Crystal Structure of the Ligand-Binding Protein EhuB from Sinorhizobium meliloti Reveals Substrate Recognition of the Compatible Solutes Ectoine and Hydroxyectoine

Journal of Molecular Biology

Volumn 374, Issue 5, 2007, Pages 1237-1250

  Hanekop, Nils ^a   Höing, Marina ^b   Sohn Bösser, Linda ^b   Jebbar, Mohamed ^c   Schmitt, Lutz ^a   Bremer, Erhard ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

ABC transporter; compatible solutes; osmoprotection; substrate binding protein; X ray crystallography

Indexed keywords

ARTICLE; CELL PROTECTION; CRYSTAL STRUCTURE; LIGAND BINDING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOREGULATION; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; SINORHIZOBIUM MELILOTI; SITE DIRECTED MUTAGENESIS;

SINORHIZOBIUM MELILOTI;

EID: 36249017396     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.071     Document Type: Article

References (54)

1. Kempf B., and Bremer E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170 (1998) 319-330
2. Horn C., Jenewein S., Sohn-Bosser L., Bremer E., and Schmitt L. Biochemical and structural analysis of the Bacillus subtilis ABC transporter OpuA and its isolated subunits. J. Mol. Microbiol. Biotechnol. 10 (2005) 76-91
3. Csonka L.N., and Epstein W. Osmoregulation. In: Neidhard F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella. Cellular and Molecular Biology (1996), American Society for Microbiology Press, Washington, DC 1210-1223
4. da Costa M.S., Santos H., and Galinski E.A. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv. Biochem. Eng. Biotechnol. 61 (1998) 117-153
5. Record Jr. M.T., Courtenay E.S., Cayley D.S., and Guttman H.J. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23 (1998) 143-148
6. Record Jr. M.T., Courtenay E.S., Cayley S., and Guttman H.J. Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem. Sci. 23 (1998) 190-194
7. Le Rudulier D., Strom A.R., Dandekar A.M., Smith L.T., and Valentine R.C. Molecular biology of osmoregulation. Science 224 (1984) 1064-1068
8. Canovas D., Borges N., Vargas C., Ventosa A., Nieto J.J., and Santos H. Role of Ngamma-acetyldiaminobutyrate as an enzyme stabilizer and an intermediate in the biosynthesis of hydroxyectoine. Appl. Environ. Microbiol. 65 (1999) 3774-3779
9. Lippert K., and Galinski E.A. Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Appl. Microbiol. Biotechnol. 37 (1992) 61-65
10. Bourot S., Sire O., Trautwetter A., Touze T., Wu L.F., Blanco C., and Bernard T. Glycine betaine-assisted protein folding in a lysA mutant of Escherichia coli. J. Biol. Chem. 275 (2000) 1050-1056
11. Arakawa T., and Timasheff S.N. The stabilization of proteins by osmolytes. Biophys. J. 47 (1985) 411-414
12. Bolen D.W., and Baskakov I.V. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J. Mol. Biol. 310 (2001) 955-963
13. Qu Y., Bolen C.L., and Bolen D.W. Osmolyte-driven contraction of a random coil protein. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9268-9273
14. Sleator R.D., and Hill C. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26 (2002) 49-71
15. Davidson A.L., and Chen J. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73 (2004) 241-268
16. Calderon M.I., Vargas C., Rojo F., Iglesias-Guerra F., Csonka L.N., Ventosa A., and Nieto J.J. Complex regulation of the synthesis of the compatible solute ectoine in the halophilic bacterium Chromohalobacter salexigens DSM 3043T. Microbiology 150 (2004) 3051-3063
17. Kuhlmann A.U., and Bremer E. Osmotically regulated synthesis of the compatible solute ectoine in Bacillus pasteurii and related Bacillus spp. Appl. Environ. Microbiol. 68 (2002) 772-783
18. Reshetnikov A.S., Khmelenina V.N., and Trotsenko Y.A. Characterization of the ectoine biosynthesis genes of haloalkalotolerant obligate methanotroph "Methylomicrobium alcaliphilum 20Z". Arch. Microbiol. 184 (2006) 286-297
19. Jebbar M., Sohn-Bosser L., Bremer E., Bernard T., and Blanco C. Ectoine-induced proteins in Sinorhizobium meliloti include an Ectoine ABC-type transporter involved in osmoprotection and ectoine catabolism. J. Bacteriol. 187 (2005) 1293-1304
20. Horn C., Sohn-Bosser L., Breed J., Welte W., Schmitt L., and Bremer E. Molecular determinants for substrate specificity of the ligand-binding protein OpuAC from Bacillus subtilis for the compatible solutes glycine betaine and proline betaine. J. Mol. Biol. 357 (2006) 592-606
21. Boos W., and Lucht J.M. Periplasmic binding protein-dependent ABC transporters. In: Neidhard F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella. Cellular and Molecular Biology (1996), American Society for Microbiology Press, Washington, DC 1175-1209
22. Gilson E., Alloing G., Schmidt T., Claverys J.P., Dudler R., and Hofnung M. Evidence for high affinity binding-protein dependent transport systems in Gram-positive bacteria and in Mycoplasma. EMBO J. 7 (1988) 3971-3974
23. Kempf B., Gade J., and Bremer E. Lipoprotein from the osmoregulated ABC transport system OpuA of Bacillus subtilis: purification of the glycine betaine binding protein and characterization of a functional lipidless mutant. J. Bacteriol. 179 (1997) 6213-6220
24. van der Heide T., and Poolman B. Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7102-7106
25. Quiocho F.A., and Ledvina P.S. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 20 (1996) 17-25
26. 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
27. 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
28. Schiefner A., Breed J., Bosser L., Kneip S., Gade J., Holtmann G., et al. Cation-pi interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli. J. Biol. Chem. 279 (2004) 5588-5596
29. 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. 275 (2004) 48270-48281
30. Lakowicz J.R. Principles of Fluorescence Spectroscopy. 2nd edit. (1999), Kluwer Academic Publishers, New York
31. 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
32. Roderick S.L., Chan W.W., Agate D.S., Olsen L.R., Vetting M.W., Rajashankar K.R., and Cohen D.E. Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat. Struct. Biol. 9 (2002) 507-511
33. Brejc K., van Dijk W.J., Klaassen R.V., Schuurmans M., van Der Oost J., Smit A.B., and Sixma T.K. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411 (2001) 269-276
34. 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
35. Armstrong N., Sun Y., Chen G.Q., and Gouaux E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395 (1998) 913-917
36. Trakhanov S., Kreimer D.I., Parkin S., Ames G.F., and Rupp B. Cadmium-induced crystallization of proteins: II. Crystallization of the Salmonella typhimurium histidine-binding protein in complex with l-histidine, l-arginine, or l-lysine. Protein Sci. 7 (1998) 600-604
37. Inbar L., Frolow F., and Lapidot A. The conformation of new tetrahydropyrimidine derivatives in solution and in the crystal. Eur. J. Biochem. 214 (1993) 897-906
38. Mao B., Pear M.R., McCammon J.A., and Quiocho F.A. Hinge-bending in l-arabinose-binding protein. The "Venus's-flytrap" model. J. Biol. Chem. 257 (1982) 1131-1133
39. Yao N., Trakhanov S., and Quiocho F.A. Refined 1.89-A structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins. Biochemistry 33 (1994) 4769-4779
40. Sun Y.J., Rose J., Wang B.C., and Hsiao C.D. The structure of glutamine-binding protein complexed with glutamine at 1.94 A resolution: comparisons with other amino acid binding proteins. J. Mol. Biol. 278 (1998) 219-229
41. Ma J.C., and Dougherty D.A. The cation-pi interaction. Chem. Rev. 97 (1997) 1303-1324
42. Mecozzi S., West Jr. A.P., and Dougherty D.A. Cation-pi interactions in aromatics of biological and medicinal interest: electrostatic potential surfaces as a useful qualitative guide. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 10566-10571
43. Kleywegt G.J. Experimental assessment of differences between related protein crystal structures. Acta Crystallogr. Sect. D 55 (1999) 1878-1884
44. Wilkinson A.J., and Verschueren K.H.G. Crystal structures of periplasmic solute binding proteins in ABC transport complexes illuminate their function. In: Holland I.B., Cole S.P., and Kuchler K. (Eds). ABC Proteins from Bacteria to Man (2003), Academic Press, Amsterdam
45. Miller J.H. A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria (1992), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
46. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. In: Carter C.W., and Sweet R.M. (Eds). Methods in Enzymology vol. 276 (1997), Academic Press, London
47. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. Sect. D 55 (1999) 849-861
48. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. Sect. A 47 (1991) 110-119
49. Murshudov G., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D 53 (1997) 240-255
50. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. Sect. D 57 (2001) 122-133
51. Lamzin V.S., and Wilson K.S. Automated refinement of protein models. Acta Crystallogr. Sect. D 49 (1993) 129-147
52. Burmeister W.P. Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Crystallogr. Sect. D 56 (2000) 328-341
53. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (1992) 472-475
54. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291