An autoinhibited state in the structure of thermotoga maritima NusG

Structure

Volumn 21, Issue 3, 2013, Pages 365-375

  Drögemüller, Johanna ^a   Stegmann, Christian M ^b,e   Mandal, Angshuman ^b   Steiner, Thomas ^c   Burmann, Björn M ^a,f   Gottesman, Max E ^d   Wöhrl, Birgitta M ^a   Rösch, Paul ^a   Wahl, Markus C ^b   Schweimer, Kristian ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d NewYork Presbyterian Hospital   (United States)

^e BAYER PHARMA AG   (Germany)

^f UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN NUSG; RNA POLYMERASE; TRANSCRIPTION TERMINATION FACTOR RHO; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ESCHERICHIA COLI; GENE DELETION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; THERMOTOGA MARITIMA; WILD TYPE;

BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; MOLECULAR DYNAMICS SIMULATION; PEPTIDE ELONGATION FACTORS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; RHO FACTOR; RIBOSOMAL PROTEINS; SPECIES SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMOTOGA MARITIMA; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI; THERMOTOGA MARITIMA;

EID: 84874931200     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.12.015     Document Type: Article

References (40)

1. I. Artsimovitch, and R. Landick Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals Proc. Natl. Acad. Sci. USA 97 2000 7090 7095
2. G.A. Belogurov, M.N. Vassylyeva, V. Svetlov, S. Klyuyev, N.V. Grishin, D.G. Vassylyev, and I. Artsimovitch Structural basis for converting a general transcription factor into an operon-specific virulence regulator Mol. Cell 26 2007 117 129
3. I. Bonin, R. Mühlberger, G.P. Bourenkov, R. Huber, A. Bacher, G. Richter, and M.C. Wahl Structural basis for the interaction of Escherichia coli NusA with protein N of phage lambda Proc. Natl. Acad. Sci. USA 101 2004 13762 13767
4. B.M. Burmann, K. Schweimer, X. Luo, M.C. Wahl, B.L. Stitt, M.E. Gottesman, and P. Rösch A NusE:NusG complex links transcription and translation Science 328 2010 501 504
5. B.M. Burmann, U. Scheckenhofer, K. Schweimer, and P. Rösch Domain interactions of the transcription-translation coupling factor Escherichia coli NusG are intermolecular and transient Biochem. J. 435 2011 783 789
6. B.M. Burmann, S.H. Knauer, A. Sevostyanova, K. Schweimer, R.A. Mooney, R. Landick, I. Artsimovitch, and P. Rösch An α helix to β barrel domain switch transforms the transcription factor RfaH into a translation factor Cell 150 2012 291 303
7. C.M. Burns, and J.P. Richardson NusG is required to overcome a kinetic limitation to Rho function at an intragenic terminator Proc. Natl. Acad. Sci. USA 92 1995 4738 4742
8. E. Burova, S.C. Hung, V. Sagitov, B.L. Stitt, and M.E. Gottesman Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro J. Bacteriol. 177 1995 1388 1392
9. J.H. Cho, V. Muralidharan, M. Vila-Perello, D.P. Raleigh, T.W. Muir, and A.G. Palmer 3rd Tuning protein autoinhibition by domain destabilization Nat. Struct. Mol. Biol. 18 2011 550 555
10. A. Eisenmann, S. Schwarz, S. Prasch, K. Schweimer, and P. Rösch The E. coli NusA carboxy-terminal domains are structurally similar and show specific RNAP- and lambdaN interaction Protein Sci. 14 2005 2018 2029
11. M. Guo, F. Xu, J. Yamada, T. Egelhofer, Y. Gao, G.A. Hartzog, M. Teng, and L. Niu Core structure of the yeast spt4-spt5 complex: a conserved module for regulation of transcription elongation Structure 16 2008 1649 1658
12. J.R. Knowlton, M. Bubunenko, M. Andrykovitch, W. Guo, K.M. Routzahn, D.S. Waugh, D.L. Court, and X. Ji A spring-loaded state of NusG in its functional cycle is suggested by X-ray crystallography and supported by site-directed mutants Biochemistry 42 2003 2275 2281
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. S. Kumar, C.J. Tsai, and R. Nussinov Factors enhancing protein thermostability Protein Eng. 13 2000 179 191
15. N.C. Kyrpides, C.R. Woese, and C.A. Ouzounis KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins Trends Biochem. Sci. 21 1996 425 426
16. J. Li, R. Horwitz, S. McCracken, and J. Greenblatt NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage lambda J. Biol. Chem. 267 1992 6012 6019
17. P. Li, I.R. Martins, G.K. Amarasinghe, and M.K. Rosen Internal dynamics control activation and activity of the autoinhibited Vav DH domain Nat. Struct. Mol. Biol. 15 2008 613 618
18. D. Liao, R. Lurz, B. Dobrinski, and P.P. Dennis A NusG-like protein from Thermotoga maritima binds to DNA and RNA J. Bacteriol. 178 1996 4089 4098
19. S.C. Lovell, I.W. Davis, W.B. Arendall 3rd, P.I. de Bakker, J.M. Word, M.G. Prisant, J.S. Richardson, and D.C. Richardson Structure validation by Calpha geometry: phi,psi and Cbeta deviation Proteins 50 2003 437 450
20. C.D. Mackereth, T. Madl, S. Bonnal, B. Simon, K. Zanier, A. Gasch, V. Rybin, J. Valcárcel, and M. Sattler Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF Nature 475 2011 408 411
21. T.F. Mah, K. Kuznedelov, A. Mushegian, K. Severinov, and J. Greenblatt The alpha subunit of E. coli RNA polymerase activates RNA binding by NusA Genes Dev. 14 2000 2664 2675
22. F.W. Martinez-Rucobo, S. Sainsbury, A.C. Cheung, and P. Cramer Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity EMBO J. 30 2011 1302 1310
23. R.A. Mooney, K. Schweimer, P. Rösch, M.E. Gottesman, and R. Landick Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators J. Mol. Biol. 391 2009 341 358
24. K.E. Nelson, R.A. Clayton, S.R. Gill, M.L. Gwinn, R.J. Dodson, D.H. Haft, E.K. Hickey, J.D. Peterson, W.C. Nelson, and K.A. Ketchum Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima Nature 399 1999 323 329
25. Z. Pasman, and P.H. von Hippel Regulation of rho-dependent transcription termination by NusG is specific to the Escherichia coli elongation complex Biochemistry 39 2000 5573 5585
26. T. Pawson, and P. Nash Protein-protein interactions define specificity in signal transduction Genes Dev. 14 2000 1027 1047
27. T. Pawson, and P. Nash Assembly of cell regulatory systems through protein interaction domains Science 300 2003 445 452
28. M.A. Pufall, and B.J. Graves Autoinhibitory domains: modular effectors of cellular regulation Annu. Rev. Cell Dev. Biol. 18 2002 421 462
29. P. Reay, K. Yamasaki, T. Terada, S. Kuramitsu, M. Shirouzu, and S. Yokoyama Structural and sequence comparisons arising from the solution structure of the transcription elongation factor NusG from Thermus thermophilus Proteins 56 2004 40 51
30. K. Schweimer, S. Prasch, P.S. Sujatha, M. Bubunenko, M.E. Gottesman, and P. Rösch NusA interaction with the α subunit of E. coli RNA polymerase is via the UP element site and releases autoinhibition Structure 19 2011 945 954
31. D.H. Shin, H.H. Nguyen, J. Jancarik, H. Yokota, R. Kim, and S.H. Kim Crystal structure of NusA from Thermotoga maritima and functional implication of the N-terminal domain Biochemistry 42 2003 13429 13437
32. C.L. Squires, J. Greenblatt, J. Li, C. Condon, and C.L. Squires Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentified cellular components Proc. Natl. Acad. Sci. USA 90 1993 970 974
33. T. Steiner, J.T. Kaiser, S. Marinkoviç, R. Huber, and M.C. Wahl Crystal structures of transcription factor NusG in light of its nucleic acid- and protein-binding activities EMBO J. 21 2002 4641 4653
34. S.L. Sullivan, and M.E. Gottesman Requirement for E. coli NusG protein in factor-dependent transcription termination Cell 68 1992 989 994
35. S.L. Sullivan, D.F. Ward, and M.E. Gottesman Effect of Escherichia coli nusG function on lambda N-mediated transcription antitermination J. Bacteriol. 174 1992 1339 1344
36. M. Torres, J.M. Balada, M. Zellars, C. Squires, and C.L. Squires In vivo effect of NusB and NusG on rRNA transcription antitermination J. Bacteriol. 186 2004 1304 1310
37. S. Wenzel, B.M. Martins, P. Rösch, and B.M. Wöhrl Crystal structure of the human transcription elongation factor DSIF hSpt4 subunit in complex with the hSpt5 dimerization interface Biochem. J. 425 2010 373 380
38. F. Werner A nexus for gene expression-molecular mechanisms of Spt5 and NusG in the three domains of life J. Mol. Biol. 417 2012 13 27
39. M. Worbs, G.P. Bourenkov, H.D. Bartunik, R. Huber, and M.C. Wahl An extended RNA binding surface through arrayed S1 and KH domains in transcription factor NusA Mol. Cell 7 2001 1177 1189
40. Y. Zhou, J.J. Filter, D.L. Court, M.E. Gottesman, and D.I. Friedman Requirement for NusG for transcription antitermination in vivo by the lambda N protein J. Bacteriol. 184 2002 3416 3418