Internal dynamics of the tryptophan repressor (TrpR) and two functionally distinct TrpR variants, L75F-TrpR and A77V-TrpR, in their l -Trp-bound forms

Biochemistry

Volumn 50, Issue 23, 2011, Pages 5140-5153

  Tripet, Brian P ^a   Goel, Anupam ^a   Copié, Valérie ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; BACKBONE DYNAMICS; COMPARISON OF SITES; CONFORMATIONAL DIFFERENCES; DATA SUPPORT; DNA BINDING; DNA RECOGNITION; DNA-BINDING DOMAIN; DNA-BINDING PROTEIN; FUNCTIONAL PROPERTIES; INTERNAL DYNAMICS; L-TRYPTOPHAN; NMR RELAXATION; NUCLEAR OVERHAUSER EFFECTS; PROTEIN FLEXIBILITY;

AMIDES; AMINO ACIDS; DNA; ESCHERICHIA COLI; MAGNETIC DOMAINS; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; RESONANCE; SPECTRAL DENSITY;

PROTEINS;

REPRESSOR PROTEIN; TRYPTOPHAN REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; ESCHERICHIA COLI; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

APOPROTEINS; BINDING SITES; DNA; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HELIX-TURN-HELIX MOTIFS; MAGNETIC RESONANCE SPECTROSCOPY; REPRESSOR PROTEINS; TRYPTOPHAN;

ESCHERICHIA COLI;

EID: 79958825506     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200389k     Document Type: Article

References (63)

1. Klig, L. S., Carey, J., and Yanofsky, C. (1988) Trp repressor interactions with the trp aroH and trpR operators: Comparison of repressor binding in vitro and repression in vivo J. Mol. Biol. 202, 769-777
2. Gunsalus, R. P. and Yanofsky, C. (1980) Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp apo-repressor Proc. Natl. Acad. Sci. U.S.A. 77, 7117-7121 (Pubitemid 11190305)
3. Zurawski, G., Gunsalus, R. P., Brown, K. D., and Yanofsky, C. (1981) Structure and regulation of aroH, the structural gene for the tryptophan-repressible 3-deoxy- d -arabino-heptulosonic acid-7-phosphate synthetase of Escherichia coli J. Mol. Biol. 145, 47-57
4. Sarsero, J. P., Wookey, P. J., and Pittard, A. J. (1991) Regulation and expression of Escherichia coli K-12 mtr gene by TyrR and trp repressor J. Bacteriol. 173, 4133-4143
5. Otwinowski, Z., Schevitz, R. W., Zhang, R. G., Lawson, C. L., Joachimiak, A., Marmorstein, R. Q., Luisi, B. F., and Sigler, P. B. (1988) Crystal structure of trp repressor/operator complex at atomic resolution Nature 335, 321-329
6. Schevitz, R. W., Otwinowski, Z., Joachimiak, A., Lawson, C. L., and Sigler, P. B. (1985) The three-dimensional structure of trp repressor Nature 317, 782-786 (Pubitemid 16195405)
7. Zhang, R. G., Joachimiak, A., Lawson, C. L., Schevitz, R. W., Otwinowski, Z., and Sigler, P. B. (1987) The crystal structure of trp apo-repressor at 1.8 Å shows how binding tryptophan enhances DNA affinity Nature 327, 591-597 (Pubitemid 17086894)
8. Arrowsmith, C., Pachter, R., Altman, R., and Jardetzky, O. (1991) The solution structures of Escherichia coli trp repressor and trp apo-repressor at an intermediate resolution Eur. J. Biochem. 202, 53-66
9. Zhao, D., Arrowsmith, C. H., Jia, X., and Jardetzky, O. (1993) Refined solution structures of the Escherichia coli trp holo- and apo-repressor J. Mol. Biol. 229, 735-746 (Pubitemid 23068048)
10. Joachimiak, A., Kelley, R. L., Gunsalus, R. P., Yanofsky, C., and Sigler, P. B. (1983) Purification and characterization of trp apo-repressor Proc. Natl. Acad. Sci. U.S.A. 80, 668-672
11. Czaplicki, J., Arrowsmith, C., and Jardetzky, O. (1991) Segmental differences in the stability of the trp repressor peptide backbone J. Biomol. NMR 1, 349-361
12. Gryk, M. R., Jardetzky, O., Klig, L. S., and Yanofsky, C. (1996) Flexibility of DNA binding domain of trp repressor required for recognition of different operator sequences Protein Sci. 5, 1195-1197 (Pubitemid 26172910)
13. 15N NMR J. Mol. Biol. 253, 576-589
14. Gryk, M. R., Finucane, M. D., Zheng, Z., and Jardetzky, O. (1995) Solution dynamics of the trp repressor: A study of amide proton exchange by T1 relaxation J. Mol. Biol. 246, 618-627
15. 15N NMR relaxation Biochemistry 34, 5212-5223
16. Zhang, H., Zhao, D., Revington, M., Lee, W., Jia, X., Arrowsmith, C., and Jardetzky, O. (1994) The solution structures of the trp repressor-operator DNA complex J. Mol. Biol. 238, 592-614 (Pubitemid 24160285)
17. Hurlburt, B. K. and Yanofsky, C. (1990) Enhanced operator binding by trp superrepressors of Escherichia coli J. Biol. Chem. 265, 7853-7858
18. Reedstrom, R. J. and Royer, C. A. (1995) Evidence for coupling of folding and function in trp repressor: Physical characterization of the superrepressor mutant AV77 J. Mol. Biol. 253, 266-276
19. Jin, L., Fukayama, J. W., Pelczer, I., and Carey, J. (1999) Long-range effects on dynamics in a temperature-sensitive mutant of trp repressor J. Mol. Biol. 285, 361-378 (Pubitemid 29034050)
20. Tyler, R., Pelczer, I., Carey, J., and Copie, V. (2002) Three-dimensional solution NMR structure of Apo-L75F-TrpR, a temperature-sensitive mutant of the tryptophan repressor protein Biochemistry 41, 11954-11962
21. Gryk, M. R. and Jardetzky, O. (1996) AV77 hinge mutation stabilizes the helix-turn-helix domain of trp repressor J. Mol. Biol. 255, 204-214 (Pubitemid 26104195)
22. Schmitt, T. H., Zheng, Z., and Jardetzky, O. (1995) Dynamics of tryptophan binding to Escherichia coli Trp repressor wild type and AV77 mutant: An NMR study Biochemistry 34, 13183-13189
23. Kelley, R. L. and Yanofsky, C. (1985) Mutational studies with the trp repressor of Escherichia coli support the helix-turn-helix model of repressor recognition of operator DNA Proc. Natl. Acad. Sci. U.S.A. 82, 483-487 (Pubitemid 15128291)
24. 15N NMR relaxation profiles of wild type and A77V mutant TrpR apo-repressors Biochemistry 49, 8006-8019
25. Paluh, J. L. and Yanofsky, C. (1986) High level production and rapid purification of the E. coli trp repressor Nucleic Acids Res. 14, 7851-7860
26. Bodenhausen, G. and Ruben, D. J. (1980) Natural Abundance Nitrogen-15 NMR by Enhanced Heteronuclear Spectroscopy Chem. Phys. Lett. 69, 185-189
27. Wittekind, M. and Mueller, L. (1993) HNCACB, a High-Sensitivity 3D NMR Experiment to Correlate Amide-Proton and Nitrogen Resonances with the α- and β-Carbon Resonances in Proteins J. Magn. Reson., Ser. B 101, 201-205
28. Grzesiek, S. and Bax, A. (1992) Correlating Backbone Amide and Side-Chain Resonances in Larger Proteins by Multiple Relayed Triple Resonance NMR J. Am. Chem. Soc. 114, 6291-6293
29. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A Multidimensional Spectral Processing System Based on Unix Pipes J. Biomol. NMR 6, 277-293
30. Goddard, T. D. and Kneller, D. G. (2002) SPARKY 3, University of California, San Francisco.
31. Pellecchia, M., Sebbel, P., Hermanns, U., Wuthrich, K., and Glockshuber, R. (1999) Pilus chaperone FimC-adhesin FimH interactions mapped by TROSY-NMR Nat. Struct. Biol. 6, 336-339 (Pubitemid 29166481)
32. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible Biochemistry 31, 5269-5278
33. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease Biochemistry 28, 8972-8979 (Pubitemid 19283459)
34. 2O in protein NMR J. Am. Chem. Soc. 115, 12593-12594
35. Shaka, A. J., Keeler, J., and Freeman, R. (1983) Evaluation of A New Broad-Band Decoupling Sequence: Waltz-16 J. Magn. Reson. 53, 313-340
36. 13C NMR spectroscopy. Application to the leucine residues of staphylococcal nuclease Biochemistry 31, 5253-5263
37. Bracken, C., Carr, P. A., Cavanagh, J., and Palmer, A. G. (1999) Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: Implications for the entropy of association with DNA J. Mol. Biol. 285, 2133-2146 (Pubitemid 29078176)
38. Bhattacharya, N., Yi, M., Zhou, H.-X., and Logan, T. M. (2007) Backbone dynamics in an intramolecular prolylpeptide-SH3 complex from the diphtheria toxin repressor, DtxR J. Mol. Biol. 374, 977-992 (Pubitemid 350052089)
39. Lipari, G. and Szabo, A. (1982) ModelFree approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity J. Am. Chem. Soc. 104, 4546-4559
40. Lipari, G. and Szabo, A. (1982) ModelFree approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results J. Am. Chem. Soc. 104, 4559-4570
41. Cole, R. and Loria, J. P. (2003) FAST-model free: A program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26, 203-213 (Pubitemid 36758441)
42. Palmer, A. (1998) ModelFree, version 4.0, http://cpmcnet.columbia.edu/ dept/gsas/biochem/labs/palmer.
43. Mandel, A. M., Akke, M., and Palmer, A. G. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme J. Mol. Biol. 246, 144-163
44. 15N relaxation parameters J. Biomol. NMR 20, 149-165 (Pubitemid 32677758)
45. Tjandra, N., Feller, S. E., Pastor, R. W., and Bax, A. (1995) Rotational diffusion anisotropy of human ubiquitin from N-15 NMR relaxation J. Am. Chem. Soc. 117, 12562-12566
46. 15N glycine]benzyl ester J. Am. Chem. Soc. 110, 2378-2383
47. Farrow, N. A., Zhang, O. W., Szabo, A., Torchia, D. A., and Kay, L. E. (1995) Spectral density function mapping using N-15 relaxation data exclusively J. Biomol. NMR 6, 153-162
48. Peng, J. W. and Wagner, G. (1992) Mapping of spectral density functions using heteronuclear NMR relaxation measurements J. Magn. Reson. 98, 308-332
49. Kay, L. E. (2005) NMR studies of protein structures and dynamics J. Magn. Reson. 173, 193-207 (Pubitemid 40352443)
50. Palmer, A. G. (2004) NMR characterization of the dynamics of biomolecules Chem. Rev. 104, 3623-3640
51. Boehr, D. D., Dyson, J., and Wright, P. E. (2006) An NMR perspective on enzyme dynamics Chem. Rev. 106, 3055-3079 (Pubitemid 44376926)
52. Gardino, A. K. and Kern, D. (2007) Functional dynamics of response regulators using NMR relaxation techniques Methods Enzymol. 423, 149-165 (Pubitemid 46991094)
53. Franzoni, L., Lucke, C., Perz, C., Cavazzini, D., Rademacher, M., Ludwig, C., Spisni, A., and Ruterjans, H. (2002) Structure and backbone dynamics of apo- and holo-cellular retinol-binding protein in solution J. Biol. Chem. 277, 21983-21997 (Pubitemid 34952353)
54. Zhu, L., Hu, J., Whitson, R., Itakura, K., and Chen, Y. (2001) Dynamics of the Mrf-2 DNA-binding domain free and in complex with DNA Biochemistry 40, 9142-9150 (Pubitemid 32730035)
55. Dangi, B., Pelupessey, P., Martin, R. G., Rosner, J. L., Louis, J. M., and Gronenborn, A. M. (2001) Structure and dynamics of MarA-DNA complexes: An NMR investigation J. Mol. Biol. 314, 113-127 (Pubitemid 33097296)
56. Brown, C., Campos-Leon, K., Strickland, M., Williams, C., Fairweather, V., Brady, L. R., Crump, M. P., and Gaston, K. (2011) Protein flexibility directs DNA recognition by the papillomavirus E2 proteins Nucleic Acids Res. 39, 2969-2980
57. Swint-Kruse, L., Zhan, H., Fairbanks, B. M., Maheshwari, A., and Matthews., K. S. (2003) Perturbation from a distance: Mutations that alter LacI function through long-range effects Biochemistry 42, 14004-14016 (Pubitemid 37466626)
58. Xu, J. and Matthews, K. S. (2009) Flexibility in the inducer binding region is crucial for allostery in the Escherichia coli lactose repressor Biochemistry 48, 4988-4998
59. Flynn, T. C., Swint-Kruse, L., Kong, Y., Booth, C., Matthews, K. S., and Ma, J. (2003) Allosteric transition pathways in the lactose repressor protein core domains: Asymmetric motions in a homodimer Protein Sci. 12, 2523-2541 (Pubitemid 37310792)
60. Tretyachenko-Ladokhina, V., Ross, J. B. A., and Senear, D. F. (2002) Thermodynamics of E. coli cytidine repressor interactions with DNA: Distinct modes of binding to different operators suggest a role in differential gene regulation J. Mol. Biol. 316, 531-546 (Pubitemid 34729239)
61. Tretyachenko-Ladokhina, V., Cocco, M. J., and Senear, D. F. (2006) Flexibility and adaptability in binding of E. coli cytidine repressor to different operators suggests a role in differential gene regulation J. Mol. Biol. 362, 271-286 (Pubitemid 44278846)
62. Swint-Kruse, L. and Matthews, K. S. (2009) Allostery in the LacI/GalR family: Variations on a theme Curr. Opin. Microbiol. 12, 129-137
63. Stacklies, W., Xia, F., and Grater, F. (2009) Dynamic allostery in the methionine repressor revealed by force distribution analysis PLoS Comput. Biol. 5, 1-11