A disorder-to-order transition coupled to DNA binding in the essential zinc-finger DNA-binding domain of yeast ADR1

Journal of Molecular Biology

Volumn 279, Issue 4, 1998, Pages 929-943

  Hyre, David E ^a,b   Klevit, Rachel E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b University of Washington   (United States)

Author keywords

DNA binding protein; Dynamics; NMR spin relaxation; Solvent exchange; Zinc finger

Indexed keywords

FUNGAL DNA; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

AMINO TERMINAL SEQUENCE; ANISOTROPY; ARTICLE; CARBOXY TERMINAL SEQUENCE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; YEAST;

EID: 0032546749     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1811     Document Type: Article

References (62)

1. 2+ binding by calbindin D9k. J. Am. Chem. Soc. 115, 9832-9833.
2. Arrington, C. B. & Robertson, A. D. (1997). Microsecond protein folding kinetics from native-state hydrogen exchange. Biochemistry, 36, 8686-8691.
3. Bai, Y., Milne, J. S., Mayne, L. & Englander, S. W. (1993). Primary structure effects on peptide group hydrogen exchange. Proteins, 17, 75-86.
4. Barbato, G., Ikura, M., Kay, L. E., Pastor, R. W. & Bax, A. (1992). Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry, 31, 5269-5278.
5. 4-histidine zinc finger domain: insights into ADR1-UAS1 protein-DNA recognition. Biochemistry, 33, 4460-4470.
6. Blumberg, H., Eisen, A., Sledziewski, A., Bader, D. & Young, E. T. (1987). Two zinc fingers of a yeast regulatory protein shown by genetic evidence to be essential for its function. Nature, 328, 443-445.
7. Brüschweiler, R., Liao, X. & Wright, P. E. (1995). Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science, 268, 886-889.
8. Cheng, C., Kacherovsky, N., Dombek, K. M., Camier, S., Thukral, S. K., Rhim, E. & Young, E. T. (1994). Identification of potential target genes for Adr1p through characterization of essential nucleotides in UAS1. Mol. Cell. Biol. 14, 3842-3852.
9. 1H NMR spectroscopy. Biochemistry, 29, 7387-7401.
10. Clubb, R. T., Omichinski, J. G., Sakaguchi, K., Appella, E., Gronenborn, A. M. & Clore, G. M. (1995). Backbone dynamics of the oligomerization domain of p53 determined from 15N NMR relaxation measurements. Protein Sci. 4, 855-62.
11. Copié, V., Battles, J. A., Schwab, J. M. & Torchia, D. A. (1996). Secondary structure of beta-hydroxydecanoyl thiol ester dehydrase, a 39-kDa protein, derived from H alpha, C alpha, C beta and CO signal assignments and the chemical shift index: comparison with the crystal structure. J. Biomol. NMR, 7, 335-40.
12. Damaschun, G., Damaschun, H., Gast, K., Misselwitz, R., Muller, J. J., Pfeil, W. & Zirwer, D. (1993). Cold denaturation-induced conformational changes in phosphoglycerate kinase from yeast. Biochemistry, 32, 7739-7746.
13. deLorimier, R., Hellinga, H. W. & Spicer, L. D. (1996). NMR studies of structure, hydrogen exchange, and main-chain dynamics in a disrupted-core mutant of thioredoxin. Protein Sci. 5, 2552-2565.
14. Devore, J. (1982). Probability and Statistics for Engineering and the Physical Sciences, Brooks/Cole Publishing Company, Pacific Grove, CA.
15. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D. & Kay, L. E. (1994). Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry, 33, 5984-6003.
16. Farrow, N. A., Zhang, O., Forman-Kay, J. D. & Kay, L. E. (1995a). Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer. Biochemistry, 34, 868-878.
17. Farrow, N. A., Zhang, O., Szabo, A., Torchia, D. A. & Kay, L. E. (1995b). Spectral density function mapping using 15N relaxation data exclusively. J. Biomol. NMR, 6, 153-162.
18. Folta-Stogniew, E. & Russu, I. M. (1996). Base-catalysis of imino proton exchange in DNA: effects of catalyst upon DNA structure and dynamics. Biochemistry, 35, 8439-8449.
19. Foster, M. P., Wuttke, D. S., Radhakrishnan, I., Case, D. A., Gottesfeld, J. M. & Wright, P. E. (1997). Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIIIA. Nature Struct. Biol. 4, 605-608.
20. 2O in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115, 12593-12594.
21. Habazettl, J., Myers, L. C., Yuan, F., Verdine, G. L. & Wagner, G. (1996). Backbone dynamics, amide hydrogen exchange, and resonance assignments of the DNA methylphosphotriester repair domain of Escherichia coli Ada using NMR. Biochemistry, 35, 9335-9348.
22. Hoffman, R. C., Horvath, S. J. & Klevit, R. E. (1993). Structures of DNA-binding mutant zinc finger domains: implications for DNA binding. Protein Sci. 2, 951-965.
23. Hvidt, A. (1964). A discussion of the pH dependence of the hydrogen-deuterium exchange of proteins. Compt. Rend. Trav. Lab. Carlsberg, 34, 299-317.
24. Ishima, R. & Nagayama, K. (1995). Protein backbone dynamics revealed by quasi spectral density function analysis of amide N-15 nuclei. Biochemistry, 34, 3162-3171.
25. Johnson, M. L. (1994). Use of least-squares techniques in biochemistry. Methods Enzymol. 240, 1-22.
26. Johnston, P. D. & Redfield, A. G. (1978). Pulsed FT-NMR double resonance studies of yeast tRNAPhe: specific nuclear Overhauser effects and reinterpretation of low temperature relaxation data. Nucl. Acids Res. 5, 3913-3927.
27. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
28. Kellermayer, M. S., Smith, S. B., Granzier, H. L. & Bustamante, C. (1997). Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science, 276, 1112-1116.
29. a nuclear spin relaxation. J. Biomol. NMR, 9, 287-298.
30. Lefevre, J. F., Dayie, K. T., Peng, J. W. & Wagner, G. (1996). Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry, 35, 2674-2686.
31. 15N Overhauser effects. J. Magn. Reson. Ser. B, 105, 45-51.
32. Li, Y.-C. & Montelione, G. T. (1995). Human type-alpha transforming growth factor undergoes slow conformational exchange between multiple backbone conformations as characterized by nitrogen-15 relaxation measurements. Biochemistry, 34, 2408-2423.
33. Li, Z., Raychaudhuri, S. & Wand, A. J. (1996). Insights into the local residual entropy of proteins provided by NMR relaxation. Protein Sci. 5, 2647-2650.
34. Lipari, G. & Szabo, A. (1982a). 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.
35. Lipari, G. & Szabo, A. (1982b). 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.
36. 15N spin relaxation studies of protein mobility. Biochemistry, 36, 7305-7312.
37. Markus, M. A., Dayie, K. T., Matsudaira, P. & Wagner, G. (1996). Local mobility within villin 14 T probed via heteronuclear relaxation measurements and a reduced spectral density mapping. Biochemistry, 35, 1722-1732.
38. Nicholson, L. K., Yamazaki, T., Torchia, D. A., Grzesiek, S., Bax, A., Stahl, S. J., Kaufman, J. D., Wingfield, P. T., Lam, P. Y., Jadhav, P. K., Hodge, C. N., Domaille, P. J. & Chang, C. H. (1995). Flexibility and function in HIV-1 protease. Nature Struct. Biol. 2, 274-280.
39. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113, 4371-4380.
40. Párraga, G., Horvath, S., Hood, L., Young, E. T. & Klevit, R. E. (1990). Spectroscopic studies of wild-type and mutant "zinc finger" peptides: determinants of domain folding and structure. Proc. Natl Acad. Sci. USA, 87, 137-141.
41. Pavletich, N. P. & Pabo, C. O. (1991). Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 Å. Science, 252, 809-817.
42. Peng, J. W. & Wagner, G. (1992). Mapping of the spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry, 31, 8571-8586.
43. Peng, J. W. & Wagner, G. (1995). Frequency spectrum of NH bonds in eglin c from spectral density mapping at multiple fields. Biochemistry, 34, 16733-16752.
44. Piotto, M., Saudek, V. & Sklen'ar, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
45. Schmiedeskamp, M. R. & Klevit, R. E. (1994). Zinc finger diversity. Curr. Opin. Struct. Biol. 4, 28-35.
46. Schmiedeskamp, M. R. & Klevit, R. E. (1997). Paramagnetic cobalt as a probe of the orientation of an accessory DNA-binding region of the yeast ADR1 zinc-finger protein. Biochemistry, 36, 14003-14011.
47. Schmiedeskamp, M. R., Rajagopal, P. & Klevit, R. E. (1997). NMR chemical shift perturbation mapping of DNA binding by a zinc-finger domain from the yeast transcription factor ADR1. Protein Sci. 6, 1835-1848.
48. Shuster, J., Yu, J., Cox, D., Chan, R. V., Smith, M. & Young, E. (1986). ADR1-mediated regulation of ADH2 requires an inverted repeat sequence. Mol. Cell. Biol. 6, 1894-1902.
49. Simon, M., Adam, G., Rapatz, W., Spevak, W. & Ruis, H. (1991). The Saccharomyces cerevisiae ADR1 gene is a positive regulator of transcription of genes encoding peroxisomal proteins. Mol. Cell. Biol. 11, 699-704.
50. Slijper, M., Boelens, R., Davis, A. L., Konings, R. N., van-der-Marel, G. A., van-Boom, J. H. & Kaptein, R. (1997). Backbone and side chain dynamics of lac repressor headpiece (1-56) and its complex with DNA. Biochemistry, 36, 249-254.
51. Spera, S., Ikura, M. & Bax, A. (1991). Measurement of the exchange rates of rapidly exchanging amide protons: application to the study of calmodulin and its complex with a myosin light chain kinase fragment. J. Biomol. NMR, 1, 155-165.
52. 15N NMR relaxation measurements. Biochemistry, 31, 4394-4406.
53. Thukral, S. K., Tavianini, M. A., Blumberg, H. & Young, E. T. (1989). Localization of a minimal binding domain and activation regions in yeast regulatory protein ADR1. Mol. Cell. Biol. 9, 2360-2369.
54. Thukral, S. K., Eisen, A. & Young, E. T. (1991a). Two monomers of yeast transcription factor ADR1 bind a palindromic sequence symmetrically to activate ADH2 expression. Mol. Cell. Biol. 11, 1566-1577.
55. Thukral, S. K., Morrison, M. L. & Young, E. T. (1991b). Alanine scanning site-directed mutagenesis of the zinc fingers of transcription factor ADR1: residues that contact DNA and that transactivate. Proc. Natl Acad. Sci. USA, 88, 9188-9192.
56. 15N-NMR relaxation measurements. Eur. J. Biochem. 230, 1014-1024.
57. Tjandra, N., Wingfield, P., Stahl, S. & Bax, A. (1996). Anisotropic rotational diffusion of perdeuterated HIV protease from 15N NMR relaxation measurements at two magnetic fields. J. Biomol. NMR, 8, 273-284.
58. 13C chemical-shift data. J. Biomol. NMR, 4, 171-180.
59. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids, Wiley-Interscience, New York.
60. Xu, R. X., Horvath, S. J. & Klevit, R. E. (1991). ADR1a, a zinc finger peptide, exists in two folded conformations. Biochemistry, 30, 3365-3371.
61. Yang, D., Mok, Y.-K., Forman-Kay, J. D., Farrow, N. A. & Kay, L. E. (1997). Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation. J. Mol. Biol. 272, 790-804.
62. Zink, T., Ross, A., Luers, K., Cieslar, C., Rudolph, R. & Holak, T. A. (1994). Structure and dynamics of the human granulocyte colony-stimulating factor determined by NMR spectroscopy. Loop mobility in a four-helix-bundle protein. Biochemistry, 33, 8453-8463.