Structural Analysis of the Recognition of the Negative Regulator NmrA and DNA by the Zinc Finger from the GATA-Type Transcription Factor AreA

Journal of Molecular Biology

Volumn 381, Issue 2, 2008, Pages 373-382

  Kotaka, Masayo ^a   Johnson, Christopher ^b   Lamb, Heather K ^b   Hawkins, Alastair R ^b   Ren, Jingshan ^a   Stammers, David K ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

AreA; GATA type; NmrA; protein:protein interactions; zinc fingers

Indexed keywords

DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN; PROTEIN NMRA; TRANSCRIPTION FACTOR GATA; ZINC FINGER PROTEIN;

ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; OXIDATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EMERICELLA NIDULANS; EUKARYOTA;

EID: 47049121925     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.05.077     Document Type: Article

References (43)

1. Hall T.M. Multiple modes of RNA recognition by zinc finger proteins. Curr. Opin. Struct. Biol. 15 (2005) 367-373
2. Matthews J.M., and Sunde M. Zinc fingers-folds for many occasions. IUBMB Life 54 (2002) 351-355
3. Gamsjaeger R., Liew C.K., Loughlin F.E., Crossley M., and Mackay J.P. Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem. Sci. 32 (2007) 63-70
4. Merika M., and Orkin S.H. DNA-binding specificity of GATA family transcription factors. Mol. Cell. Biol. 13 (1993) 3999-4010
5. Omichinski J.G., Clore G.M., Schaad O., Felsenfeld G., Trainor C., Appella E., et al. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 261 (1993) 438-446
6. Trainor C.D., Omichinski J.G., Vandergon T.L., Gronenborn A.M., Clore G.M., and Felsenfeld G. A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol. Cell. Biol. 16 (1996) 2238-2247
7. Cantor A.B., and Orkin S.H. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21 (2002) 3368-3376
8. Liew C.K., Simpson R.J., Kwan A.H., Crofts L.A., Loughlin F.E., Matthews J.M., et al. Zinc fingers as protein recognition motifs: structural basis for the GATA-1/friend of GATA interaction. Proc. Natl Acad. Sci. USA 102 (2005) 583-588
9. Davis M.A., and Hynes M.J. Complementation of areA-regulatory gene mutations of Aspergillus nidulans by the heterologous regulatory gene nit-2 of Neurospora crassa. Proc. Natl Acad. Sci. USA 84 (1987) 3753-3757
10. Fu Y.H., and Marzluf G.A. nit-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. Proc. Natl. Acad. Sci. USA 87 (1990) 5331-5335
11. Marzluf G.A. Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61 (1997) 17-32
12. Platt A., Langdon T., Arst Jr. H.N., Kirk D., Tollervey D., Sanchez J.M., and Caddick M.X. Nitrogen metabolite signalling involves the C-terminus and the GATA domain of the Aspergillus transcription factor AREA and the 3′ untranslated region of its mRNA. EMBO J. 15 (1996) 2791-2801
13. Muro-Pastor M.I., Gonzalez R., Strauss J., Narendja F., and Scazzocchio C. The GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter. EMBO J. 18 (1999) 1584-1597
14. Monahan B.J., Askin M.C., Hynes M.J., and Davis M.A. Differential expression of Aspergillus nidulans ammonium permease genes is regulated by GATA transcription factor AreA. Eukaryot. Cell 5 (2006) 226-237
15. Kudla B., Caddick M.X., Langdon T., Martinez-Rossi N.M., Bennett C.F., Sibley S., et al. The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 9 (1990) 1355-1364
16. Muro-Pastor M.I., Strauss J., Ramon A., and Scazzocchio C. A paradoxical mutant GATA factor. Eukaryot. Cell 3 (2004) 393-405
17. Scazzocchio C. The fungal GATA factors. Curr. Opin. Microbiol. 3 (2000) 126-131
18. Stammers D.K., Ren J., Leslie K., Nichols C.E., Lamb H.K., Cocklin S., et al. The structure of the negative transcriptional regulator NmrA reveals a structural superfamily which includes the short-chain dehydrogenase/reductases. EMBO J. 20 (2001) 6619-6626
19. Lamb H.K., Leslie K., Dodds A.L., Nutley M., Cooper A., Johnson C., et al. The negative transcriptional regulator NmrA discriminates between oxidized and reduced dinucleotides. J. Biol. Chem. 278 (2003) 32107-32114
20. Zheng X., Dai X., Zhao Y., Chen Q., Lu F., Yao D., et al. Restructuring of the dinucleotide-binding fold in an NADP(H) sensor protein. Proc. Natl Acad. Sci. USA 104 (2007) 8809-8814
21. Starich M.R., Wikstrom M., Arst Jr. H.N., Clore G.M., and Gronenborn A.M. The solution structure of a fungal AREA protein-DNA complex: an alternative binding mode for the basic carboxyl tail of GATA factors. J. Mol. Biol. 277 (1998) 605-620
22. Starich M.R., Wikstrom M., Schumacher S., Arst Jr. H.N., Gronenborn A.M., and Clore G.M. The solution structure of the Leu22 → Val mutant AREA DNA binding domain complexed with a TGATAG core element defines a role for hydrophobic packing in the determination of specificity. J. Mol. Biol. 277 (1998) 621-634
23. Lamb H.K., Ren J., Park A., Johnson C., Leslie K., Cocklin S., et al. Modulation of the ligand binding properties of the transcription repressor NmrA by GATA-containing DNA and site-directed mutagenesis. Protein Sci. 13 (2004) 3127-3138
24. Penengo L., Mapelli M., Murachelli A.G., Confalonieri S., Magri L., Musacchio A., et al. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 124 (2006) 1183-1195
25. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
26. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
27. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2256-2268
28. Tjandra N., Omichinski J.G., Gronenborn A.M., Clore G.M., and Bax A. Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 4 (1997) 732-738
29. Lo Conte L., Chothia C., and Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285 (1999) 2177-2198
30. Blankenfeldt W., Kerr I.D., Giraud M.F., McMiken H.J., Leonard G., Whitfield C., et al. Variation on a theme of SDR. dTDP-6-deoxy-l-lyxo-4-hexulose reductase (RmlD) shows a new Mg2+-dependent dimerization mode. Structure 10 (2002) 773-786
31. Allard S.T., Giraud M.F., Whitfield C., Graninger M., Messner P., and Naismith J.H. The crystal structure of dTDP-d-glucose 4,6-dehydratase (RmlB) from Salmonella enterica serovar Typhimurium, the second enzyme in the dTDP-l-rhamnose pathway. J. Mol. Biol. 307 (2001) 283-295
32. Xiao X., Fu Y.H., and Marzluf G.A. The negative-acting NMR regulatory protein of Neurospora crassa binds to and inhibits the DNA-binding activity of the positive-acting nitrogen regulatory protein NIT2. Biochemistry 34 (1995) 8861-8868
33. Wong K.H., Hynes M.J., Todd R.B., and Davis M.A. Transcriptional control of nmrA by the bZIP transcription factor MeaB reveals a new level of nitrogen regulation in Aspergillus nidulans. Mol. Microbiol. 66 (2007) 534-551
34. Small A.J., Todd R.B., Zanker M.C., Delimitrou S., Hynes M.J., and Davis M.A. Functional analysis of TamA, a coactivator of nitrogen-regulated gene expression in Aspergillus nidulans. Mol. Genet. Genomics 265 (2001) 636-646
35. Small A.J., Hynes M.J., and Davis M.A. The TamA protein fused to a DNA-binding domain can recruit AreA, the major nitrogen regulatory protein, to activate gene expression in Aspergillus nidulans. Genetics 153 (1999) 95-105
36. Polotnianka R., Monahan B.J., Hynes M.J., and Davis M.A. TamA interacts with LeuB, the homologue of Saccharomyces cerevisiae Leu3p, to regulate gdhA expression in Aspergillus nidulans. Mol. Genet. Genomics 272 (2004) 452-459
37. Kinghorn J.R., and Pateman J.A. Studies of partially repressed mutants at the tamA and areA loci in Aspergillus nidulans. Mol. Gen. Genet. 140 (1975) 137-147
38. Nichols C.E., Cocklin S., Dodds A., Ren J., Lamb H., Hawkins A.R., and Stammers D.K. Expression, purification and crystallization of Aspergillus nidulans NmrA, a negative regulatory protein involved in nitrogen-metabolite repression. Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 (2001) 1722-1725
39. Walter T.S., Diprose J.M., Mayo C.J., Siebold C., Pickford M.G., Carter L., et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 (2005) 651-657
40. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
41. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
42. Jones T.A., and Kjeldgaard M. Electron-density map interpretation. Methods Enzymol. 277 (1997) 173-208
43. Stuart D.I., Levine M., Muirhead H., and Stammers D.K. Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 Å. J. Mol. Biol. 134 (1979) 109-142