Solution Structure of an Archaeal DNA Binding Protein with an Eukaryotic Zinc Finger Fold

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Guillière, Florence ^a,b,c,e   Danioux, Chloé ^a,d   Jaubert, Carole ^a,d   Desnoues, Nicole ^a   Delepierre, Muriel ^a   Prangishvili, David ^a   Sezonov, Guennadi ^a,d   Guijarro, J Iñaki ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIANUS FILAMENTOUS VIRUS 1 PROTEIN 06; DNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC FINGER PROTEIN;

ACIDIANUS HOSPITALIS; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; CRENARCHAEOTA; DNA SEQUENCE; GEL MOBILITY SHIFT ASSAY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; ZINC FINGER MOTIF;

ACIDIANUS; AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; DNA-BINDING PROTEINS; EUKARYOTA; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; VIRAL PROTEINS; ZINC FINGERS;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 84872253945     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052908     Document Type: Article

References (64)

1. Aravind L, Koonin E, (1999) DNA-binding proteins and evolution of transcription regulation in the archaea. Nucleic Acids Res 27: 4658-4670.
2. Bell SD, Jackson SP, (2001) Mechanism and regulation of transcription in archaea. Curr Opin Microbiol 4: 208-213.
3. Armache KJ, Mitterweger S, Meinhart A, Cramer P, (2005) Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J Biol Chem 280: 7131-7134.
4. Hirata A, Klein BJ, Murakami KS, (2008) The X-ray crystal structure of RNA polymerase from Archaea. Nature 451: 851-854.
5. Perez-Rueda E, Janga SC, (2010) Identification and genomic analysis of transcription factors in archaeal genomes exemplifies their functional architecture and evolutionary origin. Mol Biol Evol 27: 1449-1459.
6. Bell SD, (2005) Archaeal transcriptional regulation-variation on a bacterial theme? Trends Microbiol 13: 262-265.
7. Kessler A, Sezonov G, Guijarro JI, Desnoues N, Rose T, et al. (2006) A novel archaeal regulatory protein, Sta1, activates transcription from viral promoters. Nuc Ac Res 34: 4837-4845.
8. Abella M, Rodriguez S, Paytubi S, Campoy S, White MF, et al. (2007) The Sulfolobus solfataricus radA paralogue sso0777 is DNA damage inducible and positively regulated by the Sta1 protein. Nucleic Acids Res 35: 6788-6797.
9. Miller J, McLachlan AD, Klug A, (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. Embo J 4: 1609-1614.
10. Bouhouche N, Syvanen M, Kado CI, (2000) The origin of prokaryotic C2H2 zinc finger regulators. Trends Microbiol 8: 77-81.
11. Brown RS, (2005) Zinc finger proteins: getting a grip on RNA. Curr Opin Struct Biol 15: 94-98.
12. Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP, (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci 32: 63-70.
13. Wolfe SA, Nekludova L, Pabo CO, (2000) DNA recognition by Cys2His2 zinc finger proteins. Annu Rev Biophys Biomol Struct 29: 183-212.
14. Klug A, (2010) The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu Rev Biochem 79: 213-231.
15. Dutnall RN, Neuhaus D, Rhodes D, (1996) The solution structure of the first zinc finger domain of SWI5: a novel structural extension to a common fold. Structure 4: 599-611.
16. Omichinski JG, Pedone PV, Felsenfeld G, Gronenborn AM, Clore GM, (1997) The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat Struct Biol 4: 122-132.
17. Bowers PM, Schaufler LE, Klevit RE, (1999) A folding transition and novel zinc finger accessory domain in the transcription factor ADR1. Nat Struct Biol 6: 478-485.
18. Prangishvili D, Garrett RA, (2004) Exceptionally diverse morphotypes and genomes of crenarchaeal hyperthermophilic viruses. Biochem Soc Trans 32: 204-208.
19. Prangishvili D, Garrett R, Koonin E, (2006) Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 117: 52-67.
20. Guilliere F, Peixeiro N, Kessler A, Raynal B, Desnoues N, et al. (2009) Structure, function, and targets of the transcriptional regulator SvtR from the hyperthermophilic archaeal virus SIRV1. J Biol Chem 284: 22222-22237.
21. Schlenker C, Goel A, Tripet BP, Menon S, Willi T, et al. (2012) Structural studies of E73 from a hyperthermophilic archaeal virus identify the "RH3" domain, an elaborated ribbon-helix-helix motif involved in DNA recognition. Biochemistry 51: 2899-2910.
22. Bettstetter M, Peng X, Garrett RA, Prangishvili D, (2003) AFV1, a novel virus infecting hyperthermophilic archaea of the genus acidianus. Virology 315: 68-79.
23. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T, (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4: 2411-2423.
24. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
25. Johnson BA, Blevins RA, (1994) NMRView: a computer program for the visualisation and analysis of NMR data. J Biomol NMR 4: 603-614.
26. Kay LE, Keifer P, Saarinen T, (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114: 10663-10665.
27. Muhandiram DR, Kay LE, (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J Magn Reson Series B 103: 203-216.
28. Grzesiek S, Anglister J, Bax A, (1993) Correlation of backbone amide and aliphatic side-chain resonances in 13C/15N-enriched proteins by isotropic mixing of 13C magnetization. J Magn Reson Series B 101: 114-119.
29. Logan TM, Olejniczak ET, Xu RX, Fesik SW, (1993) A general method for assigning NMR spectra of denatured proteins using 3D HC(CO)NH-TOCSY triple resonance experiments. J Biomol NMR 3: 225-231.
30. Yamazaki T, Forman-Kay JD, Kay LE, (1993) Two-dimensional NMR experiments for correlating 13Cβ and 1Hδ/ε chemical shifts of aromatic residues in 13C-labeled proteins via scalar couplings. J Am Chem Soc 115: 11054-11055.
31. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, et al. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003.
32. Zhang O, Kay LE, Olivier JP, Forman-Kay D, (1994) Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J Biomol NMR 4: 845-858.
33. Vuister GW, Bax A, (1993) Quantitative J correlation: a new approach for measuring homonuclear three-bond J HNHα coupling constants in 15N enriched proteins. J Am Chem Soc 115: 7772-7777.
34. Grzesiek S, Kuboniwa H, Hinck AP, Bax A, (1995) Multiple-quantum line narrowing for measurement of Hα-Hβ J couplings in isotopically enriched proteins. J Am Chem Soc 117: 5312-5315.
35. Cornilescu G, Delaglio F, Bax A, (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302.
36. Schanda P, Forge V, Brutscher B, (2006) HET-SOFAST NMR for fast detection of structural compactness and heterogeneity along polypeptide chains. Magn Reson Chem 44 Spec No: S177-184.
37. Nilges M, Macias MJ, O'Donoghue SI, Oschkinat H, (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from β-spectrin. J Mol Biol 269: 408-422.
38. Rieping W, Habeck M, Bardiaux B, Bernard A, Malliavin TE, et al. (2007) ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23: 381-382.
39. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Cryst D54: 905-921.
40. Mandel AM, Akke M, Palmer AG, (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J Mol Biol 246: 144-163.
41. Linge JP, Habeck M, Rieping M, Nilges M, (2003) Refinement of protein structures in explicit solvent. Prot: Struct Funct & Genet 50: 496-506.
42. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
43. Hooft RW, Vriend G, Sander C, Abola EE, (1996) Errors in protein structures. Nature 381: 272.
44. Koradi R, Billeter M, Wüthrich K, (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graphics 14: 51-55.
45. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
46. Sharma D, Rajarathnam K, (2000) 13C NMR chemical shifts can predict disulfide bond formation. J Biomol NMR 18: 165-171.
47. Barraud P, Schubert M, Allain FH, (2012) A strong (1)(3)C chemical shift signature provides the coordination mode of histidines in zinc-binding proteins. J Biomol NMR 53: 93-101.
48. Alberts IL, Nadassy K, Wodak SJ, (1998) Analysis of zinc binding sites in protein crystal structures. Protein Sci 7: 1700-1716.
49. Pavletich NP, Pabo CO, (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252: 809-817.
50. Isalan M, Choo Y, Klug A, (1997) Synergy between adjacent zinc fingers in sequence-specific DNA recognition. Proc Natl Acad Sci U S A 94: 5617-5621.
51. Isalan M, Klug A, Choo Y, (1998) Comprehensive DNA recognition through concerted interactions from adjacent zinc fingers. Biochemistry 37: 12026-12033.
52. Wiedenheft B, Stedman K, Roberto F, Willits D, Gleske AK, et al. (2004) Comparative genomic analysis of hyperthermophilic archaeal Fuselloviridae viruses. J Virol 78: 1954-1961.
53. Palm P, Schleper C, Grampp B, Yeats S, McWilliam P, et al. (1991) Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185: 242-250.
54. Stedman KM, She Q, Phan H, Arnold HP, Holz I, et al. (2003) Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res Microbiol 154: 295-302.
55. Peng X, (2008) Evidence for the horizontal transfer of an integrase gene from a fusellovirus to a pRN-like plasmid within a single strain of Sulfolobus and the implications for plasmid survival. Microbiology 154: 383-391.
56. Redder P, Peng X, Brugger K, Shah SA, Roesch F, et al. (2009) Four newly isolated fuselloviruses from extreme geothermal environments reveal unusual morphologies and a possible interviral recombination mechanism. Environ Microbiol 11: 2849-2862.
57. Simpson RJ, Cram ED, Czolij R, Matthews JM, Crossley M, et al. (2003) CCHX zinc finger derivatives retain the ability to bind Zn(II) and mediate protein-DNA interactions. J Biol Chem 278: 28011-28018.
58. Cordier F, Vinolo E, Veron M, Delepierre M, Agou F, (2008) Solution structure of NEMO zinc finger and impact of an anhidrotic ectodermal dysplasia with immunodeficiency-related point mutation. J Mol Biol 377: 1419-1432.
59. Pavletich NP, Pabo CO, (1993) Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261: 1701-1707.
60. Stoll R, Lee BM, Debler EW, Laity JH, Wilson IA, et al. (2007) Structure of the Wilms tumor suppressor protein zinc finger domain bound to DNA. J Mol Biol 372: 1227-1245.
61. Mackay JP, Kowalski K, Fox AH, Czolij R, King GF, et al. (1998) Involvement of the N-finger in the self-association of GATA-1. J Biol Chem 273: 30560-30567.
62. Newton A, Mackay J, Crossley M, (2001) The N-terminal zinc finger of the erythroid transcription factor GATA-1 binds GATC motifs in DNA. J Biol Chem 276: 35794-35801.
63. Liew CK, Simpson RJ, Kwan AH, Crofts LA, Loughlin FE, et al. (2005) Zinc fingers as protein recognition motifs: structural basis for the GATA-1/friend of GATA interaction. Proc Natl Acad Sci U S A 102: 583-588.
64. Feng B, Marzluf GA, (1998) Interaction between major nitrogen regulatory protein NIT2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa. Mol Cell Biol 18: 3983-3990.