Backbone amide dynamics studies of Apo-L75F-TrpR, a temperature-sensitive mutant of the tryptophan repressor protein (TrpR): Comparison with the 15N NMR relaxation profiles of wild-type and A77V mutant Apo-TrpR repressors

Biochemistry

Volumn 49, Issue 37, 2010, Pages 8006-8019

  Goel, Anupam ^a   Tripet, Brian P ^a   Tyler, Robert C ^a,b   Nebert, Lucas D ^a   Copié, Valérie ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; AMINO ACIDS; BINDING ENERGY; DYNAMICS; ESCHERICHIA COLI; MAGNETIC FIELDS; SPECTRAL DENSITY; TENSORS;

APOPROTEINS; BIOPHYSICAL CHARACTERISTICS; CHARACTERISTIC TIME; CHEMICAL EXCHANGE; COREPRESSORS; CORRELATION TIME; DIFFUSION TENSOR; DNA-BINDING DOMAIN; HETERONUCLEAR; INTERNAL DYNAMICS; INTERNAL MOTION; L-TRYPTOPHAN; LARMOR FREQUENCIES; LIGAND BINDING PROPERTIES; MAGNETIC FIELD STRENGTHS; NMR RELAXATION; ORDER PARAMETER; PICOSECONDS; ROTATIONAL DIFFUSION PROPERTIES; TEMPERATURE-SENSITIVE; WILD TYPES;

PROTEINS;

AMIDE; APOPROTEIN; MUTANT PROTEIN; REPRESSOR PROTEIN; TRYPTOPHAN REPRESSOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; TRPR PROTEIN, E COLI; TRYPTOPHAN;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; DNA BINDING; ESCHERICHIA COLI; LIGAND BINDING; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; TEMPERATURE SENSITIVITY; WILD TYPE; CHEMISTRY; DIFFUSION; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN SECONDARY STRUCTURE; TEMPERATURE;

ESCHERICHIA COLI;

AMIDES; APOPROTEINS; BACTERIAL PROTEINS; DIFFUSION; ESCHERICHIA COLI; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN STRUCTURE, SECONDARY; REPRESSOR PROTEINS; TEMPERATURE; TRYPTOPHAN;

EID: 77956602946     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100508u     Document Type: Article

References (77)

1. Joachimiak, A., Kelley, R. L., Gunsalus, R. P., Yanofsky, C., and Sigler, P. B. (1983) Purification and characterization of trp aporepressor Proc. Natl. Acad. Sci. U.S.A. 80, 668-672
2. Sigler, P. B. (1992) Transcriptional Regulation, Cold Spring Harbor Laboratory Press, Plainview, NY.
3. Klig, L. S., Carey, J., and Janofsky, 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
4. Gunsalus, R. P. and Yanofsky, C. (1980) Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp aporepressor Proc. Natl. Acad. Sci. U.S.A. 77, 7117-7121
5. 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
6. 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
7. Carey, J., Lewis, D. E., Lavoie, T. A., and Yang, J. (1991) How does trp repressor bind to its operator? J. Biol. Chem. 266, 24509-24513
8. Lavoie, T. A. and Carey, J. (1994) Adaptability and specificity in DNA binding by trp repressor Nucleic Acid Mol. Biol. 8, 185-196
9. Marmorstein, R. Q., Joachimiak, A., Sprinzl, M., and Sigler, P. B. (1987) The structural basis for the interaction between l -tryptophan and the Escherichia coli trp aporepressor J. Biol. Chem. 262, 4922-4927
10. Luisi, B. F. and Sigler, P. B. (1990) The stereochemistry and biochemistry of the trp repressor-operator complex Biochim. Biophys. Acta 1048, 113-126
11. Yang, J., Gunasekera, A., Lavoie, T. A., Jin, L., Lewis, D. E. A., and Carey, J. (1996) In vivo and in vitro studies of TrpR-DNA interactions J. Mol. Biol. 258, 37-52
12. 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
13. Zhang, R. G., Joachimiak, A., Lawson, C. L., Schevitz, R. W., Otwinowski, Z., and Sigler, P. B. (1987) The crystal structure of trp aporepressor at 1.8 A shows how binding tryptophan enhances DNA affinity Nature 327, 591-597
14. 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
15. Arrowsmith, C., Pachter, R., Altman, R., and Jardetzky, O. (1991) The solution structures of Escherichia coli trp repressor and trp aporepressor at an intermediate resolution Eur. J. Biochem. 202, 53-66
16. Zhao, D., Arrowsmith, C. H., Jia, X., and Jardetzky, O. (1993) Refined solution structures of the Escherichia coli trp holo- and aporepressor J. Mol. Biol. 229, 735-746
17. 15N NMR J. Mol. Biol. 253, 576-589
18. 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
19. 15N NMR relaxation Biochemistry 34, 5212-5223
20. 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
21. 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
22. Bae, S. J., Chou, W. Y., Matthews, K. S., and Sturtevant, J. M. (1988) Tryptophan repressor of E. coli shows unusual thermal stability Proc. Natl. Acad. Sci. U.S.A. 85, 6731-6732
23. Gittelman, M. S. and Matthews, C. R. (1990) Folding and stability of trp aporepressor from Escherichia coli Biochemistry 29, 7011-7020
24. 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
25. 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
26. Chou, W. Y. and Matthews, K. S. (1989) Serine to cysteine mutations in trp repressor protein alter tryptophan and operator binding J. Biol. Chem. 264, 18314-18319
27. Bass, S., Sorrells, V., and Youderian, P. (1988) Mutant Trp repressors with new DNA-binding specificities Science 242, 240-245
28. 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
29. 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
30. 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
31. Marmorstein, R. Q. and Sigler, P. B. (1989) Stereochemical effects of l -tryptophan and its analogues on trp repressors affinity for operator-DNA J. Biol. Chem. 264, 9149-9154
32. Lawson, C. L. (1996) Structural consequences of two methyl additions in the E. coli trp repressor l -tryptophan binding pocket. In Proceedings of the 9th Convention in Biomolecular Stereodynamics (Sarma, R. H. and Sarma, M. H., Ed.) pp 83 - 90, Adenine Press, Schenectady, NY.
33. Bennett, G. N. and Yanofsky, C. (1978) Sequence analysis of operator constitutive mutants of the tryptophan operon of Escherichia coli J. Mol. Biol. 121, 179-192
34. 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
35. Kay, L. E. (1998) Protein dynamics from NMR Biochem. Cell Biol. 76, 145-152
36. Palmer, A. G., Kroenke, C. D., and Loria, J. P. (2001) NMR methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339, 204-238
37. Palmer, A. G. (2001) NMR probes of molecular dynamics: Overview and comparison with other techniques Annu. Rev. Biophys. Biomol. Struct. 30, 129-155
38. Wand, J. A. (2001) Dynamic activation of protein function: A view emerging from NMR spectroscopy Nat. Struct. Biol. 8, 926-931
39. Lee, A. L., Flynn, P. F., and Wand, A. J. (1999) Comparison of H-2 and C-13 NMR relaxation techniques for the study of protein methyl group dynamics in solution J. Am. Chem. Soc. 121, 2891-2902
40. 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
41. Bodenhausen, G. and Ruben, D. J. (1980) Natural Abundance Nitrogen-15 NMR by Enhanced Heteronuclear Spectroscopy Chem. Phys. Lett. 69, 185-189
42. 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
43. 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
44. Kay, L. E., Ikura, M., Tschudin, R., and Bax, A. (1990) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins J. Magn. Reson. 89, 496-514
45. 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
46. 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
47. Goddard, T. D. and Kneller, D. G. (2002) SPARKY 3, University of California, San Francisco.
48. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible Biochemistry 31, 5269-5278
49. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease Biochemistry 28, 8972-8979
50. 2O in Protein NMR J. Am. Chem. Soc. 115, 12593-12594
51. Carr, H. Y. and Purcell, E. M. (1954) Effects of Diffusion on Free Precession in Nuclear Magnetic Resonance Experiments Phys. Rev. 94, 630
52. Meiboom, S. and Gill, D. (1958) Modified Spin-Echo Method for Measuring Nuclear Relaxation Times Rev. Sci. Instrum. 29, 688-691
53. 13C heteronuclear NMR spectroscopy J. Am. Chem. Soc. 113, 4371-4380
54. 13C NMR spectroscopy. Application to the leucine residues of staphylococcal nuclease Biochemistry 31, 5253-5263
55. Bracken, C., Carr, P. A., Cavanagh, J., and Palmer, A. G., III (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
56. Bhattacharya, N., Yi, M., Zhou, H.-X., and Logan, T. M. (2007) Backbone dynamics in an intramolecular prolylpeptide-SH3 complex from the diphteria toxin repressor, DtxR J. Mol. Biol. 374, 977-992
57. 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
58. Blumenschein, T. M. A., Stone, D. B., Fletterick, R. J., Mendelson, R. A., and Sykes, B. A. (2006) Dynamics of the C-terminal region of TnI in the troponin complex in solution Biophys. J. 90, 2436-2444
59. 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
60. Palmer, A. (1998) ModelFree, version 4.0. http://cpmcnet.columbia.edu/ dept/gsas/biochem/labs/palmer.
61. Lipari, G. and Szabo, A. (1982) Model-Free Approach to the Interpretation of Nuclear Magnetic-Resonance Relaxation in Macromolecules. 1. Theory and Range of Validity J. Am. Chem. Soc. 104, 4546-4559
62. Lipari, G. and Szabo, A. (1982) Model-Free Approach to the Interpretation of Nuclear Magnetic-Resonance Relaxation in Macromolecules. 2. Analysis of Experimental Results J. Am. Chem. Soc. 104, 4559-4570
63. 15N relaxation parameters J. Biomol. NMR 20, 149-165
64. 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
65. Peng, J. W. and Wagner, G. (1992) Mapping of the Spectral Densities of N-H Bond Motions in Eglin-C Using Heteronuclear Relaxation Experiments Biochemistry 31, 8571-8586
66. Peng, J. W. and Wagner, G. (1992) Mapping of Spectral Density-Functions Using Heteronuclear NMR Relaxation Measurements J. Magn. Reson. 98, 308-332
67. 15N NMR relaxation Biochemistry 33, 5984-6003
68. Formaneck, M. S., Ma, L., and Cui, Q. (2006) Reconciling the "old" and "new" view of protein allostery: A molecular simulation study of chemotaxis Y protein (chey) Proteins: Struct., Funct., Bioinf. 63, 846-867
69. Karplus, M. and Kuryan, J. (2005) Molecular dynamics and protein function Proc. Natl. Acad. Sci. U.S.A. 102, 6679-6685
70. Kern, D. and Zuiderweg, E. R. P. (2003) The role of dynamics in allosteric regulation Curr. Opin. Struct. Biol. 13, 748-757
71. Popovych, N., Sun, S., Ebright, R. H., and Kalodimos, C. G. (2006) Dynamically driven protein allostery Nat. Struct. Biol. 13, 831-838
72. Clarkson, M. W., Gilmore, S. A., Edgell, M. H., and Lee, A. L. (2006) Dynamic coupling and allosteric behavior in a nonallosteric protein Biochemistry 45, 7693-7699
73. Finucane, M. D. and Jardetzky, O. (2003) Surface plasmon resonance studies of wild-type and AV77 tryptophan repressor resolve ambiguities in super-repressor activity Protein Sci. 12, 1613-1620
74. 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
75. Reedstrom, R. J., Martin, K. S., Vangala, S., Mahoney, S., Wilker, E. W., and Royer, C. A. (1996) Characterization of charge change super-repressor mutants of trp repressor: Effects on oligomerization conformation, ligation and stability J. Mol. Biol. 264, 32-45
76. Grillo, A. O. and Royer, C. A. (2000) The basis for the super-repressor phenotypes of the AV77 and EK18 mutants of trp repressor J. Mol. Biol. 295, 17-28
77. Carey, J. (1988) Gel Retardation at Low pH Resolves trp Repressor-DNA Complexes for Quantitative Study Proc. Natl. Acad. Sci. U.S.A. 85, 975-979