Hierarchical Binding of the TodT Response Regulator to Its Multiple Recognition Sites at the tod Pathway Operon Promoter

Journal of Molecular Biology

Volumn 376, Issue 2, 2008, Pages 325-337

  Lacal, Jesús ^a   Guazzaroni, María Eugenia ^a   Busch, Andreas ^a   Krell, Tino ^a   Ramos, Juan L ^a  

^a CSIC   (Spain)

Author keywords

DNA protein interactions; Pseudomonas; response regulator; sensor kinase; TodT

Indexed keywords

AMINO ACID DERIVATIVE; BACTERIAL PROTEIN; PROTEIN TODT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; DNA BINDING; GEL MOBILITY SHIFT ASSAY; IN VITRO STUDY; IN VIVO STUDY; MICROCALORIMETRY; MUTATIONAL ANALYSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; STOICHIOMETRY;

PSEUDOMONAS;

EID: 38349194474     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.004     Document Type: Article

References (65)

1. Ramos J.L., Gallegos M.T., Marqués S., Ramos-González M.I., Espinosa-Urgel M., and Segura A. Responses of Gram-negative bacteria to certain environmental stressors. Curr. Opin. Microbiol. 4 (2001) 166-171
2. Bijlsma J.J., and Groisman E.A. Making informed decisions: regulatory interactions between two-component systems. Trends Microbiol. 11 (2003) 359-366
3. Elsen S., Swem L.R., Swem D.L., and Bauer C.E. RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiol. Mol. Biol. Rev. 68 (2004) 263-279
4. Kern D., Volkman B.F., Luginbuhl P., Nohaile M.J., Kustu S., and Wemmer D.E. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 402 (1999) 894-898
5. Lacal J., Busch A., Guazzaroni M.E., Krell T., and Ramos J.L. The TodS-TodT two-component regulatory system recognizes a wide range of effectors and works with DNA-bending proteins. Proc. Natl Acad. Sci. USA 103 (2006) 8191-8196
6. Mascher T., Helmann J.D., and Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70 (2006) 910-938
7. Jones D.F., Stenzel R.A., and Donohue T.J. Mutational analysis of the C-terminal domain of the Rhodobacter sphaeroides response regulator PrrA. Microbiology 151 (2005) 4103-4110
8. Ventre I., Filloux A., and Lazdunski A. Two-component signal transduction systems: a key to the adaptative potential of Pseudomonas aeruginosa. In: Ramos J.L. (Ed). Pseudomonas Vol. II: Virulence and Gene Regulation (2004), Kluwer Academic/Plenum Publishers, New York, NY 257-288 Chapter 9
9. Blanco A.G., Sola M., Gomis-Ruth F.X., and Coll M. Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10 (2002) 701-713
10. Eldalak A., and Hullet F.M. Cys303 in the histidine kinase PhoR is crucial for the phosphotransfer reaction in the PhoPR two-component system in Bacillus subtilis. J. Bacteriol. 189 (2007) 410-421
11. Hirooka K., Kunikane S., Matsuoka H., Yoshida K.-I., Kumamote K., Tojo S., and Fujita Y. Dual regulation of the Bacillus subtilis regulon comprising the lmrAB and yxaGH operons and yxaF gene by two transcriptional repressors, LmrA and YxaF, in response to flavonoids. J. Bacteriol. 189 (2007) 5170-5182
12. Kivistik P.A., Putrins M., Püvi K., Ilves H., Kivisaar M., and Horak R. The ColRS two-component system regulates membrane functions and protects Pseudomonas putida against phenol. J. Bacteriol. 188 (2006) 8109-8117
13. McKessar S.J., and Hakenbeck R. The two-component regulatory system TCS08 is involved in cellobiose metabolism of Streptococcus pneumoniae R6. J. Bacteriol. 189 (2007) 1342-1350
14. 2+-induced gene regulation in Pseudomonas aeruginosa. J. Bacteriol. 188 (2006) 3995-4006
15. Stock A.M., Robinson V.L., and Goudreau P.N. Two-component signal transduction. Annu. Rev. Biochem. 69 (2000) 183-215
16. Segura A., Rojas A., Hurtado A., Huertas M.J., and Ramos J.L. Comparative genomic analysis of solvent extrusion pumps in Pseudomonas strains exhibiting different degrees of solvent tolerance. Extremophiles 7 (2003) 371-376
17. Zylstra G.J., and Gibson D.T. Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli. J. Biol. Chem. 264 (1989) 14940-14946
18. Lau P.C.K., Wang Y., Patel A., Labbé D., Bergeron H., Brousseau R., et al. A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc. Natl Acad. Sci. USA 94 (1997) 1453-1458
19. Mosqueda G., Ramos-González M.I., and Ramos J.L. Toluene metabolism by the solvent-tolerant Pseudomonas putida DOT-T1 strain, and its role in solvent impermeabilization. Gene 232 (1999) 69-76
20. Busch A., Lacal J., Marcos A., Ramos J.L., and Krell T. Bacterial sensor kinase TodS interacts with agonistic and antagonistic signals. Proc. Natl Acad. Sci. USA 104 (2007) 13774-13779
21. Bourret R.B. Census of prokaryotic senses. J. Bacteriol. 188 (2006) 4165-4168
22. D'Souza M., Glass E.M., Syed M.H., Zhang Y., Rodriguez A., Maltsev N., and Galperin M.Y. SENTRA: a database of signal transduction proteins for comparative genome analysis. Nucleic Acids Res. 35 (2007) D271-D273
23. Galperin M.Y. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188 (2006) 4169-4182
24. Leoni L., Ascenzi P., Bocedi A., Rampioni G., Castellini L., and Zennaro E. Styrene-catabolism regulation in Pseudomonas fluorescens ST: phosphorylation of StyR induces dimerization and cooperative DNA-binding. Biochem. Biophys. Res. Commun. 303 (2003) 926-931
25. Leoni L., Rampioni G., Di Stefano V., and Zennaro E. Dual role of response regulator StyR in styrene catabolism regulation. Appl. Environ. Microbiol. 71 (2005) 5411-5419
26. Leoni L., Rampioni G., and Zennaro E. Styrene, an unpalatable substrate with complex regulatory networks. In: Ramos J.L., and Filloux A. (Eds). Pseudomonas Vol. V: A Model System in Biology (2007), Springer, Dorchester, The Netherlands 59-88 Chapter 3
27. Milani M., Leoni L., Rampioni G., Zennaro E., Ascenzi P., and Bolognesi M. An active-like structure in the unphosphorylated StyR response regulator suggests a phosphorylation-dependent activation mechanism. Structure 13 (2005) 1289-1297
28. Cui Y., Chatterjee A., Hasegawa H., and Chatterjee A.K. Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J. Bacteriol. 188 (2006) 4715-4726
29. Ecc, homologues within the LuxR family, retain the ability to function as activators of transcription. J. Bacteriol. 185 (2003) 7001-7007
30. Shultzaberger R.K., Chen Z., Lewis K.A., and Schneider T.D. Anatomy of Escherichia coli sigma-70 promoters. Nucleic Acids Res. 35 (2006) 771-788
31. 70 subunit is responsible for the recognition of the 'extended - 10' motif at promoters. EMBO J. 16 (1997) 4034-4040
32. 70-dependent promoter requiring a - 35 DNA element and an extended - 10 TGn motif. J. Bacteriol. 188 (2006) 8352-8359
33. Keilty S., and Rosenberg M. Constitutive function of a positively regulated promoter reveals new sequences essential for activity. J. Biol. Chem. 262 (1987) 6389-6395
34. Kumar A., Malloch R.A., Fujita N., Smillie D.A., Ishihama A., and Hayward R.S. The minus 35-recognition region of Escherichia coli sigma 70 is inessential for initiation of transcription at an "extended minus 10" promoter. J. Mol. Biol. 232 (1993) 406-418
35. Collado-Vides J., Magasanik B., and Gralla J.G. Control site location and transcriptional regulation in Escherichia coli. Microbiol. Rev. 55 (1991) 371-394
36. Rhodius V.A., and Busby S.J. Positive activation of gene expression. Curr. Opin. Microbiol. 1 (1998) 152-159
37. Nixon B.T., Ronson C.W., and Ausubel F.M. Two component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc. Natl Acad. Sci. USA 83 (1986) 7850-7854
38. Pérez-Martín J., and de Lorenzo V. Clues and consequences of DNA bending in transcription. Annu. Rev. Microbiol. 51 (1997) 593-628
39. Tropel D., and van der Meer J.R. Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol. Mol. Biol. Rev. 68 (2004) 474-500
40. Todd M.J., and Gomez J. Enzyme kinetics determined using calorimetry: a general assay for enzymatic activity?. Anal. Biochem. 296 (2001) 179-187
41. Spaink H.P., Okker R.J.H., Wijffelman C.A., Pees E., and Lugtenberg B. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol. Biol. 9 (1987) 27-39
42. Raleigh E.A., Trimarchi R., and Revel H. Genetics and physical mapping of merA (rglA) and mcrB (rglB) loci of Escherichia coli K12. Genetics 122 (1989) 279-296
43. Studier F.W., Rosenberg A.-H., Dunn J.J., and Dubendoff J.W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185 (1990) 60-89
44. Ramos J.L., Duque E., Huertas M.J., and Haïdour A. Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons. J. Bacteriol. 177 (1995) 3911-3916
45. Ramos-González M.I., Olson M., Gatenby A.A., Mosqueda G., Manzanera M., Campos M.J., et al. Cross-regulation between a novel two-component signal transduction system for catabolism of toluene in Pseudomonas mendocina and the TodST system from Pseudomonas putida. J. Bacteriol. 184 (2002) 7062-7067
46. Hawley D.K., and McClure W.R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 11 (1983) 2237-2255
47. Benoff B., Yang H., Lawson C.L., Parkinson G., Liu J., Blatter E., et al. Structural basis of transcription activation: the CAP-αCTD-DNA complex. Science 297 (2002) 1562-1566
48. Gerischer U., Segura A., and Ornston L.N. PcaU, a transcriptional activator of genes for protocatechuate utilization in Acinetobacter. J. Bacteriol. 180 (1998) 1512-1524
49. Guo Z., and Houghton J.E. PcaR-mediated activation and repression of pca genes from Pseudomonas putida are propagated by its binding to both the - 35 and the - 10 promoter elements. Mol. Microbiol. 32 (1999) 253-263
50. Aiba H., Nakasai F., Mizushima S., and Mizuno T. Phosphorylation of a bacterial activator protein, OmpR, by a protein kinase, EnvZ, results in stimulation of its DNA-binding ability. J. Biochem. 106 (1989) 5-7
51. Harrison-McMonagle P., Denissova N., Martínez-Hackert E., Ebright R.H., and Stock A.M. Orientation of OmpR monomers within an OmpR:DNA complex determined by DNA affinity cleaving. J. Mol. Biol. 285 (1999) 555-566
52. Yoshida Y., Qin L., Egger L.A., and Inouye M. Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J. Biol. Chem. 281 (2006) 17114-17123
53. Bergstrom L.C., Qin L., Harlocker S.L., Egger L.A., and Inouye M. Hierarchical and co-operative binding of OmpR to a fusion construct containing the ompC and ompF upstream regulatory sequences of Escherichia coli. Genes Cells 3 (1998) 777-788
54. Harlocker S.L., Bergstrom L., and Inouye M. Tandem binding of six OmpR proteins to the ompF upstream regulatory sequence of Escherichia coli. J. Biol. Chem. 270 (1995) 26849-26856
55. Rice P.A., Yang S., Mizuchi K., and Nash H.A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87 (1996) 1296-1306
56. Busby S., and Ebright R.H. Transcription activation by catabolite activator protein (CAP). J. Mol. Biol. 293 (1999) 199-213
57. Hagerman P.J. Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem. 17 (1988) 265-286
58. Maris A.E., Sawaya M.R., Kaczor-Grzeskowiak M., Jarvis M.R., Bearson S.M., Kopka M.L., et al. Dimerization allows DNA target site recognition by the NarL response regulator. Nat. Struct. Biol. 9 (2002) 771-778
59. Walthers D., Tran V.K., and Kenney L.J. Interdomain linkers of homologous response regulators determine their mechanism of action. J. Bacteriol. 185 (2003) 317-324
60. Birck C., Chen Y., Hulett F.M., and Samana J.P. The crystal structure of the phosphorylation domain in PhoP reveals a functional tandem association mediated by an asymmetric interface. J. Bacteriol. 185 (2003) 254-261
61. Birck C., Mourey L., Gouet P., Fabry B., Schumacher J., Rousseau P., et al. Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure Fold. Des. 7 (1999) 1505-1515
62. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. (1999), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
63. González-Pérez M.M., Ramos J.L., Gallegos M.T., and Marqués S. Critical nucleotides in the upstream region of the XylS-dependent TOL meta-cleavage pathway operon promoter as deduced from analysis of mutants. J. Biol. Chem. 274 (1999) 2286-2290
64. Guazzaroni M.E., Krell T., Felipe A., Ruíz R., Meng C., Zhang X., et al. The multidrug efflux regulator TtgV recognizes a wide range of structurally different effectors in solution and complexed with target DNA: evidence from isothermal titration calorimetry. J. Biol. Chem. 280 (2005) 20887-20893
65. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding contacts and heats of binding using a new titration calorimeter. Anal. Biochem. 179 (1989) 131-137