Crystal structures of DntR inducer binding domains in complex with salicylate offer insights into the activation of LysR-type transcriptional regulators

Molecular Microbiology

Volumn 81, Issue 2, 2011, Pages 354-367

  Devesse, Laurence ^a,b   Smirnova, Irina ^c,d   Lönneborg, Rosa ^d   Kapp, Ulrike ^a   Brzezinski, Peter ^d   Leonard, Gordon A ^a   Dian, Cyril ^e  

^a EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^b University of Bath   (United Kingdom)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; LYSR TYPE TRANSCRIPTION REGULATOR; PROTEIN DNTR; SALICYLIC ACID; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; INDUCER BINDING DOMAIN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN VARIANT; TRANSCRIPTION INITIATION;

ALLOSTERIC REGULATION; BINDING SITES; BURKHOLDERIA; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MUTANT PROTEINS; POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SALICYLATES; TRANSCRIPTION FACTORS;

EID: 79960168122     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07673.x     Document Type: Article

References (46)

1. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., etal. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst D66: 213-221.
2. Bundy, B.M., Collier, L.S., Hoover, T.R., and Neidle, E.L. (2002) Synergistic transcriptional activation by one regulatory protein in response to two metabolites. Proc Natl Acad Sci USA 99: 7693-7698.
3. Choi, H., Kim, S., Mukhopadhyay, P., Cho, S., Woo, J., Storz, G., and Ryu, S.E. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105: 103-113.
4. Clark, T.J., Phillips, R.S., Bundy, B.M., Momany, C., and Neidle, E.L. (2004) Benzoate decreases the binding of cis, cis-muconate to the BenM regulator despite the synergistic effect of both compounds on transcriptional activation. J Bacteriol 186: 1200-1204.
5. Danley, D.E. (2006) Crystallization to obtain protein-ligand complexes for structure-aided drug design. Acta Cryst D62: 569-575.
6. Dauter, Z., Dauter, M., de La Fortelle, E., Bricogne, G., and Sheldrick, G.M. (1999) Can anomalous signal of sulfur become a tool for solving protein crystal structures? J Mol Biol 289: 83-92.
7. Dickerson, R.E., Goodsell, D.S., and Neidle, S. (1994) '...the tyranny of the lattice...'. Proc Natl Acad Sci USA 91: 3579-3583.
8. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010) Features and development of Coot. Acta Cryst D66: 486-501.
9. Evans, P.R. (2005) Scaling and assessment of data quality. Acta Cryst D62: 72-82.
10. Ezezika, O.C., Haddad, S., Clark, T.J., Neidle, E.L., and Momany, C. (2007) Distinct effector-binding sites enable synergistic transcriptional activation by BenM, a LysR-type regulator. J Mol Biol 367: 616-629.
11. Flot, D., Mairs, T., Giraud, T., Guijarro, M., Lesourd, M., Rey, V., etal. (2010) The ID23-2 structural biology microfocus beamline at the ESRF. J Synchrotron Rad 17: 107-118.
12. French, G.S., and Wilson, K.S. (1978) On the treatment of negative intensity observations. Acta Cryst A34: 517-525.
13. Haigler, B.E., and Spain, J.C. (1993) Biodegradation of 4-nitrotoluene by Pseudomonas sp. strain 4NT. Appl Environ Microbiol 59: 2239-2243.
14. Hayward, S., and Berendsen, H.J.C. (1998) Systematic Analysis of domain motions in proteins from conformational change; new results on citrate synthase and T4 lysozyme. Proteins: Struct Funct Bioinf 30: 144-154.
15. Indyk, L., and Fisher, H.F. (1998) Theoretical aspects of isothermal titration calorimetry. Methods Enzymol 295: 350-364.
16. Johnson, G.R., Jain, R.K., and Spain, J.C. (2002) Origins of the 2, 4-dinitrotoluene pathway. J Bacteriol 184: 4219-4232.
17. Jones, S.E., Lloyd, L.J., Tan, K.K., and Buck, M. (2003) Secretion defects that activate the phage shock response of Escherichia coli. J Bacteriol 185: 6707-6711.
18. Kabsch, W. (2010) Integration, scaling, space-group assignment and post-refinement. Acta Cryst D66: 133-144.
19. Leslie, A.G.W. (2006) The integration of macromolecular diffraction data. Acta Cryst D62: 48-57.
20. Lessner, D.J., Parales, R.E., Narayan, S., and Gibson, G.T. (2003) Expression of the nitroarene dioxygenase genes in Comamonas sp. strain JS765 and Acidovorax sp. strain JS42 is induced by multiple aromatic compounds. J Bacteriol 185: 3895-3904.
21. Lönneborg, R., Smirnova, I., Dian, C., Leonard, G.A., and Brzezinski, P. (2007) In vivo and in vitro investigation of transcriptional regulation by DntR. J Mol Biol 372: 571-582.
22. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
23. Maddocks, S.E., and Oyston, P.C. (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609-3623.
24. Monferrer, D., Tralau, T., Kertesz, M.A., Dix, I., Solà, M., and Usón, I. (2010) Structural studies on the full-length LysR-type regulator TsaR from Comamonas testosteroni T-2 reveal a novel open conformation of the tetrameric LTTR fold. Mol Microbiol 75: 1199-1214.
25. Muraoka, S., Okumura, R., Ogawa, N., Nonaka, T., Miyashita, K., and Senda, T. (2003) Crystal structure of a full-length LysR-type transcriptional regulator, CbnR: unusual combination of two subunit forms and molecular bases for causing and changing DNA bend. J Mol Biol 328: 555-566.
26. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst D53: 240-255.
27. Ng, L.C., and Forsman, M. (2000) Whole cell biosensor for the detection of explosives. The FOA Defence Research Establishment research report.
28. Nishino, S.F., Paoli, G.C., and Spain, J.C. (2000) Aerobic degradation of dinitrotoluenes and pathway for bacterial degradation of 2, 6-dinitrotoluene. Appl Environ Microbiol 66: 2139-2147.
29. Nurizzo, D., Mairs, T., Guijarro, M., Rey, V., Meyer, J., Fajardo, P., etal. (2006) The ID23-1 structural biology beamline at the ESRF. J Synchrotron Rad 13: 227-238.
30. Parales, R.E. (2004) Nitrobenzoates and Aminobenzoates Are Chemoattractants for Pseudomonas Strains. Appl Environ Microbiol 70: 285-292.
31. Perrakis, A., Morris, R.M., and Lamzin, V.S. (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6: 458-463.
32. Porrúa, O., García-Jaramillo, M., Santero, E., and Govantes, F. (2007) The LysR-type regulator AtzR binding site: DNA sequences involved in activation, repression and cyanuric acid-dependent repositioning. Mol Microbiol 66: 410-427.
33. Quade, N., Dieckmann, M., Haffke, M., Heroven, A.K., Dersch, P., and Heinz, D.W. (2011) Structure of the effector-binding domain of the LysR-type transcription factor RovM from Yersinia pseudotuberculosis. Acta Cryst D67: 81-90.
34. Ruangprasert, A., Craven, S.H., Neidle, E.L., and Momany, C. (2010) Full-length structures of BenM and two variants reveal different oligomerization schemes for LysR-Type transcriptional regulators. J Mol Biol 404: 568-586.
35. Sainsbury, S., Lane, L.A., Ren, J., Gilbert, R.J., Saunders, N.J., Robinson, C.V., etal. (2009) The structure of CrgA from Neisseria meningitidis reveals a new octameric assembly state for LysR transcriptional regulators. Nucleic Acids Res 37: 4545-4558.
36. Sainsbury, S., Ren, J., Nettleship, J.E., Saunders, N.J., Stuart, D.I., and Owens, R.J. (2010) The structure of a reduced form of OxyR from Neisseria meningitidis. BMC Struct Biol 10: 10.
37. Schell, M.A. (1985) Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. Gene 36: 301-309.
38. Schneider, T.R., and Sheldrick, G.M. (2002) Substructure solution with SHELXD. Acta Cryst D58: 1772-1779.
39. Sheldrick, G.M. (2008) A short history of SHELX. Acta Cryst A64: 112-122.
40. Smirnova, I.A., Dian, C., Leonard, G.A., McSweeney, S., Birse, D., and Brzezinski, P. (2004) Development of a bacterial biosensor for nitrotoluenes: the crystal structure of the transcriptional regulator DntR. J Mol Biol 340: 405-418.
41. Spanggord, R.J., Spain, J.C., Nishino, S.F., and Mortelmans, K.E. (1991) Biodegradation of 2, 4-dinitrotoluene by a Pseudomonas sp. Appl Environ Microbiol 57: 3200-3205.
42. Suen, W.-C., and Spain, J.C. (1992) Cloning and characterization of Pseudomonas sp. strain DNT genes for 2, 4-dinitrotoluene degradation. J Bacteriol 175: 1831-1837.
43. Tetin, S.Y., and Hazlett, T.L. (2000) Optical spectroscopy in studies of antibody-hapten interactions. Methods 20: 341-361.
44. Tropel, D., and van der Meer, J.R. (2004) Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68: 474-500.
45. Tyrrell, R., Verschueren, K.H., Dodson, E.J., Murshudov, G.N., Addy, C., and Wilkinson, A.J. (1997) The structure of the cofactor-binding fragment of the LysR family member, CysB: a familiar fold with a surprising subunit arrangement. Structure 5: 1017-1032.
46. Zhou, X., Lou, Z., Fu, S., Yang, A., Shen, H., Li, Z., etal. (2010) Crystal structure of ArgP from Mycobacterium tuberculosis confirms two distinct conformations of full-length LysR transcriptional regulators and reveals its function in DNA binding and transcriptional regulation. J Mol Biol 396: 1012-1024.