C4-Dicarboxylates Sensing Mechanism Revealed by the Crystal Structures of DctB Sensor Domain

Journal of Molecular Biology

Volumn 383, Issue 1, 2008, Pages 49-61

  Zhou, Yan Feng ^a   Nan, Beiyan ^a   Nan, Jie ^a   Ma, Qingjun ^b   Panjikar, Santosh ^b   Liang, Yu He ^a   Wang, Yiping ^a   Su, Xiao Dong ^a  

^a PEKING UNIVERSITY   (China)

^b DESY   (Germany)

Author keywords

C4 dicarboxylates; crystal structure; DctB; histidine kinase; signal perception

Indexed keywords

APOPROTEIN; BACTERIAL PROTEIN; CARBON; CELL PROTEIN; DICARBOXYLIC ACID; MALONIC ACID; PROTEIN CITA; PROTEIN DCTB; PROTEIN DCUS; PROTEIN HISTIDINE KINASE; SUCCINIC ACID; UNCLASSIFIED DRUG; DCTB PROTEIN, SINORHIZOBIUM; DCUS PROTEIN, E COLI; DICARBOXYLATE TRANSPORTER; DPIB PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; LIGAND; PROTEIN KINASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

SINORHIZOBIUM MELILOTI;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DICARBOXYLIC ACID TRANSPORTERS; DICARBOXYLIC ACIDS; DIMERIZATION; ESCHERICHIA COLI PROTEINS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI;

EID: 52249108909     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.08.010     Document Type: Article

References (56)

1. Stock A.M., Robinson V.L., and Goudreau P.N. Two-component signal transduction. Annu. Rev. Biochem. 69 (2000) 183-215
2. Mascher T., Helmann J.D., and Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70 (2006) 910-938
3. 4-dicarboxylate transport genes from Rhizobium leguminosarum. J. Bacteriol. 160 (1984) 903-909
4. 4-dicarboxylic acid transport. Gene 85 (1989) 135-144
5. 4-dicarboxylate transport genes in Rhizobium meliloti. Mol. Microbiol. 3 (1989) 813-823
6. Yurgel S.N., and Kahn M.L. Dicarboxylate transport by rhizobia. FEMS Microbiol. Rev. 28 (2004) 489-501
7. Gu B., Lee J.H., Hoover T.R., Scholl D., and Nixon B.T. Rhizobium meliloti DctD, a sigma 54-dependent transcriptional activator, may be negatively controlled by a subdomain in the C-terminal end of its two-component receiver module. Mol. Microbiol. 13 (1994) 51-66
8. Huala E., Stigter J., and Ausubel F.M. The central domain of Rhizobium leguminosarum DctD functions independently to activate transcription. J. Bacteriol. 174 (1992) 1428-1431
9. Lee J.H., Scholl D., Nixon B.T., and Hoover T.R. Constitutive ATP hydrolysis and transcription activation by a stable, truncated form of Rhizobium meliloti DCTD, a sigma 54-dependent transcriptional activator. J. Biol. Chem. 269 (1994) 20401-20409
10. Ledebur H., Gu B., Sojda III J., and Nixon B.T. Rhizobium meliloti and Rhizobium leguminosarum dctD gene products bind to tandem sites in an activation sequence located upstream of sigma 54-dependent dctA promoters. J. Bacteriol. 172 (1990) 3888-3897
11. Scholl D., and Nixon B.T. Cooperative binding of DctD to the dctA upstream activation sequence of Rhizobium meliloti is enhanced in a constitutively active truncated mutant. J. Biol. Chem. 271 (1996) 26435-26442
12. Hendrickson W.A. Transduction of biochemical signals across cell membranes. Q. Rev. Biophys. 38 (2005) 321-330
13. Giblin L., Boesten B., Turk S., Hooykaas P., and O'Gara F. Signal transduction in the Rhizobium meliloti dicarboxylic acid transport system. FEMS Microbiol. Lett. 126 (1995) 25-30
14. Yeh J.I., Biemann H.P., Pandit J., Koshland D.E., and Kim S.H. 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
15. Yeh J.I., Biemann H.P., Prive G.G., Pandit J., Koshland Jr. D.E., and Kim S.H. High-resolution structures of the ligand binding domain of the wild-type bacterial aspartate receptor. J. Mol. Biol. 262 (1996) 186-201
16. Reinelt S., Hofmann E., Gerharz T., Bott M., and Madden D.R. The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J. Biol. Chem. 278 (2003) 39189-39196
17. Pappalardo L., Janausch I.G., Vijayan V., Zientz E., Junker J., Peti W., et al. The NMR structure of the sensory domain of the membranous two-component fumarate sensor (histidine protein kinase) DcuS of Escherichia coli. J. Biol. Chem. 278 (2003) 39185-39188
18. Borgstahl G.E., Williams D.R., and Getzoff E.D. 1.4 A structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active site, and chromophore. Biochemistry 34 (1995) 6278-6287
19. Kneuper H., Janausch I.G., Vijayan V., Zweckstetter M., Bock V., Griesinger C., and Unden G. The nature of the stimulus and of the fumarate binding site of the fumarate sensor DcuS of Escherichia coli. J. Biol. Chem. 280 (2005) 20596-20603
20. 4-dicarboxylate- or citrate-specific sensor. J. Bacteriol. 189 (2007) 4290-4298
21. Reid C.J., and Poole P.S. Roles of DctA and DctB in signal detection by the dicarboxylic acid transport system of Rhizobium leguminosarum. J. Bacteriol. 180 (1998) 2660-2669
22. Neiditch M.B., Federle M.J., Pompeani A.J., Kelly R.C., Swem D.L., Jeffrey P.D., et al. Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126 (2006) 1095-1108
23. Bader M.W., Sanowar S., Daley M.E., Schneider A.R., Cho U., Xu W., et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122 (2005) 461-472
24. Cheung J., Bingman C.A., Reyngold M., Hendrickson W.A., and Waldburger C.D. Crystal structure of a functional dimer of the PhoQ sensor domain. J. Biol. Chem. 283 (2008) 13762-13770
25. 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. Nucleic Acids Res. 22 (1994) 4673-4680
26. Gouet P., Courcelle E., Stuart D.I., and Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15 (1999) 305-308
27. 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
28. Lancaster C.R., Gross R., and Simon J. A third crystal form of Wolinella succinogenes quinol:fumarate reductase reveals domain closure at the site of fumarate reduction. Eur. J. Biochem. 268 (2001) 1820-1827
29. Iverson T.M., Luna-Chavez C., Cecchini G., and Rees D.C. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284 (1999) 1961-1966
30. Krissinel E., and Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372 (2007) 774-797
31. Lo Conte L., Chothia C., and Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285 (1999) 2177-2198
32. Kaspar S., and Bott M. The sensor kinase CitA (DpiB) of Escherichia coli functions as a high-affinity citrate receptor. Arch. Microbiol. 177 (2002) 313-321
33. Baker K.E., Ditullio K.P., Neuhard J., and Kelln R.A. Utilization of orotate as a pyrimidine source by Salmonella typhimurium and Escherichia coli requires the dicarboxylate transport protein encoded by dctA. J. Bacteriol. 178 (1996) 7099-7105
34. Yurgel S., Mortimer M.W., Rogers K.N., and Kahn M.L. New substrates for the dicarboxylate transport system of Sinorhizobium meliloti. J. Bacteriol. 182 (2000) 4216-4221
35. Gan H.H., Perlow R.A., Roy S., Ko J., Wu M., Huang J., et al. Analysis of protein sequence structure similarity relationships. Biophys. J. 83 (2002) 2781-2791
36. Gordeliy V.I., Labahn J., Moukhametzianov R., Efremov R., Granzin J., Schlesinger R., et al. Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex. Nature 419 (2002) 484-487
37. Hulko M., Berndt F., Gruber M., Linder J.U., Truffault V., Schultz A., et al. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126 (2006) 929-940
38. Inouye M. Signaling by transmembrane proteins shifts gears. Cell 126 (2006) 829-831
39. Nan B., Zhou Y., Liang Y.H., Wen J., Ma Q., Zhang S., et al. Purification and preliminary X-ray crystallographic analysis of the ligand-binding domain of Sinorhizobium meliloti DctB. Biochim. Biophys. Acta 1764 (2006) 839-841
40. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., and Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229 (1993) 105-124
41. Kristensen O., and Laurberg M. Expression, refolding and crystallization of Aquifex aeolicus elongation factor P. Acta Crystallogr. Sect. D 58 (2002) 1039-1041
42. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
43. Kabsch W. Automatic processing of rotation diffraction data from crystals of internally unknown symmetry and cell constants. J. Appl. Crystallogr. 26 (1993) 795-800
44. Panjikar S., Parthasarathy V., Lamzin V.S., Weiss M.S., and Tucker P.A. Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr. Sect. D 61 (2005) 449-457
45. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50 (1994) 760-763
46. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr. Sect. D 58 (2002) 1772-1779
47. Cowtan K. DM: an automated procedure for phase improvement by density modification. CCP4/ESF-EACBM Newsl. Protein Crystallogr. 31 (1994) 34-38
48. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463
49. Wang J.W., Chen J.R., Gu Y.X., Zheng C.D., and Fan H.F. Direct-method SAD phasing with partial-structure iteration: towards automation. Acta Crystallogr. Sect. D 60 (2004) 1991-1996
50. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 60 (2004) 2126-2132
51. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D 53 (1997) 240-255
52. 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
53. Davis I.W., Murray L.W., Richardson J.S., and Richardson D.C. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32 (2004) W615-W619
54. Rossmann M.G., and Blow D.M. The detection of sub-units within the crystallographic asymmetric unit. Acta Crystallogr. 15 (1962) 24-31
55. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
56. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D 54 (1998) 905-921