The Transcriptional Repressor TtgV Recognizes a Complex Operator as a Tetramer and Induces Convex DNA Bending

Journal of Molecular Biology

Volumn 369, Issue 4, 2007, Pages 927-939

  Guazzaroni, María Eugenia ^a   Krell, Tino ^a   Gutiérrez del Arroyo, Paloma ^b,c   Vélez, Marisela ^c   Jiménez, Mercedes ^d   Rivas, Germán ^d   Ramos, Juan L ^a  

^a CSIC   (Spain)

^b CSIC   (Spain)

^c INSTITUTO NICOLÁS CABRERA   (Spain)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

AFM; DNA bending; DNA binding; IclR family; TtgV

Indexed keywords

CURVED DNA; DIMETHYL SULFATE; RNA POLYMERASE; TETRAMER;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CIRCULAR DICHROISM; DNA BINDING; DNA FOOTPRINTING; GENE TARGETING; GENETIC TRANSCRIPTION; ISOTHERM; OLIGOMERIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; STATISTICAL SIGNIFICANCE; STOICHIOMETRY; ULTRACENTRIFUGATION;

PSEUDOMONAS PUTIDA;

EID: 34248587997     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.022     Document Type: Article

References (55)

1. Molina-Henares A.J., Krell T., Guazzaroni M.E., Segura A., and Ramos J.L. Members of the IclR family of transcriptional activators and repressors exhibit conserved features outside the DNA binding domain. FEMS Microbiol. Rev. 30 (2006) 157-186
2. Krell T., Molina-Henares A.J., and Ramos J.L. The IclR family of transcriptional activators and repressors can be defined by a single profile. Protein Sci. 15 (2006) 1207-1213
3. 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
4. Nasser W., Reverchon S., Condemine G., and Robert-Baudouy J. Specific interactions of Erwinia chrysanthemi KdgR repressor with different operators of genes involved in pectinolysis. J. Mol. Biol. 236 (1994) 427-440
5. Ferrández A., García J.L., and Díaz E. Genetic characterization and expression in heterologous hosts of the 3-3-(hydroxyphenyl)-propionate catabolic pathway of Escherichia coli K-12. J. Bacteriol. 170 (1997) 2573-2581
6. Di Marco A.A., and Ornston L.N. Regulation of p-hydroxybenzoate hydroxylase synthesis by PobR bound to an operator in Acinetobacter calcoaceticus. J. Bacteriol. 176 (1994) 4277-4284
7. Pan B., Unnikrishnan I., and La Porte D.C. The binding site of the IclR repressor protein overlaps the promoter of aceBAK. J. Bacteriol. 178 (1996) 3982-3984
8. Popp R., Kohl T., Patz P., Trautwein G., and Gerischer U. Differential DNA. binding of transcriptional regulator PcaU from Acinetobacter sp. strain ADP1. J. Bacteriol. 184 (2002) 1988-1997
9. 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
10. Zhang R.G., Kim Y., Skarina T., Beasley S., Laskowski R., and Arrowsmith C. Crystal structure of Thermotoga maritima 0065, a member of the IclR transcriptional factor family. J. Biol. Chem. 277 (2002) 19183-19190
11. Thomson N.R., Nasser W., McGowan S., Sebaihia M., and Salmond G.P. Erwinia carotovora has two KdgR-like proteins belonging to the IclR family of transcriptional regulator: identification and characterization of the RexZ activator and the KdgR repressor of pathogenesis. Microbiology 145 (1999) 1531-1545
12. Krell, T., Terán, W., López-Mayorga, O., Rivas, G., Jiménez, M., Molina-Henares, A., Gallegos, M.T. & Ramos, J.L. (2007). Optimisation of the palindromic order of TtgR operator enhances binding cooperativity. J. Mol.Biol. In the press.
13. Negré D., Cortay J.C., Galinier A., Sauve P., and Cozzone A.J. Specific interactions between the IclR repressor of the acetate operon of Escherichia coli and its operator. J. Mol. Biol. 228 (1992) 23-29
14. Donald L.J., Hosfield D.J., Cuvelier S.L., Ens W., Standing K.G., and Duckworth H.W. Mass spectrometric study of the Escherichia coli repressor proteins, Ic1R and Gc1R, and their complexes with DNA. Protein Sci. 10 (2001) 1370-1380
15. Rojas A., Duque E., Mosqueda G., Golden G., Hurtado A., Ramos J.L., and Segura A. Three efflux pumps are required to provide efficient tolerance to toluene in Pseudomonas putida DOT-T1E. J. Bacteriol. 183 (2001) 3967-3973
16. Rojas A., Segura A., Guazzaroni M.E., Terán W., Hurtado A., Gallegos M.T., and Ramos J.L. In vivo and in vitro evidence that TtgV is the specific regulator of the TtgGHI multidrug and solvent efflux pump of Pseudomonas putida. J. Bacteriol. 185 (2003) 4755-4763
17. 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
18. Ramos J.L., Duque E., Godoy P., and Segura A. Efflux pumps involved in toluene tolerance in P. putida DOT-T1E. J. Bacteriol. 180 (1998) 3323-3329
19. Guazzaroni M.E., Terán W., Zhang X., Gallegos M.T., and Ramos J.L. TtgV bound to a complex operator site represses transcription of the single promoter for the multidrug and solvent extrusion TtgGHI pump. J. Bacteriol. 186 (2004) 2921-2927
20. 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
21. Waxman E., Laws W.R., Laue T.M., Nemerson Y., and Ross J. Human factor VIIa and its complex with soluble tissue factor: evaluation of asymmetry and conformational dynamics by ultracentrifugation and fluorescence anisotropy decay methods. Biochemistry 32 (1993) 3005-3012
22. Guazzaroni, M.E., Gallegos, M.T., Ramos, J.L. & Krell, T. (2007) Different modes of binding of mono- and biaromatic effectors to the transcriptional regulator TtgV. Role in differential derepression from its cognate operator. J. Biol. Chem. In the press.
23. Chan A., Kilkuskie R., and Hanlon S. Correlations between the duplex winding angle and the circular dichroism spectrum of calf thymus DNA. Biochemistry 18 (1979) 84-91
24. Woody R.W. Circular dichroism. Methods Enzymol. 246 (1995) 34-71
25. Johnson Jr. W.C. Circular dichroism and its empirical application to biopolymers. Methods Biochem. Anal. 31 (1985) 61-163
26. Guthold M., Bezanilla M., Erie D.A., Jenkins B., Hansma H.G., and Bustamante C. Following the assembly of RNA polymerase-DNA complexes in aqueous solutions with the scanning force microscope. Proc. Natl Acad. Sci. USA 91 (1994) 12927-12931
27. Bustamante C., and Rivetti C. Visualizing protein-nucleic acid interactions on a large scale with the scanning force microscope. Annu. Biophys. Biomol. Struct. 25 (1996) 395-429
28. Hansma H.G. Surface biology of DNA by atomic force microscopy. Annu. Rev. Phys. Chem. 52 (2001) 71-92
29. Erie D.A., Yang G., Schultz H.C., and Bustamante C. DNA bending by Cro protein in specific and nonspecific complexes: implications for protein site recognition and specificity. Science 266 (1994) 1562-1566
30. Seong G.H., Kobatake E., Miura K., Nakazawa A., and Aizawa M. Direct atomic force microscopy visualisation of integration host factor-induced DNA bending stucture of the promoter regulatory region on the Pseudomonas TOL plasmid. Biochem. Biophys. Res. Commun. 291 (2002) 361-366
31. Nomura K., Nasser W., Kawagishi H., and Tsuyumu S. The pir gene of Erwinia chrysanthemi EC16 regulates hyperinduction of pectate lyase virulence genes in response to plant signals. Proc. Natl Acad. Sci. USA 95 (1998) 14034-14039
32. Walker J.R., Altamentova S., Ezersky A., Lorca G., Skarina T., Kudritska M., et al. Structural and biochemical study of effector molecule recognition by the E. coli glyoxylate and allantoin utilization regulatory protein AllR. J. Mol. Biol. 358 (2006) 810-828
33. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78 (2000) 1606-1619
34. Muraoka M., Okumura R., Uragami Y., Nokata T., Ogawa N., Miyashita K., and Senda T. Purification and crystallization of a LysR-type transcriptional regulator CBNR from Ralstonia eutropha NH9. Protein Pept. Letters 10 (2003) 325-329
35. Ogawa N., McFall S., Klem T.J., Miyashita K., and Chakrabarty A.M. Transcriptional activation of the chlorocatechol degradative genes of Ralstonia eutropha NH9. J. Bacteriol. 181 (1999) 6697-6705
36. Kalodimos C.G., Bonvin A.M., Salinas R.K., Wechselberger R., Boelens R., and Kaptein R. Plasticity in protein-DNA recognition: Lac repressor interacts with its natural operator 01 through alternative conformations of its DNA-binding domain. EMBO J. 21 (2002) 2866-2876
37. 15N NMR. J. Mol. Biol. 270 (1997) 496-510
38. Nasser W., Reverchon C., Condemine G., and Robert-Baudouy J. Specific interactions of Erwinia chrysanthemi KdgR repressor with different operators of genes involved in pectinolysis. J. Mol. Biol. 236 (1994) 427-440
39. Chen S., and Calvo J.M. Leucine-induced dissociation of Escherichia coli Lrp hexadecamers to octamers. J. Mol. Biol. 318 (2002) 1031-1042
40. Schleif R. AraC protein: a love-hate relationship. Bioessays 25 (2003) 274-282
41. Vilar J.M., and Saiz L. DNA looping in gene regulation: from the assembly of macromolecular complexes to the control of transcriptional noise. Curr. Opin. Genet. Dev. 15 (2005) 136-144
42. Zwieb C., Kim J., and Adhya S. DNA bending by negative regulatory proteins: Gal and Lac repressors. Genes Dev. 3 (1989) 606-611
43. Travers A.A. DNA conformation and protein binding. Annu. Rev. Biochem. 58 (1989) 427-452
44. García R.A., Bustamante C.J., and Reich N.O. Sequence-specific recognition by cytosine C5 and adenine N6 DNA methyltransferases requires different deformations of DNA. Proc. Natl Acad. Sci. USA 93 (1996) 7618-7622
45. Dickerson R.E., and Chiu T.K. Helix bending as a factor in protein/DNA recognition. Biopolymers 44 (1997) 361-403
46. Schumacher M.A., Choi K.Y., Zalkin H., and Brennan R.G. Crystal structure of LacI member, PurR, bound to DNA: minor groove binding by alpha helices. Science 266 (1994) 763-770
47. Lewis M., Chang G., Horton N.C., Kercher M.A., Pace H.C., Schumacher M.A., et al. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271 (1996) 1247-1254
48. Schumacher M.A., Allen G.S., Diel M., Seidel G., Hillen W., and Brennan R.G. Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P. Cell 118 (2004) 731-741
49. Miwa Y., Nakata A., Ogiwara A., Yamamoto M., and Fujita Y. Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucl. Acids Res. 28 (2000) 1206-1210
50. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179 (1989) 131-137
51. van Holde K.E. Sedimentation. Physical Biochemistry. 2nd edit. (1986), Prentice-Hall, Englewood Cliffs, NJ 110-136
52. Laue T.M., Shah B.D., Ridgeway T.M., and Pelletier S.L. Interpretation of analytical sedimentation data for proteins. In: Harding S.E., Rowe A.J., and Horton J.C. (Eds). Analytical Ultracentrifugation in Biochemistry and Polymer Science (1992), Royal Society of Chemistry, Cambridge, UK 90-125
53. Minton A.P. Conservation of signal: a new algorithm for the elimination of the reference concentration as an independently variable parameter in the analysis of sedimentation equilibrium. In: Schuster T.M., and Laue T.M. (Eds). Modern Analytical Ultracentrifugation (1994), Birkhauser, Boston, MA 81-93
54. Cole J.A. Analysis of heterogeneous interactions. Methods Enzymol. 384 (2004) 212-232
55. Schulz A., Mucke N., Langowski J., and Rippe K. Scanning force microscopy of Escherichia coli RNA polymerase sigma 54 holoenzyme complexes with DNA in buffer and in air. J. Mol. Biol. 283 (1998) 821-836