Structural Insights into Nonspecific Binding of DNA by TrmBL2, an Archaeal Chromatin Protein

Journal of Molecular Biology

Volumn 427, Issue 20, 2015, Pages 3216-3229

  Ahmad, Misbha Ud Din ^a   Waege, Ingrid ^b   Hausner, Winfried ^b   Thomm, Michael ^b   Boos, Winfried ^a   Diederichs, Kay ^a   Welte, Wolfram ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Archaea; chromatin protein; nonspecific DNA binding; protein DNA complex; TrmBL2

Indexed keywords

DEOXYRIBOSE; DIMER; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; HELIX LOOP HELIX PROTEIN; NUCLEIC ACID BASE; PHOSPHATE; PROTEIN TRMBL2; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; CHROMATIN; DNA;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PYROCOCCUS FURIOSUS; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHROMATIN; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CHROMATIN; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PYROCOCCUS FURIOSUS; SEQUENCE ALIGNMENT;

EID: 84942363868     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.08.012     Document Type: Article

References (60)

1. S.J. Lee, C. Moulakakis, S.M. Koning, W. Hausner, M. Thomm, and W. Boos TrmB, a sugar sensing regulator of ABC transporter genes in Pyrococcus furiosus exhibits dual promoter specificity and is controlled by different inducers Mol. Microbiol. 57 2005 1797 1807
2. M. Krug, S.J. Lee, W. Boos, K. Diederichs, and W. Welte The three-dimensional structure of TrmB, a transcriptional regulator of dual function in the hyperthermophilic archaeon Pyrococcus furiosus in complex with sucrose Protein Sci. 22 2013 800 808
3. S.J. Lee, M. Surma, S. Seitz, W. Hausner, M. Thomm, and W. Boos Characterization of the TrmB-like protein, PF0124, a TGM-recognizing global transcriptional regulator of the hyperthermophilic archaeon Pyrococcus furiosus Mol. Microbiol. 65 2007 305 318
4. S.-J. Lee, A. Engelmann, R. Horlacher, Q. Qu, G. Vierke, C. Hebbeln, M. Thomm, and W. Boos TrmB, a sugar-specific transcriptional regulator of the trehalose/maltose ABC transporter from the hyperthermophilic archaeon Thermococcus litoralis J. Biol. Chem. 278 2003 983 990
5. A. Gindner, W. Hausner, and M. Thomm The TrmB family: A versatile group of transcriptional regulators in Archaea Extremophiles 18 2014 925 936
6. T. Kanai, J. Akerboom, S. Takedomi, H.J. van de Werken, F. Blombach, J. van der Oost, T. Murakami, H. Atomi, and T. Imanaka A global transcriptional regulator in Thermococcus kodakaraensis controls the expression levels of both glycolytic and gluconeogenic enzyme-encoding genes J. Biol. Chem. 282 2007 33659 33670
7. H.J. van de Werken, C.H. Verhees, J. Akerboom, W.M. de Vos, and J. van der Oost Identification of a glycolytic regulon in the archaea Pyrococcus and Thermococcus FEMS Microbiol. Lett. 260 2006 69 76
8. H. Maruyama, M. Shin, T. Oda, R. Matsumi, R.L. Ohniwa, T. Itoh, K. Shirahige, T. Imanaka, H. Atomi, S.H. Yoshimura, and K. Takeyasu Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis Mol. Biol. Cell 22 2011 386 398
9. A.K. Efremov, Y. Qu, H. Maruyama, C.J. Lim, K. Takeyasu, and J. Yan Transcriptional repressor TrmBL2 from Thermococcus kodakarensis forms filamentous nucleoprotein structures and competes with histones for DNA binding in a salt- and DNA supercoiling-dependent manner J. Biol. Chem. 290 2015 15770 15784
10. K. Sandman, and J.N. Reeve Archaeal histones and the origin of the histone fold Curr. Opin. Microbiol. 9 2006 520 525
11. N. Laurens, R.P. Driessen, I. Heller, D. Vorselen, M.C. Noom, F.J. Hol, M.F. White, R.T. Dame, and G.J. Wuite Alba shapes the archaeal genome using a delicate balance of bridging and stiffening the DNA Nat. Commun. 3 2012 1328
12. E. Peeters, R.P. Driessen, F. Werner, and R.T. Dame The interplay between nucleoid organization and transcription in archaeal genomes Nat. Rev. Microbiol. 13 2015 333 341
13. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268
14. P. Emsley, and K. Cowtan Coot: Model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
15. M. Lewis, G. Chang, N.C. Horton, M.A. Kercher, H.C. Pace, M.A. Schumacher, R.G. Brennan, and P. Lu Crystal structure of the lactose operon repressor and its complexes with DNA and inducer Science 271 1996 1247 1254
16. M.A. Schumacher, K.Y. Choi, H. Zalkin, and R.G. Brennan Crystal structure of LacI member, PurR, bound to DNA: Minor groove binding by alpha helices Science 266 1994 763 770
17. W. Hinrichs, C. Kisker, M. Duvel, A. Muller, K. Tovar, W. Hillen, and W. Saenger Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance Science 264 1994 418 420
18. R.G. Brennan, and B.W. Matthews The helix-turn-helix DNA binding motif J. Biol. Chem. 264 1989 1903 1906
19. A. Vangone, R. Spinelli, V. Scarano, L. Cavallo, and R. Oliva COCOMAPS: A Web application to analyze and visualize contacts at the interface of biomolecular complexes Bioinformatics 27 2011 2915 2916
20. D. Lu, S. Fillet, C. Meng, Y. Alguel, P. Kloppsteck, J. Bergeron, T. Krell, M.T. Gallegos, J. Ramos, and X. Zhang Crystal structure of TtgV in complex with its DNA operator reveals a general model for cooperative DNA binding of tetrameric gene regulators Genes Dev. 24 2010 2556 2565
21. J. Ribeiro, F. Melo, and A. Schuller PDIviz: Analysis and visualization of protein-DNA binding interfaces Bioinformatics 31 2015 2751 2753
22. J.A. Stuckey, and J.E. Dixon Crystal structure of a phospholipase D family member Nat. Struct. Biol. 6 1999 278 284
23. E.V. Koonin A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins Trends Biochem. Sci. 21 1996 242 243
24. C.P. Ponting, and I.D. Kerr A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: Identification of duplicated repeats and potential active site residues Protein Sci. 5 1996 914 922
25. L. Chen, L.R. Chen, X.E. Zhou, Y. Wang, M.A. Kahsai, A.T. Clark, S.P. Edmondson, Z.J. Liu, J.P. Rose, B.C. Wang, E.J. Meehan, and J.W. Shriver The hyperthermophile protein Sso10a is a dimer of winged helix DNA-binding domains linked by an antiparallel coiled coil rod J. Mol. Biol. 341 2004 73 91
26. E.E. Heldwein, and R.G. Brennan Crystal structure of the transcription activator BmrR bound to DNA and a drug Nature 409 2001 378 382
27. S.C. Schultz, G.C. Shields, and T.A. Steitz Crystal structure of a CAP-DNA complex: The DNA is bent by 90 degrees Science 253 1991 1001 1007
28. G.M. Harami, M. Gyimesi, and M. Kovacs From keys to bulldozers: Expanding roles for winged helix domains in nucleic-acid-binding proteins Trends Biochem. Sci. 38 2013 364 371
29. A. Meinhart, J. Blobel, and P. Cramer An extended winged helix domain in general transcription factor E/IIE alpha J. Biol. Chem. 278 2003 48267 48274
30. C. Wolberger, and R. Campbell New perch for the winged helix Nat. Struct. Biol. 7 2000 261 262
31. K.S. Gajiwala, H. Chen, F. Cornille, B.P. Roques, W. Reith, B. Mach, and S.K. Burley Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding Nature 403 2000 916 921
32. R. Amit, A.B. Oppenheim, and J. Stavans Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor Biophys. J. 84 2003 2467 2473
33. Y. Liu, H. Chen, L.J. Kenney, and J. Yan A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes Genes Dev. 24 2010 339 344
34. H. Shindo, T. Iwaki, R. Ieda, H. Kurumizaka, C. Ueguchi, T. Mizuno, S. Morikawa, H. Nakamura, and H. Kuboniwa Solution structure of the DNA binding domain of a nucleoid-associated protein, H-NS, from Escherichia coli FEBS Lett. 360 1995 125 131
35. S.T. Arold, P.G. Leonard, G.N. Parkinson, and J.E. Ladbury H-NS forms a superhelical protein scaffold for DNA condensation Proc. Natl. Acad. Sci. U. S. A. 107 2010 15728 15732
36. Y.G. Gao, S.Y. Su, H. Robinson, S. Padmanabhan, L. Lim, B.S. McCrary, S.P. Edmondson, J.W. Shriver, and A.H. Wang The crystal structure of the hyperthermophile chromosomal protein Sso7d bound to DNA Nat. Struct. Biol. 5 1998 782 786
37. Z. Zhang, L. Guo, and L. Huang Archaeal chromatin proteins Sci. China Life Sci. 55 2012 377 385
38. E.L. Cam, F. Culard, E. Larquet, E. Delain, and J.A. Cognet DNA bending induced by the archaebacterial histone-like protein MC1 J. Mol. Biol. 285 1999 1011 1021
39. M. Crnigoj, Z. Podlesek, M. Zorko, R. Jerala, G. Anderluh, and N.P. Ulrih Interactions of archaeal chromatin proteins Alba1 and Alba2 with nucleic acids PLoS One 8 2013 e58237
40. R.J. DeLange, G.R. Green, and D.G. Searcy A histone-like protein (HTa) from Thermoplasma acidophilum. I. Purification and properties J. Biol. Chem. 256 1981 900 904
41. L. Guo, Y. Feng, Z. Zhang, H. Yao, Y. Luo, J. Wang, and L. Huang Biochemical and structural characterization of Cren7, a novel chromatin protein conserved among Crenarchaea Nucleic Acids Res. 36 2008 1129 1137
42. J.G. McAfee, S.P. Edmondson, I. Zegar, and J.W. Shriver Equilibrium DNA binding of Sac7d protein from the hyperthermophile Sulfolobus acidocaldarius: Fluorescence and circular dichroism studies Biochemistry 35 1996 4034 4045
43. B.S. McCrary, S.P. Edmondson, and J.W. Shriver Hyperthermophile protein folding thermodynamics: Differential scanning calorimetry and chemical denaturation of Sac7d J. Mol. Biol. 264 1996 784 805
44. I. Waege, G. Schmid, S. Thumann, M. Thomm, and W. Hausner Shuttle vector-based transformation system for Pyrococcus furiosus Appl. Environ. Microbiol. 76 2010 3308 3313
45. B. Sommer, I. Waege, D. Pollmann, T. Seitz, M. Thomm, R. Sterner, and W. Hausner Activation of a chimeric Rpb5/RpoH subunit using library selection PLoS One 9 2014 e87485
46. W. Kabsch XDS Acta Crystallogr. D. Biol. Crystallogr. 66 2010 125 132
47. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
48. P.D. Adams, K. Gopal, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.K. Pai, R.J. Read, T.D. Romo, J.C. Sacchettini, N.K. Sauter, L.C. Storoni, and T.C. Terwilliger Recent developments in the PHENIX software for automated crystallographic structure determination J. Synchrotron Radiat. 11 2004 53 55
49. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
50. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
51. J. Painter, and E.A. Merritt Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr. D Biol. Crystallogr. 62 2006 439 450
52. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
53. F. DiMaio, N. Echols, J.J. Headd, T.C. Terwilliger, P.D. Adams, and D. Baker Improved low-resolution crystallographic refinement with Phenix and Rosetta Nat. Methods 10 2013 1102 1104
54. J.M. Duarte, A. Srebniak, M.A. Scharer, and G. Capitani Protein interface classification by evolutionary analysis BMC Bioinf. 13 2012 334
55. R. Lavery, M. Moakher, J.H. Maddocks, D. Petkeviciute, and K. Zakrzewska Conformational analysis of nucleic acids revisited: Curves + Nucleic Acids Res. 37 2009 5917 5929
56. W. Kabsch, and C. Sander Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
57. X. Robert, and P. Gouet Deciphering key features in protein structures with the new ENDscript server Nucleic Acids Res. 42 2014 W320 W324
58. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U. S. A. 98 2001 10037 10041
59. T.J. Dolinsky, J.E. Nielsen, J.A. McCammon, and N.A. Baker PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32 2004 W665 W667
60. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, G. Klebe, and N.A. Baker PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35 2007 W522 W525