Solution structures of the trihelix DNA-binding domains of the wild-type and a phosphomimetic mutant of Arabidopsis GT-1: Mechanism for an increase in DNA-binding affinity through phosphorylation

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 14, 2010, Pages 3033-3047

  Nagata, Takashi ^a   Niyada, Emi ^a   Fujimoto, Natsuki ^a   Nagasaki, Yuuya ^a   Noto, Kazuaki ^a   Miyanoiri, Youhei ^a   Murata, Jun ^b   Hiratsuka, Kazuyuki ^b   Katahira, Masato ^a,c  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b YOKOHAMA NATIONAL UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

GT 1; NMR; Phosphomimetic mutant; Phosphorylation; Solution structure; Transcription factor; Trihelix DNA binding domain

Indexed keywords

TELOMERIC REPEAT BINDING FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GT1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; BINDING AFFINITY; DNA BINDING MOTIF; DNA PROTEIN COMPLEX; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; TITRIMETRY; WILD TYPE;

AMINO ACID SEQUENCE; ARABIDOPSIS; BINDING SITES; DNA, PLANT; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 77957948557     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22827     Document Type: Article

References (67)

1. Batschauer A. Photoreceptors of higher plants. Planta 1998;206:479-492.
2. Kim JI, Kozhukh GV, Song PS. Phytochrome-mediated signal transduction pathways in plants. Biochem Biophys Res Commun 2002;298:457-463.
3. Mustilli AC, Bowler C. Tuning in to the signals controlling photoregulated gene expression in plants. EMBO J 1997;16:5801-5806.
4. Neuhaus G, Bowler C, Kern R, Chua NH. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 1993;73:937-952.
5. Bowler C, Neuhaus G, Yamagata H, Chua NH. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 1994;77:73-81.
6. Wu Y, Hiratsuka K, Neuhaus G, Chua NH. Calcium and cGMP target distinct phytochrome-responsive elements. Plant J 1996;10:1149-1154.
7. Kuhlemeier C, Fluhr R, Green PJ, Chua NH. Sequences in the pea rbcS3A gene have homology to constitutive mammalian enhancers but function as negative regulatory elements. Genes Dev 1987;1:247-255.
8. Kuhlemeier C, Cuozzo M, Green PJ, Goyvaerts E, Ward K, Chua NH. Localization and conditional redundancy of regulatory elements in rbcS-3A, a pea gene encoding the small subunit of ribulose-bisphosphate carboxylase. Proc Natl Acad Sci USA 1988;85:4662-4666.
9. Green PJ, Kay SA, Chua NH. Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J 1987;6:2543-2549.
10. Green PJ, Yong MH, Cuozzo M, Kano-Murakami Y, Silverstein P, Chua NH. Binding site requirements for pea nuclear protein factor GT-1 correlate with sequences required for light-dependent transcriptional activation of the rbcS-3A gene. EMBO J 1988;7:4035-4044.
11. Gilmartin PM, Chua NH. Localization of a phytochrome-responsive element within the upstream region of pea rbcS-3A. Mol Cell Biol 1990;10:5565-5568.
12. Lam E, Chua NH. GT-1 binding site confers light responsive expression in transgenic tobacco. Science 1990;248:471-474.
13. Hiratsuka K, Wu X, Fukuzawa H, Chua NH. Molecular dissection of GT-1 from Arabidopsis. Plant Cell 1994;6:1805-1813.
14. Zhou DX. Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 1999;4:210-214.
15. Fang Y, Xie K, Hou X, Hu H, Xiong L. Systematic analysis of GT factor family of rice reveals a novel subfamily involved in stress responses. Mol Genet Genomics 2010;283:157-169.
16. Maréchal E, Hiratsuka K, Delgado J, Nairn A, Qin J, Chait BT, Chua NH. Modulation of GT-1 DNA-binding activity by calciumdependent phosphorylation. Plant Mol Biol 1999;40:373-386.
17. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 1995;80:225-236.
18. Tsai KL, Sun YJ, Huang CY, Yang JY, Hung MC, Hsiao CD. Crystal structure of the human FOXO3a-DBD/DNA complex suggests the effects of post-translational modification. Nucleic Acids Res 2007;35:6984-6994.
19. Brownlie P, Ceska T, Lamers M, Romier C, Stier G, Teo H, Suck D. The crystal structure of an intact human Max-DNA complex: new insights into mechanisms of transcriptional control. Structure 1997;5:509-520.
20. Remenyi A, Tomilin A, Pohl E, Lins K, Philippsen A, Reinbold R, Scholer HR, Wilmanns M. Differential dimer activities of the transcription factor Oct-1 by DNA-induced interface swapping. Mol Cell 2001;8:569-580.
21. Pellegrini L, Tan S, Richmond TJ. Structure of serum response factor core bound to DNA. Nature 1995;376:490-498.
22. Smalle J, Kurepa J, Haegman M, Gielen J, Van Montagu M, Van Der Straeten D. The trihelix DNA-binding motif in higher plants is not restricted to the transcription factors GT-1 and GT-2. Proc Natl Acad Sci USA 1998;95:3318-3322.
23. Liu L, White MJ, MacRae TH. Transcription factors and their genes in higher plants functional domains, evolution and regulation. Eur J Biochem 1999;262:247-257.
24. Ito M. Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res 2005;118:61-69.
25. Nagano Y. Several features of the GT-factor trihelix domain resemble those of the Myb DNA-binding domain. Plant Physiol 2000;124:491-494.
26. Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y. 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 1992;89:6428-6432.
27. Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y. Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 1994;79:639-648.
28. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 1995;6:277-293.
29. Kobayashi N, Iwahara J, Koshiba S, Tomizawa T, Tochio N, Guntert P, Kigawa T, Yokoyama S. KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J Biomol NMR 2007;39:31-52.
30. Johnson BA, Blevins RA. NMRView: a computer program for the visualization and analysis of NMR data. J Biomol NMR 1994;4:604-613.
31. Goddard TD, Kneller DG. SPARKY3. San Francisco: University of California; 2004. Available at: http://www.cgl.ucsf.edu/home/sparky.
32. Nagata T, Suzuki S, Endo R, Shirouzu M, Terada T, Inoue M, Kigawa T, Kobayashi N, Guntert P, Tanaka A, Hayashizaki Y, Muto Y, Yokoyama S. The RRM domain of poly(A)-specific ribonuclease has a noncanonical binding site for mRNA cap analog recognition. Nucleic Acids Res 2008;36:4754-4767.
33. Furukawa A, Nagata T, Matsugami A, Habu Y, Sugiyama R, Hayashi F, Kobayashi N, Yokoyama S, Takaku H, Katahira M. Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. EMBO J 2009;28:440-451.
34. Clore GM, Gronenborn AM. Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol 1998;16:22-34.
35. Bax A. Multidimensional nuclear magnetic resonance methods for protein studies. Curr Opin Struct Biol 1994;4:738-744.
36. Cavanagh J, Fairbrother WJ, Palmer AG, III, Skelton NJ. Protein NMR spectroscopy, principles and practice. San Diego, CA: Academic Press; 1996. 587 p.
37. Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, Sykes BD, Wright PE, Wuthrich K. Recommendations for the presentation of NMR structures of proteins and nucleic acids. IUPAC-IUBMBIUPAB Inter-Union Task Group on the Standardization of Data Bases of Protein and Nucleic Acid Structures Determined by NMR Spectroscopy. J Biomol NMR 1998;12:1-23.
38. Mashima T, Matsugami A, Nishikawa F, Nishikawa S, Katahira M. Unique quadruplex structure and interaction of an RNA aptamer against bovine prion protein. Nucleic Acids Res 2009;37:6249-6258.
39. Matsugami A, Okuizumi T, Uesugi S, Katahira M. Intramolecular higher order packing of parallel quadruplexes comprising a G:G:G:G tetrad and a G(:A):G(:A):G(:A):G heptad of GGA triplet repeat DNA. J Biol Chem 2003;278:28147-28153.
40. Mulder FA, Schipper D, Bott R, Boelens R. Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J Mol Biol 1999;292:111-123.
41. Guntert P. Automated NMR structure calculation with CYANA. Methods Mol Biol 2004;278:353-378.
42. Guntert P, Mumenthaler C, Wuthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 1997;273:283-298.
43. Herrmann T, Guntert P, Wuthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 2002;319:209-227.
44. Aitio H, Permi P. Semi-constant-time HMSQC (SCT-HMSQC-HA) for the measurement of (3)J(H(N))(H(alpha)) couplings in (15)Nlabeled proteins. J Magn Reson 2000;143:391-396.
45. Cornilescu G, Delaglio F, Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 1999;13:289-302.
46. Powers R, Garrett DS, March CJ, Frieden EA, Gronenborn AM, Clore GM. The high-resolution, three-dimensional solution structure of human interleukin-4 determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry 1993;32:6744-6762.
47. Guntert P, Braun W, Wuthrich K. Efficient computation of threedimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J Mol Biol 1991;217:517-530.
48. Koradi R, Billeter M, Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 1996;14:51-55.
49. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 1996;8:477-486.
50. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004;60:2256-2268.
51. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 2003;31:3497-3500.
52. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004;25:1605-1612.
53. Meng EC, Pettersen EF, Couch GS, Huang CC, Ferrin TE. Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinformatics 2006;7:339.1-10.
54. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001;98:10037-10041.
55. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 2004;32:W665-W667.
56. Sanner MF, Olson AJ, Spehner JC. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 1996;38:305-320.
57. Dominguez C, Boelens R, Bonvin AM. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 2003;125:1731-1737.
58. de Vries SJ, van Dijk AD, Krzeminski M, van Dijk M, Thureau A, Hsu V, Wassenaar T, Bonvin AM. HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 2007;69:726-733.
59. van Dijk M, van Dijk AD, Hsu V, Boelens R, Bonvin AM. Information-driven protein-DNA docking using HADDOCK: it is a matter of flexibility. Nucleic Acids Res 2006;34:3317-3325.
60. Nilges M, O'Donoghue SI. Ambiguous NOEs and automated NOE assignment. Prog NMR Spectrosc 1998;32:107-139.
61. van Dijk M, Bonvin AM. 3D-DART: a DNA structure modelling server. Nucleic Acids Res 2009;37:W235-W239.
62. Katahira M, Miyanoiri Y, Enokizono Y, Matsuda G, Nagata T, Ishikawa F, Uesugi S. Structure of the C-terminal RNA-binding domain of hnRNP D0 (AUF1), its interactions with RNA and DNA, and change in backbone dynamics upon complex formation with DNA. J Mol Biol 2001;311:973-988.
63. Nagata T, Kanno R, Kurihara Y, Uesugi S, Imai T, Sakakibara S, Okano H, Katahira M. Structure, backbone dynamics and interactions with RNA of the C-terminal RNA-binding domain of a mouse neural RNA-binding protein, Musashi1. J Mol Biol 1999;287:315-330.
64. Luscombe NM, Austin SE, Berman HM, Thornton JM. An overview of the structures of protein-DNA complexes. Genome Biol 2000;1(REVIEWS001):1-37.
65. Gehring WJ, Qian YQ, Billeter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wuthrich K. Homeodomain-DNA recognition. Cell 1994;78:211-23.
66. Wuthrich K. NMR of proteins and nucleic acids. New York: Wiley; 1986. 292 p.
67. Court R, Chapman L, Fairall L, Rhodes D. How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep 2005;6:39-45.