Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: Implications for the entropy of association with DNA

Journal of Molecular Biology

Volumn 285, Issue 5, 1999, Pages 2133-2146

  Bracken, Clay ^a   Carr, Peter A ^a   Cavanagh, John ^b   Palmer III, Arthur G ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

Chemical shifts; DNA binding; Dynamics; GCN4; NMR spectroscopy

Indexed keywords

AMIDE; CARBON 13; CARBON MONOXIDE; DNA; LEUCINE; NITROGEN; NITROGEN 15; PEPTIDE; TRANSCRIPTION FACTOR;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DIFFUSION; DNA BINDING; ENTROPY; FREQUENCY ANALYSIS; MOTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; ROTATION; SPECTROMETRY; TEMPERATURE DEPENDENCE; THERMODYNAMICS; YEAST;

EID: 0033525126     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2429     Document Type: Article

References (77)

1. Abragam A. Principles of Nuclear Magnetism. 1961;Clarendon Press, Oxford.
2. 9k. J. Am. Chem. Soc. 115:1993;9832-9833.
3. 15N-labeled proteins. J. Biomol. NMR. 11:1998;451-456.
4. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry. 31:1992;5269-5278.
5. Barkhuijsen H., de Beer R., van Ormondt D. Improved algorithm for noniterative time-domain model fitting to exponentially damped magnetic resonance signals. J. Magn. Reson. 73:1987;553-557.
6. Berger C., Ilian J., Bosshard H. R. Coupled folding and site-specific binding of the GCN4-bZIP transcription factor to the AP-1 and ATF/CREB DNA sites studied by microcalorimetry. Biochemistry. 35:1996;14984-14991.
7. Blanco F. J., Herranz J., Gonzalez C., Jimenez M. A., Rico M., Santoro J., Nieto J. L. NMR chemical shifts: a tool to characterize distortions of peptide and protein helices. J. Am. Chem. Soc. 114:1992;9676-9677.
8. 15N-labeled proteins. J. Biomol. NMR. 9:1997;94-100.
9. Bremi T., Brüschweiler R. Locally anisotropic internal polypeptide backbone dynamics by NMR relaxation. J. Am. Chem. Soc. 119:1997;6672-6673.
10. Chen Y. J., Yang K., Chan K. Determination of the helix and beta form of proteins in aqueous solution by circular dichroism. Biochemistry. 13:1974;3350-3359.
11. Creamer T. P., Rose G. D. Side-chain entropy opposes alpha-helix formation but rationalizes experimentally determined helix-forming propensities. Proc. Natl Acad. Sci. USA. 89:1992;5937-5941.
12. Dill K. A. Theory of folding and stability of globular proteins. Biochemistry. 24:1985;1501-1509.
13. Dill K. A., Alonso D. O. V., Hutchinson K. Thermal stabilities of globular proteins. Biochemistry. 28:1989;5439-5449.
14. Dyson H. J., Wright P. E. Defining solution conformations of small linear peptides. Annu. Rev. Biophys. Biophys. Chem. 20:1991;519-538.
15. Ellenberger T. E., Brandl C. J., Struhl K., Harrison S. C. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α-helices: crystal structure of the protein-DNA complex. Cell. 71:1992;1223-1237.
16. Farrow N. A., Zhang O., Forman-Kay J. D., Kay L. E. Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer. Biochemistry. 34:1995a;868-878.
17. 15N relaxation data exclusively. J. Biomol. NMR. 6:1995b;153-162.
18. Farrow N. A., Zhang O., Forman-Kay J. D., Kay L. E. Characterization of the backbone dynamics of folded and denatured states of an SH3 domain. Biochemistry. 36:1997;2390-2402.
19. Fersht A. R., Serrano L. Principles of protein stability derived from protein engineering experiments. Curr. Opin. Struct. Biol. 3:1993;75-83.
20. Fischer M. W. F., Zeng L., Pang Y., Hu W., Majumdar A., Zuiderweg E. R. P. Experimental characterization of models for backbone picosecond dynamics in proteins. Quantification of NMR auto- and cross-correlation relaxation mechanisms involving different nuclei of the peptide plane. J. Am. Chem. Soc. 119:1997;12629-12642.
21. Grzesiek S., Bax A. Improved 3D triple resonance NMR techniques applied to 31 kDa protein. J. Magn. Reson. 96:1992a;432-440.
22. Grzesiek S., Bax A. Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114:1992b;6291-6293.
23. Harrison S. C., Aggarwal A. K. DNA recognition by proteins with the helix-turn-helix motif. Annu. Rev. Biochem. 59:1990;933-969.
24. 15N] glycine benzyl ester. J. Am. Chem. Soc. 110:1988;2378-2383.
25. Holtzer M. E., Holtzer A., Skolnik J. On realization of the helix-coil theory for protein chains in solutions containing dodecyl sulfate. Experiments on tropomyosin and bovine serum albumin. Macromolecules. 16:1983;173-180.
26. Hope I. A., Struhl K. Functional dissection of a eukaryotic transcriptional activator protein, GCN4 of yeast. Cell. 46:1986;885-894.
27. Hyre D. E., Klevit R. E. A disorder-to-order transition coupled to DNA binding in the essential zinc-finger DNA binding domain of yeast ADR1. J. Mol. Biol. 279:1998;929-943.
28. Ishima R., Nagayama K. Quasi-spectral density function analysis for nitrogen-15 nuclei in proteins. J. Magn. Reson. ser. B. 108:1995;73-76.
29. 13C chemical shifts in the model peptide N-acetyl-N′-methylglycinamide. J. Am. Chem. Soc. 115:1993;10883-10887.
30. 2O saturation. J. Magn. Reson. ser. A. 109:1994;129-133.
31. Kay L. E., Muhandiram D. R., Wolf G., Shoelson S. E., Forman-Kay J. D. Correlation between binding and dynamics at SH2 domain interfaces. Nature Struct. Biol. 5:1998;156-163.
32. König P., Richmond T. J. The X-ray structure of the GCN4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. J. Mol. Biol. 233:1993;139-154.
33. Koradi R., Billiter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
34. 9kstudied by two-dimensional proton-detected NMR spectroscopy. Biochemistry. 31:1992;4856-4866.
35. 1H 2D NMR Spectra by interactive computer graphics. J. Magn. Reson. 84:1989;627-633.
36. Waf1/Cip1/Sid1in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc. Natl Acad. Sci. USA. 93:1996;11504-11509.
37. Kuntz I. D., Kosen P. A., Craig E. C. Amide chemical shifts in many helices in peptides and proteins are periodic. J. Am. Chem. Soc. 113:1991;1406-1408.
38. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 240:1988;1759-1764.
39. 13C alpha nuclear spin relaxation. J. Biomol. NMR. 9:1997;287-298.
40. Lefevre J.-F., Dayie K. T., Peng J. W., Wagner G. Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry. 35:1996;2674-2686.
41. Li Z., Raychaudhuri S., Wand A. J. Insights into the local residual entropy of proteins provided by NMR relaxation. Protein Sci. 5:1996;2647-2650.
42. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104:1982a;4546-4559.
43. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104:1982b;4559-4570.
44. 15N NMR study of gramicidin S in water and organic solvents. J. Am. Chem. Soc. 106:1984;1939-1941.
45. 15N NMR relaxation studies. Biochemistry. 35:1996;4867-4877.
46. Mandel A. M., Akke M., Palmer A. G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246:1995;144-163.
47. Mandel A. M., Akke M., Palmer A. G. Dynamics of ribonuclease H: temperature dependence of motions on multiple time scales. Biochemistry. 35:1996;16009-16023.
48. 15N-labeled proteins. J. Am. Chem. Soc. 111:1989;1515-1517.
49. Oas T. G., McIntosh L. P., O'Shea E. K., Dahlquist F. W., Kim P. S. Secondary structure of a leucine zipper determined by nuclear magnetic resonance spectroscopy. Biochemistry. 29:1990;2891-2894.
50. Oldfield E. Chemical shifts and three-dimensional protein structures. J. Biomol. NMR. 5:1995;217-225.
51. O'Neil K. T., Shuman J. D., Ampe C., DeGrado W. F. DNA-induced increase in the α-helical content of C/EBP and GCN4. Biochemistry. 30:1991;9030-9034.
52. Pabo C. O. Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem. 61:1992;1053-1095.
53. Palmer A. G. Probing molecular motion by NMR. Curr. Opin. Struct. Biol. 7:1997;732-737.
54. Pathak D., Sigler P. B. Updating structure-function relationships in the b-Zip family of transcription factors. Curr. Opin. Struct. Biol. 2:1992;116-123.
55. Peng J. W., Wagner G. Frequency spectrum of NH bonds in eglin c from spectral density mapping at multiple fields. Biochemistry. 34:1995;16733-16752.
56. Pickett S. D., Sternberg M. J. E. Empirical scale of side-chain conformational entropy in protein-folding. J. Mol. Biol. 231:1993;825-839.
57. Rizo J., Gierasch L. M. Constrained peptide: models of bioactive peptides and protein substructures. Annu. Rev. Biochem. 61:1992;387-418.
58. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
59. Saudek V., Pastore A., Morelli M. A. C., Frank R., Gauspohl H., Gibson T., Weih F., Roesch P. Solution structure of the DNA-binding domain of the yeast transcription activator protein GCN4. Protein Eng. 4:1990;3-10.
60. Saudek V., Pasley H. S., Gibson T., Gausepohl H., Frank R., Pastore A. Solution structure of the basic region from the transcriptional activator GCN4. Biochemistry. 30:1991a;1310-1317.
61. Saudek V., Pastore A., Castiglione Morelli M. A., Frank R., Gausepohl H., Gibson T. The solution structure of a leucine-zipper motif peptide. Protein Eng. 4:1991b;519-529.
62. Seerama N., Woody R. A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal. Biochem. 209:1993;32-44.
63. Shaka A. J., Barker P. B., Freeman R. Computer-optimized decoupling scheme for wideband applications and low-level operation. J. Magn. Reson. 64:1985;547-552.
64. 13C NMR. J. Am. Chem. Soc. 116:1994;2500-2507.
65. 15N spin relaxation measurements. J. Magn. Reson. ser. B. 102:1993;253-264.
66. Spolar R. S., Record M. T. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
67. Steitz T. A. Structural studies of protein-nucleic acid interaction: the sources of sequence-specific binding. Quart. Rev. Biophys. 23:1990;205-280.
68. Weiss M. A. Thermal unfolding studies of a leucine zipper domain and its specific DNA complex: implications for scissor's grip recognition. Biochemistry. 29:1990;8020-8024.
69. Weiss M. A., Ellenberger T., Wobbe C. R., Lee J. P., Harrison S. C., Struhl K. Folding transition in the DNA-binding domain of GCN4 on specific binding to DNA. Nature. 347:1990;575-578.
70. Wishart D. S., Sykes B. D., Richards F. M. The chemical shift index: a fast and simple method for the interpretation of protein secondary structure through NMR spectroscopy. Biochemistry. 31:1992;1647-1651.
71. 15N random coil NMR chemical shifts of the common amino acids. I. Investigation of nearest-neighbor effects. J. Biomol. NMR. 5:1995a;67-81.
72. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR. 6:1995b;135-140.
73. Wittekind M., Mueller L. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with alpha- and beta carbon resonances in proteins. J. Magn. Reson. ser. B. 101:1993;201-205.
74. Yang A., Honig B. Free-energy determinants of secondary structure formation. 1. Alpha-helicies. J. Mol. Biol. 252:1995;351-365.
75. Yang D., Kay L. E. Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding. J. Mol. Biol. 263:1996;369-382.
76. Yang D., Mok Y. K., Forman-Kay J. D., Farrow N. A., Kay L. E. Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation. J. Mol. Biol. 272:1997;790-804.
77. Zhou N. E., Zhu B. Y., Sykes B. D., Hodges R. S. Relationship between amide proton chemical shifts and hydrogen bonding in amphipathic α-helical peptides. J. Am. Chem. Soc. 114:1992;4320-4326.