., and Saier Jr. M.H. The tripartite tricarboxylate transporter (TTT) family. Res. Microbiol. 154 (2003) 457-465
5. Kelly D.J., and Thomas G.H. The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol. Rev. 25 (2001) 405-424
6. Neiditch M.B., Federle M.J., Miller S.T., Bassler B.L., and Hughson F.M. Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol. Cell 18 (2005) 507-518
7. Antoine R., Huvent I., Chemlal K., Deray I., Raze D., Locht C., and Jacob-Dubuisson F. The periplasmic binding protein of a tripartite tricarboxylate transporter is involved in signal transduction. J. Mol. Biol. 351 (2005) 799-809
8. Felder C.B., Graul R.C., Lee A.Y., Merkle H.P., and Sadee W. The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAPS PharmSci. 1 (1999) E2
9. Huvent I., Belrhali H., Antoine R., Bompard C., Locht C., Jacob-Dubuisson F., and Villeret V. Crystal structure of Bordetella pertussis BugD solute receptor unveils the basis of ligand binding in a new family of periplasmic binding proteins. J. Mol. Biol. 356 (2006) 1014-1026
10. Huvent I., Belrhali H., Antoine R., Bompard C., Locht C., Jacob-Dubuisson F., and Villeret V. Structural analysis of Bordetella pertussis BugE solute receptor in a bound conformation. Acta Crystallog. sect. D 62 (2006) 1375-1381
11. Muller A., Severi E., Mulligan C., Watts A.G., Kelly D.J., Wilson K.S., et al. Conservation of structure and mechanism in primary and secondary transporters exemplified by SiaP, a sialic acid binding virulence factor from Haemophilus influenzae. J. Biol. Chem. 281 (2006) 22212-22222
12. Oh B.H., Pandit J., Kang C.H., Nikaido K., Gokcen S., Ames G.F., and Kim S.H. Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein with and without a ligand. J. Biol. Chem. 268 (1993) 11348-11355
13. Rabus R., Jack D.L., Kelly D.J., and Saier Jr. M.H. TRAP transporters: an ancient family of extracytoplasmic solute-receptor-dependent secondary active transporters. Microbiology 145 (1999) 3431-3445
14. Forward J.A., Behrendt M.C., Wyborn N.R., Cross R., and Kelly D.J. 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
15. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 (1994) 4673-4680
16. Antoine R., Jacob-Dubuisson F., Drobecq H., Willery E., Lesjean S., and Locht C. Overrepresentation of a gene family encoding extracytoplasmic solute receptors in Bordetella. J. Bacteriol. 185 (2003) 1470-1474
17. Locht C., Antoine R., and Jacob-Dubuisson F. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4 (2001) 82-89
18. Schiefner A., Holtmann G., Diederichs K., Welte W., and Bremer E. Structural basis for the binding of compatible solutes by ProX from the hyperthermophilic archaeon Archaeoglobus fulgidus. J. Biol. Chem. 279 (2004) 48270-48281
19. Fukami-Kobayashi K., Tateno Y., and Nishikawa K. Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J. Mol. Biol. 286 (1999) 279-290
20. He J.J., and Quiocho F.A. Dominant role of local dipoles in stabilizing uncompensated charges on a sulfate sequestered in a periplasmic active transport protein. Protein Sci. 2 (1993) 1643-1647
21. Wang Z., Choudhary A., Ledvina P.S., and Quiocho F.A. 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. Yao N., Trakhanov S., and Quiocho F.A. 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
23. Hsiao C.D., Sun Y.J., Rose J., Cottam P.F., Ho C., and Wang B.C. Crystals of glutamine-binding protein in various conformational states. J. Mol. Biol. 240 (1994) 87-91
24. Spurlino J.C., Lu G.Y., and Quiocho F.A. 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
25. Sugiyama S., Vassylyev D.G., Matsushima M., Kashiwagi K., Igarashi K., and Morikawa K. Crystal structure of PotD, the primary receptor of the polyamine transport system in Escherichia coli. J. Biol. Chem. 271 (1996) 9519-9525
26. Takahashi H., Inagaki E., Kuroishi C., and Tahirov T.H. Structure of the Thermus thermophilus putative periplasmic glutamate/glutamine-binding protein. Acta Crystallog. sect. D 60 (2004) 1846-1854
27. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
28. Sharff A.J., Rodseth L.E., Spurlino J.C., and Quiocho F.A. 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
29. Magnusson U., Chaudhuri B.N., Ko J., Park C., Jones T.A., and Mowbray S.L. Hinge-bending motion of D-allose-binding protein from Escherichia coli: three open conformations. J. Biol. Chem. 277 (2002) 14077-14084
30. Magnusson U., Salopek-Sondi B., Luck L.A., and Mowbray S.L. X-ray structures of the leucine-binding protein illustrate conformational changes and the basis of ligand specificity. J. Biol. Chem. 279 (2004) 8747-8752
31. Bjorkman A.J., and Mowbray S.L. Multiple open forms of ribose-binding protein trace the path of its conformational change. J. Mol. Biol. 279 (1998) 651-664
32. Tame J.R., Murshudov G.N., Dodson E.J., Neil T.K., Dodson G.G., Higgins C.F., and Wilkinson A.J. The structural basis of sequence-independent peptide binding by OppA protein. Science 264 (1994) 1578-1581
33. Walmsley A.R., Shaw J.G., and Kelly D.J. The mechanism of ligand binding to the periplasmic C4-dicarboxylate binding protein (DctP) from Rhodobacter capsulatus. J. Biol. Chem. 267 (1992) 8064-8072
34. Cummins P.M., and O'Connor B. Pyroglutamyl peptidase: an overview of the three known enzymatic forms. Biochim. Biophys. Acta 1429 (1998) 1-17
35. Smirnova G.V., and Oktyabrsky O.N. Glutathione in bacteria. Biochemistry (Mosc.) 70 (2005) 1199-1211
36. Park S., and Imlay J.A. High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J. Bacteriol. 185 (2003) 1942-1950
37. Thalen M., van den I.J., Jiskoot W., Zomer B., Roholl P., de Gooijer C., et al. Rational medium design for Bordetella pertussis: basic metabolism. J. Biotechnol. 75 (1999) 147-159
38. Parkhill J., Sebaihia M., Preston A., Murphy L.D., Thomson N., Harris D.E., et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nature Genet. 35 (2003) 32-40
39. Rucktooa P., Huvent I., Antoine R., Lecher S., Jacob-Dubuisson F., Villeret V., and Bompard C. Crystallization and preliminary X-ray diffraction analysis of two extracytoplasmic solute receptors of the DctP family from Bordetella pertussis. Acta Crystallog. sect. F 62 (2006) 970-972
40. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 26 (1993) 795-800
41. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallog. sect. D 58 (2002) 1772-1779
42. Bricogne G., Vonrhein C., Flensburg C., Schiltz M., and Paciorek W. 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
43. Perrakis A., Sixma T.K., Wilson K.S., and Lamzin V.S. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallog. sect. D 53 (1997) 448-455
44. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D, 50, 760-763
45. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., and Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallog. sect. D 55 (1999) 247-255
46. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
47. Navaza J. Implementation of molecular replacement in AMoRe. Acta Crystallog. sect. D 57 (2001) 1367-1372
48. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallog. sect. D 60 (2004) 2256-2268
49. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucl. Acids Res. 31 (2003) 3381-3385
50. Holm L., and Sander C. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20 (1995) 478-480
51. Stibitz S. Use of conditionally counterselectable suicide vectors for allelic exchange. Methods Enzymol. 235 (1994) 458-465
52. Antoine R., Raze D., and Locht C. Genomics of Bordetella pertussis toxins. Int. J. Med. Microbiol. 290 (2000) 301-305
53. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA, USA
54. Wallace A.C., Laskowski R.A., and Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8 (1995) 127-134