A novel mode of DNA recognition by a β-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA

EMBO Journal

Volumn 17, Issue 18, 1998, Pages 5484-5496

  Allen, Mark D ^a   Yamasaki, Kazuhiko ^a   Ohme Takagi, Masaru ^a   Tateno, Masaru ^a   Suzuki, Masashi ^a,b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Arabidopsis thaliana; DNA recognition; DNA protein interaction; NMR; Restrained molecular dynamic calculation

Indexed keywords

ARGININE; SUGAR PHOSPHATE; TRYPTOPHAN; VEGETABLE PROTEIN;

ALPHA HELIX; ARABIDOPSIS; ARTICLE; CALCULATION; DNA PROTEIN COMPLEX; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARGININE; DNA, PLANT; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; PLANT PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, SECONDARY; TRYPTOPHAN;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 0032530719     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.18.5484     Document Type: Article

References (67)

1. Babcock, M.S., Pednault, E.P.D. and Olson, W.K. (1994) Nucleic acid structure analysis: mathematics for local Cartesian and helical structure parameters that are truly comparable between structures. J. Mol. Biol., 237, 125-156.
2. 13C enriched proteins. J. Biomol. NMR, 1, 99-104.
3. Benson, D.A., Boguski, M.S., Lipman, D.J. and Ostell, J. (1997) GenBank. Nucleic Acids Res., 25, 1-6.
4. Bernstein, F.C., Koetzle, T.F., Williams, G.J.B., Meyer, E.F. Jr, Brice, M.D., Rodgers, J.R., Kennard, O., Shimanouchi, T. and Tasumi, M. (1977) The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol., 112, 535-542.
5. Billeter, M., Qian, Y.Q., Otting, G., Müller, M., Gehring, W. and Wüthrich, K. (1993) Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol., 234, 1084-1097.
6. Bodenhausen, G. and Ruben, D. (1980) Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett., 569, 185-200.
7. Bowles, D.J. (1990) Defense-related proteins in higher plants. Annu. Rev. Biochem., 59, 873-907.
8. Braunschwieler, L. and Ernst, R.R. (1983) Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson., 53, 521-528.
9. Braunschwieler, L., Bodenhausen, G. and Ernst, R.R. (1983) Analysis of networks of couple spins by multiple quantum NMR. Mol. Phys., 48, 535-560.
10. Breg, J.N., Opheusden, J.H., Burgering, M.J., Boelens, R. and Kaptain, R. (1990) Structure of Arc repressor in solution: evidence for a family of beta-sheet DNA-binding proteins. Nature, 346, 586-589.
11. Brocklehurst, S.M. and Perham, R.N. (1993) Prediction of the three-dimensional structures of the biotinylated domain from yeast pyruvate carboxylase and of the lipoylated H-protein from the pea leaf glycogen cleavage system: a new automated method for the prediction of protein tertiary structure. Protein Sci., 2, 626-639.
12. Brünger, A.T. (1992) X-PLOR Version 3.1: A System for Crystallography and NMR. Yale University Press, New Haven, CT.
13. Brünger, A.T., Clore, G.M., Gronenborn, A.M. and Karplus, M. (1986) Three-dimensional structure of proteins determined by molecular dynamics with interproton distance restraints: application to crambin. Proc. Natl Acad. Sci. USA, 83, 3801-3805.
14. Büttner, M. and Singh, K.B. (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-indelible, GCC box binding protein interacts with an ocs element binding protein. Proc. Natl Acad. Sci. USA, 94, 5961-5966.
15. Chuprina, V.P., Rullmann, J.A.C., Lamerichs, R.M.J.N., Van Boom, J.H., Boelens, R. and 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.
16. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W. and Kollman, P.A. (1995) A second generation force field for the simulation of proteins, nucleic acids and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
17. Darden, T.A., York, D. and Pedersen, L.G. (1993) Particle mesh Ewald: an N log (N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
18. Dutnall, R.N., Neuhaus, D. and Rhodes, D. (1996) The solution structure of the first zinc finger of SWI5: A novel structure extension to a common fold. Structure, 4, 599-611.
19. Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q.J., Generates, D., Perez, P. and Smyth, D.R. (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis thaliana with pleiotropic roles in ovule development and floral organ growth. Plant Cell, 8, 155-168.
20. Fukuoh, A., Iwasaki, H., Ishioka, K. and Shinagawa, H. (1997) ATP-dependent resolution of R-loops at the ColE1 replication origin by Escherichia coli RecG protein, Holliday junction-specific helicase. EMBO J., 16, 203-209.
21. Green, R. and Fluhr, R. (1995) UV-B induced PR-1 accumulation is mediated by active oxygen species. Plant Cell, 7, 203-212.
22. Guenot, J., Fletterick, R.J. and Kollaman, P.A. (1994) A negative electrostatic determinant mediates the association between the Escherichia coli trp repressor and its operator DNA. Protein Sci., 3, 1276-1285.
23. Hammond-Kosack, K.E. and Jones, J.D. (1996) Resistance gene dependent plant defence responses. Plant Cell, 8, 1773-1791.
24. Hegde, R.S., Grossman, S.R., Laimins, L.A. and Sigler, P.B. (1992) Crystal structure at 1.7 Å of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature, 359, 505-512.
25. Ikura, M. and Bax, A. (1992) Isotope-filtered 2D NMR of a protein-peptide complex: study of a skeletal muscle myosin light chain kinase fragment bound to calmodulin. J. Am. Chem. Soc., 114, 2433-2440.
26. 15N spectra of larger proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy; application to calmodulin. Biochemistry, 29, 4659-4667.
27. Janin, J. and Chothia, C. (1980) Packing of alpha-helices onto beta-pleated sheets and the anatomy of alpha/beta proteins. J. Mol. Biol., 143, 95-128.
28. Jeener, J., Meier, B.H., Bachmann, P. and Ernst, R.R. (1979) Investigation of exchange processes to two-dimensional NMR spectroscopy. J. Chem. Phys., 71, 4546-4553.
29. Jofuku, K.D., denBoer, B.G.W., Montagu, M.V. and Okamuro, J.K. (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell, 6, 1211-1225.
30. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926.
31. Kalia, Y.N., Brocklehurst, S.M., Hipps, D.S., Appella, E., Sakaguchi, K. and Perham, R.N. (1993) The high-resolution structure of the peripheral subunit-binding domain of dihydrogenase multienzyme complex of Bacillus stearothermophilus. J. Mol. Biol., 230, 323-341.
32. Klucher, K.M., Chow, H., Reiser, L. and Fischer, R.L. (1996) The AINTEGUMENTA gene of Arabidopsis thaliana required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell, 8, 137-153.
33. Kraulis, P.J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
34. Kuboniwa, H., Grzesiek, S., Delaglio, F. and Bax, A. (1994) Measurement of Hn-Hα J. couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods. J. Biomol. NMR, 4, 871-878.
35. Laskowski, R.A., Rullmann, J.A.C., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
36. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Comm., 113, 967-974.
37. 15N-labeled proteins. J. Am. Chem. Soc., 111, 1515-1517.
38. 15N Hartmann-Hahn-multiple quantum coherence and nuclear overhauser-multiple quantum correlation spectroscopy: application on interleukin 1b. Biochemistry, 28, 6150-6156.
39. Morris, A.L., MacArthur, M.W., Hutchinson, E.G. and Thornton, J.M. (1992) Stereochemical quality of protein structure coordinates. Proteins, 12, 345-364.
40. Neidhardt, F.C., Bloch, P.L. and Smith, D.F. (1974) Culture medium for enterobacteria. J. Bacteriol., 119, 736-747.
41. Nilges, M., Clore, G.M. and Gronenborn, A.M. (1988a) Detennination of the three-dimensional structures of proteins from inter-proton distance data by dynamic simulated annealing from a random array of atoms. FEBS Lett., 239, 129-136.
42. Nilges, M., Gronenborn, A.M., Brünger, A.T. and Clore, G.M. (1988b) Determination of the three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine protease inhibitor 2. Protein Eng., 2, 27-38.
43. Ohme-Takagi, M. and Shinshi, H. (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell, 7, 173-182.
44. Okamuro, J.K., Caster, B., Villarroel, R., Montagu, M.V. and Jofuku, K.D. (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl Acad. Sci. USA, 94, 7076-7081.
45. Omichinski, J.G., Clore, G.M., Schaad, O., Felsenfeld, G., Trainor, C., Appella, E., Stahi, S.J. and Gronenborn, A.M. (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science, 261, 438-446.
46. Omichinski, J.G., Pedone, P.V., Felsenfeld, G., Gronenborn, A.M. and Clore, G.M. (1997) The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nature Struct. Biol., 4, 122-132.
47. 1H]-NMR spectroscopy: combined use with isotope labelling for studies of macromolecular comformation and intermolecular interactions. Quant. Rev. Biophys, 23, 39-96.
48. Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham III, T.E., Ferguson, D.M., Seibel, G.L., Singh, U.C., Weiner, P.K. and Kollman, P.A. (1994) AMBER 4.1. University of California, San Francisco, CA.
49. Powell, M.J.D. (1977) Restart procedures for the conjugate gradient method. Math. Program., 12, 241-254.
50. Raumann, B.E., Rould, M.A., Pabo, C.O. and Sauer, R.T. (1994) DNA recognition by β-sheets in the Arc repressor-operator crystal structure. Nature, 367, 754-757.
51. Rice, P.A., Yang, S., Mizuuchi, K. and Nash, H.A. (1996) Crystal structure of an IHF-DNA complex: a protein-included DNA u-turn. Cell, 87, 1295-1306.
52. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.-Y. and Hunt, M. (1996) Systemic acquired resistance. Plant Cell, 8, 1809-1819.
53. Shaka, A.J., Barker, P.D. and Freeman, R. (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation. J. Magn. Reson., 64, 547-552.
54. Sibanda, B.L., Blundel, T.L. and Thomton, J.M. (1989) Conformation of β-hairpins in protein structures: a systematic classification with applications to modelling by homology, electron density fitting and protein engineering. J. Mol. Biol., 206, 759-777.
55. Somers, W.S. and Phillips, S.E.V. (1992) Crystal structure of the met repressor-operator complex at 2.8 Å resolution reveals DNA recognition by β-strands. Nature, 359, 387-393.
56. Stockinger, E.J., Gilmour, S.J. and Thomashow, M.F. (1997) Arabidopsis thaliana CBFI encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl Acad. Sci. USA, 94, 1035-1040.
57. Suzuki, M. (1995) DNA recognition by a β-sheet. Protein Eng., 8, 1-4.
58. Suzuki, M. and Yagi, N. (1995a) Stereochemical basis of DNA bending by transcription factors. Nucleic Acids Res., 23, 2083-2091.
59. Suzuki, M. and Yagi, N. (1995b) DNA recognition by a β-sheet (2): stereochemical basis of DNA bending by the β-sheets of MetJ and Arc repressors. Proc. Japan Acad., B71, 1108-1113.
60. Suzuki, M. and Yagi, N. (1996) An in-the-groove view of DNA structures in complexes with proteins. J. Mol. Biol., 255, 677-687.
61. Suzuki, M., Amano, N., Kakinuma, J. and Tateno, M. (1997) Use of a 3D structure data base for understanding sequence-dependent conformational aspects of DNA. J. Mol. Biol., 274, 421-434.
62. van Gunsteren, W.F. and Berendsen, H.J.C. (1977) Algorithms for macromolecular dynamics and constraints dynamics. Mol. Phys., 34, 1311-1327.
63. Vis, H., Mariani, M., Vorgias, C.E., Wilson, K.S., Kaptain, R. and Boelens, R. (1995) Solution structure of the HU protein from Bacillus stearothermophilus. J. Mol. Biol., 254, 692-703.
64. Weigel, D. (1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell, 7, 388-389.
65. Werner, H.M., Huth, J.R., Gronenborn, A.M. and Clore, G.M. (1995) Molecular basis of human 46X, Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell, 81, 705-714.
66. Wilson, K., Long, D., Swinburne, J. and Coupland, G. (1996) A dissociation insertion causes a semi-dominant mutant that increases the expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell, 8, 659-671.
67. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids. John Wiley and Sons, New York.