Structural classification of HTH DNA-binding domains and protein-DNA interaction modes

Journal of Molecular Biology

Volumn 262, Issue 2, 1996, Pages 294-313

  Wintjens, René ^a   Rooman, Marianne ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Contact patterns; Helix arrangements; HTH motif; Recurrent turn motifs; Structure alignments

Indexed keywords

DNA BINDING PROTEIN; HELIX LOOP HELIX PROTEIN;

ARTICLE; DNA BINDING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN SECONDARY STRUCTURE;

EID: 0030595337     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0514     Document Type: Article

References (90)

1. Aggarwal, A. K., Rodgers, D. W., Drottar, M., Ptashne, M. & Harrison, S. C. (1988). Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science, 242, 899-907.
2. Alard, P. (1991). Computations of surface areas and energies in the field of macromolecules. PhD thesis, Université Libre de Bruxelles, Belgium.
3. Andersen, W. F., Ohlendorf, D. H., Takeda, Y. & Matthews, B. W. (1981). Structure of the cro repressor from bacteriophage lambda and its interaction with DNA. Nature, 290, 754-758.
4. Assa-Munt, N., Mortishire-Smith, R. J., Aurora, R., Herr, W. & Wright, P. E. (1993). The solution structure of the Oct-1 POU-specific domain reveals a striking similarity to the bacteriophage λ repressor DNA-binding domain. Cell, 73, 193-205.
5. Aurora, R., Srinivasan, R. & Rose, G. D. (1994). Rules for the α-helix termination by glycine. Science, 264, 1126-1130.
6. Beamer, L. J. & Pabo, C. O. (1992). Refined 1.8 Å crystal structure of the lambda repressor-operator complex. J. Mol. Biol. 227, 177-196.
7. Bernstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, E. F., Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). The Protein Data Bank: a computed-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
8. 1H nuclear magnetic resonance spectroscopy. J. Mol. Biol. 214, 183-197.
9. Billeter, M., Qian, Y.-Q., Otting, G. Müller, M., Gehring, W. & Wüthrich, K. (1993). Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol. 234, 1084-1097.
10. Boutonnet, N. S. (1995). Comparaisons automatiques des structures tertiaires des protéines par un algorithme de classification à liens multiples. PhD thesis, Université de Paris VI, France.
11. Boutonnet, N. S., Rooman, M. J. & Wodak, S. J. (1995a). Automatic analysis of protein conformational changes by multiple linkage clustering. J. Mol. Biol. 253, 633-647.
12. Boutonnet, N. S., Rooman, M. J., Ochagavia, M.-E., Richelle, J. & Wodak, S. J. (1995b). Optimal protein structure alignments by multiple linkage clustering: application to distantly related proteins. Protein Eng. 8, 647-662.
13. Branden, C. & Tooze, J. (1991). Introduction to Protein Structure, Garland Publishing Co., New York.
14. Brennan, R. G. (1991). Interactions of the helix-turn-helix binding domain. Curr. Opin. Struct. Biol. 1, 80-88.
15. Brennan, R. G. (1992). DNA recognition by the helix-turn-helix motif. Curr. Opin. Struct. Biol. 2, 100-108.
16. Brennan, R. G. (1993). The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell, 74, 773-776.
17. Brennan, R. G. & Matthews, B. W. (1989). The helix-turn-helix DNA binding motif. J. Biol. Chem. 264, 1903-1906.
18. Cerf, C., Lippens, G., Ramakrishnan, V., Muyldermans, S., Segers, A., Wyns, L., Wodak, S. J. & Hallenga, K. (1994). Homo-and heteronuclear two-dimensional NMR studies of the globular domain of histone H1: full assignment, tertiary structure, and comparison with the globular domain of histone H5. Biochemistry, 33, 11079-11086.
19. Ceska, T. A., Lamers, M., Monaci, P., Nicosia, A., Cortese, R. & Suck, D. (1993). The X-ray structure of an atypical homeodomain present in the rat liver transcription factor LFB1/HNF1 and implications for DNA binding. EMBO J. 12, 1805-1810.
20. Chothia, C., Levitt, M. & Richardson, D. (1981). Helix to helix packing in proteins. J. Mol. Biol. 145, 215-250.
21. Chuprina, V. P., Rullmann, J. A. C., Lamerichs, R. M. J. N., van Boom, J. H., Boelens R. & Kaptein, R. (1993). Structure of the complex of lac repressor headpiece and an 11 base-pair half-operator determined by nuclear magnetic resonance spectroscopy and restrained molecular dynamics. J. Mol. Biol. 234, 446-462.
22. Clark, K. L., Halay, E. D., Lai, E. & Burley, S. K. (1993). Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature, 364, 412-420.
23. Clubb, R. T., Omichinski, J. G., Savilahti, H., Mizuuchi, K., Gronenborn, A. M. & Clore, G. M. (1994). A novel class of winged helix-turn-helix protein: the DNA-binding domain of Mu transposase. Structure, 2, 1041-1048.
24. Delhaise, P., Bardiaux, M. & Wodak, S. J. (1984). Interactive computer animation of macromolecules. J. Mol. Graph. 2, 103-106.
25. Damberger, F. F., Pelton, J. G., Liu, C., Cho, H., Harrison, C. J., Nelson, H. C. & Wemmer, D. E. (1995). Refined solution structure and dynamics of the DNA-binding domain of the heat shock factor from Kluyveromyces lactis. J. Mol. Biol. 254, 704-719.
26. Dekker, N., Cox, M., Boelens, R., Verrijzer, C. P., van der Vliet, P. C. & Kaptein, R. (1993). Solution structure of the POU-specific DNA-binding domain of Oct-1. Nature, 362, 852-855.
27. Donaldson, L. W., Petersen, J. M., Graves, B. J. & McIntosh, L. P. (1996). Solution structure of the ets domain from murine ETS-1: a winged helix-turn-helix DNA binding motif. EMBO J. 15, 125-134.
28. Feng, J.-A., Johnson, R. C. & Dickerson, R. E. (1994). Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science, 263, 348-355.
29. Finney, M. (1990). The homeodomain of the transcription factor LFB1 has a 21 amino acid loop between helix 2 and helix 3. Cell, 60, 5-6.
30. 1H NMR spectroscopy. EMBO J. 13, 3936-3944.
31. Goad, W. B. & Kanehisa, M. I. (1982). Pattern recognition in nucleic acid sequences. I. A general method for finding local homologies and symmetries. Nucl. Acids. Res. 10, 247-263.
32. Harper, E. T. & Rose, G. B. (1993). Helix stop signals in proteins and peptides: the capping box. Biochemistry, 32, 7605-7609.
33. Harrison, C. J., Bohm, A. A. & Nelson, H. C. M. (1994). Crystal structure of the DNA binding domain of the heat shock transcription factor. Science, 263, 224-227.
34. Harrison, S. C. (1991). A structural taxonomy of DNA-binding domains. Nature, 353, 715-719.
35. Harrison, S. C. & Aggarwal, A. K. (1990). DNA recognition by proteins with the helix-turn-helix motif. Annu. Rev. Biochem. 59, 933-969.
36. Herr, W., Sturm, R. A., Clerc, R. G., Corcoran, L. M., Baltimore, D., Sharp, P. A., Ingraham, H. A., Rosenfeld, M. G., Finney, M., Ruvkun, G. & Horvitz, H. R. (1988). The POU domain: a large conserved region in the mammalian pit-1, ocf-1, oct-2, and Caenorhabditis elegans unc-86 gene product. Gene Dev. 2, 1513-1516.
37. Holm, L., Sander, C., Ruterjans, H., Schnarr, M., Fogh, R., Boelens, R. & Kaptein, R. (1994). LexA repressor and iron uptake regulator from Escherichia coli: new members of the CAP-like DNA binding domain superfamily. Protein Eng. 7, 1449-1453.
38. Hutchinson, G. E. & Thornton, J. M. (1996). PROMOTF, a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212-220.
39. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure, pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
40. Kissinger, C. R., Liu, B. S., Martin-Blanco, E., Kornberg, T. B. & Pabo, C. O. (1990). Crystal structure of an engrailed homeodomain-DNA complex at 2.8Å resolution: a framework for understanding homeodomain-DNA interactions. Cell, 63, 579-590.
41. Klemm, J. D., Rould, M. A., Aurora, R., Herr, W. & Pabo, C. O. (1994). Crystal structure of the Oct-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules. Cell, 77, 21-32.
42. Kostrewa, D., Granzin, J., Stock, D., Choe, H. W., Labahn, J. & Saenger, W. (1992). Crystal structure of the factor for inversion stimulation FIS at 2.0 Å resolution. J. Mol. Biol. 226, 209-226.
43. Lai, E., Clark, K. L., Burley, S. K. & Darnell, J. E. (1993). Hepatocyte nuclear factor 3/fork head or "winged helix" proteins: a family of transcription factors of diverse biologic function. Proc. Natl Acad. Sci. USA, 90, 10421-10423.
44. Lawson, C. L., Zhang, R., Schevitz, R. W., Otwinowski, Z., Joachimiak, A. & Sigler, P. B. (1988). Flexibility of the DNA-binding domains of trp repressor. Proteins: Struct. Fund. Genet. 3, 18-31.
45. Levitt, M. & Lifson, S. (1969). Refinement of protein conformations using a macromolecular energy minimization procedure. J. Mol. Biol. 46, 269-279.
46. Li, Y., Itadani, H., Sugita, M. & Sugiura, M. (1992). cDNA cloning and sequencing of tobacco chloroplast ribosomal protein L12. FEBS Letters, 300, 199-202.
47. Liang, H., Mao, X., Olejniczak, E. T., Nettesheim, D. G., Yu, L., Meadows, R. P., Thompson, C. B. & Fesik, S. W. (1994). Solution structure of the ets domain of Fli-1 when bound to DNA. Nature Struct. Biol. 1, 871-875.
48. Liu, T., DeRose, E. F. & Mullen, G. P. (1994). Determination of the structure of the DNA-binding domain of γ δ resolvase in solution. Protein Sci. 3, 1286-1295.
49. Matthews, B. W. (1988). No code for recognition. Nature, 335, 294-295.
50. McKay, D. B. & Steitz, T. A. (1981). Structure of catabolite gene activator protein at 2.9 Å resolution suggest binding to left-handed B-DNA. Nature, 290, 744-749.
51. Mizuuchi, K. (1992). Transpositional recombination: mechanistic insights from studies of Mu and other elements. Annu. Rev. Biochem. 61, 1011-1051.
52. Mondragon, A. & Harrison, S. C. (1991). The phage 434 Cro/OR1 complex at 2.5 Å resolution. J. Mol. Biol. 219, 321-334.
53. Mondragon, A., Subbiah, S., Almo, S. C., Drottar, M. & Harrison, S. C. (1989a). Structure of the amino-terminal domain of phage 434 repressor at 2.0 Å resolution. J. Mol. Biol. 205, 189-200.
54. Mondragon, A., Wolberger, C. & Harrison, S. C. (1989b). Structure of phage 434 Cro protein at 2.35 Å resolution. J. Mol. Biol. 205, 179-188.
55. Murzin, A. G., Brenner, S. E., Hubbard, T. & Chothia, C. (1995). SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536-540.
56. Ogata, K., Hojo, H., Aimoto, S., Nakai, T., Nakamura, H., Sarai, A., Ishii, S. & Nishimura, Y. (1992). Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc. Natl Acad. Sci. USA, 89, 6428-6432.
57. Ogata, K., Morikawa, S., Nakamura, H., Sekikawa, A., Inoue, T., Kanai, H., Sarai, A., Ishii, S. & Nishimura, Y. (1994). Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell, 79, 639-648.
58. Otwinowski, Z., Schevitz, R. W., Zhang, R. G., Lawson, C. L., Joachimiak, A., Marmorstein, R. Q., Luisi, B. F. & Sigler, P. B. (1988). Crystal structure of trp repressor/operator complex at atomic resolution. Nature, 335, 321-329.
59. Pabo, C. O. & Lewis, M. (1982). The operator-binding domain of lambda repressor: structure and DNA recognition. Nature, 298, 443-447.
60. Pabo, C. O. & Sauer, R. T. (1984). Protein-DNA recognition. Annu. Rev. Biochem. 53, 293-321.
61. Pabo, C. O. & Sauer, R. T. (1992). Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem. 61, 1053-1095.
62. Qiu, X., Verlinde, C. L., Zhang, S., Schmitt, M. P., Holmes, R. K. & Hol, W. G. (1995). Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors. Structure, 3, 87-100.
63. Ramakrishnan, V., Finch, J. T., Graziano, V., Lee, P. L. & Sweet, R. M. (1993). Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature, 362, 219-223.
64. Rice, P. A. & Steitz, T. A. (1990). Ribosomal protein L7/L12 has a helix-turn-helix motif similar to that found in DNA-binding regulatory proteins. Nucl. Acids Res. 17, 3757-3762.
65. Richards, F. M. (1977). Areas, volumes, packing, and protein structure. Annu. Rev. Biophys. Bioeng. 6, 151-176.
66. Richardson, J. S. & Richardson, D. C. (1988). Helix lap-joints as ion-binding sites, DNA-binding motifs and Ca-binding "EF hands" are related by charge and sequence reversal. Proteins: Struct. Funct. Genet. 4, 229-239.
67. Rooman, M. J., Kocher, J.-P. A. & Wodak, S. J. (1991). Prediction of protein backbone conformation based on seven structure assignments. J. Mol. Biol. 221, 961-979.
68. Rosenfeld, M. G. (1991). POU-domain transcription factors: powerful developmental regulators. Genes Dev. 5, 897-907.
69. Ruvkun, G. & Finney, M. (1991). Regulation of transcription and cell identity by POU domain proteins. Cell, 64, 475-478.
70. L conformation at the ends of helices. In Protein Folding (Jaenicke, R., ed.), pp. 53-61, Elsevier/North-Holland Biomedical Press, New York.
71. Schultz, S. C., Shields, G. C. & Steitz, T. A. (1991). Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science, 253, 1001-1007.
72. Schumacher, M. A., Choi, K. Y., Zalkin, H. & Brennan, R. G. (1994). Crystal structure of lacI member, PurR, bound to DNA: minor groove binding by α helices. Science, 266, 763-770.
73. Seale, J. W., Srinivasan, R. & Rose, G. D. (1994). Sequence determinants of the capping box, a stabilizing motif at the N-termini of alpha-helices. Protein Sci. 3, 1741-1745.
74. Sevilla-Sierra, P., Otting, G. & Wüthrich, K. (1994). Determination of the nuclear magnetic resonance structure of the DNA-binding domain of the P22 c2 repressor (1 to 76) in solution and comparison with the DNA-binding domain of the 434 repressor. J. Mol. Biol. 235, 1003-1020.
75. Strzelecka, T. E., Clore, G. M. & Gronenborn, A. M. (1995). The solution structure of the μ ner protein reveals a helix-turn-helix DNA recognition motif. Structure, 3, 1087-1095.
76. Suzuki, M. (1994). A framework for the DNA-protein recognition code of the probe helix in transcription factors: the chemical and stereochemical rules. Structure, 2, 317-326.
77. Suzuki, M. & Brenner, S. E. (1995). Classification of multi-helical DNA-binding domains and application to predict the DBD structures of σ factor, LysR, OmpR/PhoB, CENP-B, Rap1, and XylS/Ada/AraC. FEBS Letters, 372, 215-221.
78. Swindells, M. B. (1995). Identification of a common fold in the replication terminator protein suggests a possible mode for DNA binding. Trends Biochem. Sci. 20, 300-302.
79. Tsao, D. H. H., Gruschus, J. M., Wang, L.-H., Nirenberg, M. & Ferretti, J. A. (1995). The three-dimensional solution structure of the NK-2 homeodomain from Drosophila. J. Mol. Biol. 251, 297-307.
80. Tullius, T. (1995). Homeodomains: together again for the first time. Structure, 3, 1143-1145.
81. Verrijzer, C. P., Alkema, M. J., van Weperen, W. W., Van Leeuwen, H. C., Strating, M. J. J. & van der Vliet, P. C. (1992). The DNA binding specificity of the bipartite POU domain and its subdomains. EMBO J. 11, 4993-5003.
82. Vuister, G. W., Kim. S.-J., Orosz, A., Marquardt, J., Wu, C. & Bax, A. (1994). Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nature Struct. Biol. 1, 605-614.
83. Werner, M. H., Clore, G. M., Fisher, C. L., Fisher, R. J., Trinh, L., Shiloach, J. & Gronenborn, A. M. (1995). The solution structure of the human ETS1-DNA complex reveals a novel mode of binding and true side chain intercalation. Cell, 83, 761-771.
84. Wilson, D. S., Guenther, B., Desplan, C. & Kuriyan, J. (1995). High resolution crystal structure of a paired (Pax) class cooperative homeodomain dimer on DNA. Cell, 82, 709-719.
85. Wilson, K. P., Shewchuk, L. M., Brennan, R. G., Otsuka, A. J. & Matthews, B. W. (1992). The Escherichia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin and DNA-binding domains. Proc. Natl Acad. Sci. USA, 89, 9257-9261.
86. Wintjens, R. T., Rooman, R. J. & Wodak, S. J. (1996). Automatic classification and analysis of αα-turn motifs in proteins. J. Mol. Biol. 255, 235-253.
87. Wolberger, C. (1996). Homeodomain interactions. Curr. Opin. Struct. Biol. 6, 62-68.
88. Wolberger, C., Vershon, A. K., Liu, B., Johnson, A. D. & Pabo, C. O. (1991). Crystal structure of a MAT alpha 2 homeodomain-operator complex suggest a general model for homeodomain-DNA interactions. Cell, 67, 517-528.
89. Xu, W., Rould, M. A., Jun, S., Desplan, C. & Pabo, C. O. (1995). Crystal structure of a paired domain-DNA complex at 2.5 Å resolution reveals structural basis for Pax developmental mutations. Cell, 80, 639-650.
90. Yura, K., Tomoda, S. & Go, M. (1993). Repeat of helix-turn-helix module in DNA-binding proteins. Protein Eng. 6, 621-628.