Crystal structure of the Vibrio cholerae quorum-sensing regulatory protein HapR

Journal of Bacteriology

Volumn 189, Issue 15, 2007, Pages 5683-5691

  De Silva, Rukman S ^a   Kovacikova, Gabriela ^b   Lin, Wei ^b   Taylor, Ronald K ^b   Skorupski, Karen ^b   Kull, F Jon ^a  

^a Dartmouth College   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; HELIX LOOP HELIX PROTEIN; LIGAND; PROTEIN HAPR; PROTEIN KINASE; PROTEIN LUXO; PROTEIN TETR; REGULATOR PROTEIN; SOLVENT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; BIOFILM; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE EXPRESSION REGULATION; GENE REPRESSION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF; QUORUM SENSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA MUTATIONAL ANALYSIS; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENES, REPORTER; HELIX-TURN-HELIX MOTIFS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; QUORUM SENSING; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; VIBRIO CHOLERAE;

VIBRIO CHOLERAE;

EID: 34547645608     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01807-06     Document Type: Article

References (51)

1. Anonymous. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
2. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98:10037-10041.
3. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
4. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
5. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
6. DeLano, W. L. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.
7. De Silva, R. S., G. Kovacikova, W. Lin, R. K. Taylor, K. Skorupski, and F. J. Kull. 2005. Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. J. Biol. Chem. 280:13779-13783.
8. Dolinsky, T. J., J. E. Nielsen, J. A. McCammon, and N. A. Baker. 2004. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32:W665-W667.
9. Dover, L. G., P. E. Corsino, I. R. Daniels, S. L. Cocklin, V. Tatituri, G. S. Besra, and K. Futterer. 2004. Crystal structure of the TetR/CamR family repressor Mycobacterium tuberculosis EthR implicated in ethionamide resistance. J. Mol. Biol. 340:1095-1105.
10. Dundas, J., Z. Ouyang, J. Tseng, A. Binkowski, Y. Turpaz, and J. Liang. 2006. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34:W116-W118.
11. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
12. Engebrecht, J., and M. Silverman. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81:4154-4158.
13. Frenois, F., J. Engohang-Ndong, C. Locht, A. R. Baulard, and V. Villeret. 2004. Structure of EthR in a ligand bound conformation reveals therapeutic perspectives against tuberculosis. Mol. Cell 16:301-307.
14. Furste, J. P., W. Pansegrau, R. Frank, H. Blocker, P. Scholz, M. Bagdasarian, and E. Lanka. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48:119-131.
15. Gouet, P., E. Courcelle, D. I. Stuart, and F. Metoz. 1999. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305-308.
16. Hammer, B. K., and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101-104.
17. Hinrichs, W., C. Kisker, M. Duvel, A. Muller, K. Tovar, W. Hillen, and W. Saenger. 1994. Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance. Science 264:418-420.
18. Holm, L., and C. Sander. 1996. Mapping the protein universe. Science 273:595-603.
19. Iwanaga, M., K. Yamamoto, N. Higa, Y. Ichinose, N. Nakasone, and M. Tanabe. 1986. Culture conditions for stimulating cholera toxin production by Vibrio cholerae O1 El Tor. Microbiol. Immunol. 30:1075-1083.
20. Jobling, M. G., and R. K. Holmes. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26:1023-1034.
21. Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47(Pt. 2):110-119.
22. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26:795-800.
23. Kovacikova, G., W. Lin, and K. Skorupski. 2004. Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Mol. Microbiol. 53:129-142.
24. Kovacikova, G., and K. Skorupski. 2001. Overlapping binding sites for the virulence gene regulators AphA, AphB, and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol. Microbiol. 41:393-407.
25. Kovacikova, G., and K. Skorupski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:1135-1147.
26. Kovacikova, G., and K. Skorupski. 1999. A Vibrio cholerae LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. J. Bacteriol. 181:4250-4256.
27. Krissinel, E., and K. Henrick. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60:2256-2268.
28. Laskowski, R. A. 1995. SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J. Mol. Graph 13:307-330.
29. Lenz, D. H., K. C. Mok, B. N. Lilley, R. V. Kulkarni, N. S. Wingreen, and B. L. Bassler. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82.
30. Lilley, B. N., and B. L. Bassler. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol. Microbiol. 36:940-954.
31. Lin, W., G. Kovacikova, and K. Skorupski. 2005. Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. J. Bacteriol. 187:3013-3019.
32. Meibom, K. L., M. Blokesch, N. A. Dolganov, C. Y. Wu, and G. K. Schoolnik. 2005. Chitin induces natural competence in Vibrio cholerae. Science 310: 1824-1827.
33. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
34. Miller, M. B., and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165-199.
35. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
36. Natsume, R., Y. Ohnishi, T. Senda, and S. Horinouchi. 2004. Crystal structure of a gamma-butyrolactone autoregulator receptor protein in Streptomyces coelicolor A3(2). J. Mol. Biol. 336:409-419.
37. Natsume, R., R. Takeshita, M. Sugiyama, Y. Ohnishi, T. Senda, and S. Horinouchi. 2003. Crystallization of CprB, an autoregulator-receptor protein from Streptomyces coelicolor A3(2). Acta Crystallogr. D Biol. Crystallogr. 59:2313-2315.
38. Orth, P., D. Schnappinger, W. Hillen, W. Saenger, and W. Hinrichs. 2000. Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat. Struct. Biol. 7:215-219.
39. Parkinson, G., A. Gunasekera, J. Vojtechovsky, X. Zhang, T. A. Kunkel, H. Berman, and R. H. Ebright, 1996. Aromatic hydrogen bond in sequence-specific protein DNA recognition. Nat. Struct. Biol. 3:837-841.
40. Piper, K. R., S. Beck von Bodman, and S. K. Farrand. 1993. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448-450.
41. Ramagopal, U. A., Z. Dauter, R. Thirumuruhan, E. Fedorov, and S. C. Almo. 2005. Radiation-induced site-specific damage of mercury derivatives: phasing and implications. Acta Crystallogr. D Biol. Crystallogr. 61:1289-1298.
42. Schumacher, M. A., and R. G. Brennan. 2002. Structural mechanisms of multidrug recognition and regulation by bacterial multidrug transcription factors. Mol. Microbiol. 45:885-893.
43. Schumacher, M. A., M. C. Miller, S. Grkovic, M. H. Brown, R. A. Skurray, and R. G. Brennan. 2002. Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J. 21:1210-1218.
44. Schumacher, M. A., M. C. Miller, S. Grkovic, M. H. Brown, R. A. Skurray, and R. G. Brennan. 2001. Structural mechanisms of QacR induction and multidrug recognition. Science 294:2158-2163.
45. Skorupski, K., and R. K. Taylor. 1999. A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol. Microbiol. 31:763-771.
46. Skorupski, K., and R. K. Taylor. 1996. Positive selection vectors for allelic exchange. Gene 169:47-52.
47. Swartzman, E., M. Silverman, and E. A. Meighen. 1992. The luxR gene product of Vibrio harveyi is a transcriptional activator of the lux promoter. J. Bacteriol. 174:7490-7493.
48. Taylor, R. K., V. L. Miller, D. B. Furlong, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84:2833-2837.
49. Terwilliger, T. C. 2002. Automated structure solution, density modification and model building. Acta Crystallogr. D Biol. Crystallogr. 58: 1937-1940.
50. Zhang, L., P. J. Murphy, A. Kerr, and M. E. Tate. 1993. Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362:446-448.
51. Zhu, J., M. B. Miller, R. E. Vance, M. Dziejman, B. L. Bassler, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:3129-3134.