Solution structure of the antitermination protein NusB of Escherichia coli: A novel all-helical fold for an RNA-binding protein

EMBO Journal

Volumn 17, Issue 14, 1998, Pages 4092-4100

  Huenges, Martin ^a   Rölz, Christian ^a   Gschwind, Ruth ^a   Peteranderl, Ralph ^a   Berglechner, Fabian ^a   Richter, Gerald ^a   Bacher, Adelbert ^a   Kessler, Horst ^a   Gemmecker, Gerd ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Antitermination; NMR spectroscopy; NusB protein; RNA binding protein; Transcription

Indexed keywords

ARGININE; CARBON 13; DEUTERIUM; NITROGEN 15; RECOMBINANT PROTEIN; RIBOSOME RNA; RNA BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE LAMBDA; ESCHERICHIA COLI; GENE REPLICATION; LYSIS; LYSOGENIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; RNA SYNTHESIS; TORSION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ARGININE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RNA, RIBOSOMAL; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); BACTERIOPHAGE LAMBDA; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 2642680831     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.14.4092     Document Type: Article

References (65)

1. Altieri,A.S., Mazulla,M.J., Zhou,H., Costantino,N., Court,D.L. and Byrd,R.A. (1997) Sequential assignments and secondary structure of the RNA-binding transcriptional regulator NusB, FEBS Lett., 415, 221-226.
2. Banner,D.W., Kokkinidis,M. and Tsernoglou,D. (1987) Structure of the ColE1 rop protein at 1.7 Å resolution. J. Mol. Biol., 196, 657-675.
3. Battiste,J.L., Mao,H., Rao,N.S., Tan,R., Muhandiram,D.R., Kay,L.E., Frankel,A.D. and Williamson,J.R. (1996) a Helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science, 273, 1547-1551.
4. Bax,A. and Grzesiek,S. (1993) Methodological advances in protein NMR. Acc. Chem. Res., 4, 131-138.
5. Bax,A., Ikura,M., Kay,L.E., Torchia,D.A. and Tschudin,R. (1990) Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Magn. Resonance, 86, 304-318.
6. Berglechner,K, Richter,G., Fischer,M., Bacher,A., Gschwind,R.M., Huenges,M., Gemmecker,G. and Kessler,H. (1997) Studies on the NusB protein of Escherichia coli. Expression and determination of secondary-structure elements. Eur. J. Biochem., 248, 338-346.
7. Berglund,H., Rak,A., Serganov,A., Garber,M. and Härd,T. (1997) Solution structure of the ribosomal RNA binding protein S15 from Thermus thermophilus. Nature Struct. Biol., 4, 20-23.
8. Bernstein,F.C., Koetzle,T.F., Williams,G.J., Meyer,E.J., Brice,M.D., Rodgers,J.R., Kennard,O., Shimanouchi,T. and Tasumi,M. (1977) Protein Data Bank: a computer based archival file for macromolecular structures. J. Mol. Biol., 112, 535-542.
9. Biamonti,G. and Riva,S. (1994) New insights into the auxiliary domains of eukaryotic RNA binding proteins. FEBS Lett., 340, 1-8.
10. Biou,V., Shu,F. and Ramakrishmin,V. (1995) X-ray crystallography shows that translational iniation factor IF3 consists of two compact α/β domains linked by an α helix. EMBO J., 14, 4056-4064.
11. Brünger,A.T. (1992) X-PLOR Manual. Version 3.1. Yale University Press, Cambridge, MA.
12. Burd,C.G. and Dreyfuss,G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
13. Bycroft,M., Grünert, S., Murzin,A.G., Proctor,M. and St Johnston,D. (1995) NMR solution structure of a dsRNA binding domain from Drosophilia staufen protein reveals homology to the N-terminal domain of ribosomal protein S5. EMBO J., 14, 3563-3571.
14. Cai,Z., Gorin,A., Frederick,R. Ye,X., Hu,W., Majumdar,A., Kettani,A. and Patel,J.D. (1998) Solution structure of P22 transcriptional antitermination N peptide-box B RNA complex. Nature Struct. Biol., 5, 203-212.
15. Calnan,B.J., Biancalana,S., Hudson,D. and Frankel,A.D. (1991) Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features for RNA-protein recognition. Genes Dev., 5, 201-210.
16. Cheng,S.W., Lynch,E.C., Leason,K.R., Court,D.L., Shapiro,B.A. and Friedman,D.I. (1991) Functional importance of sequence in the stem-loop of a transcription terminator. Science, 254, 1205-1207.
17. 13C-edited nuclear Overhauser enhancement spectroscopy of a protein in solution: application to interleukin 1β. Biochemistry, 30, 12-18.
18. Court,D.L., Patterson,T.A., Baker,T., Constantino,N., Mao,X. and Friedman,D.I. (1995) Structural and functional analyses of the transcription-translation proteins NusB and NusE. J. Bacteriol., 9, 2589-2591.
19. DeVito,J. and Das,A. (1994) Control of transition processivity in phage λ: Nus factors strengthen the termination-resistant state of RNA polymerase induced by N antiterminator. Proc. Natl Acad. Sci. USA, 91, 8660-8664.
20. Eberle,W., Pastore,A., Sander,C. and Rösch,P. (1991) The structure of ColE1 rop in solution. J. Biomol. NMR, 1, 71-82.
21. Friedman,D.I., Sauer,A.T., Baumann,M.R., Baron,L.S. and Adhya,S.L. (1981) Evidence that ribosomal protein S10 participates in the control of transcription termination. Proc. Natl Acad. Sci. USA, 78, 1115-1118.
22. Gaal,T., Bartlett,M.S., Ross,W., Turnbough,C.L. and Gaurse,R.L. (1997) Transcription regulation by initiating NTP concentration: rRNA Synthesis in bacteria. Science, 278, 2092-2097.
23. Garcia,C., Fortier,P.-L., Blanquet,S., Lallemand,J.-Y. and Dardel,F. (1995) Solution structure of the ribosome-binding domain of E.coli translation initiation factor IF3. Homology with the U1A protein of the eukaryotic spliceosome. J. Mol. Biol., 254, 247-259.
24. Gemmecker,G., Jahnke,W. and Kessler,H. (1993) Measurement of fast proton exchange rates in isotopically labeled compounds. J. Am. Chem. Soc., 115, 11620-11621.
25. 15N-enriched proteins. Application to HIV-1 Nef. J. Am. Chem. Soc., 117, 9594-9595.
26. Harada,K., Martin,S.S. and Frankel,A.D. (1996) Selection of RNA binding peptides in vivo. Nature, 380, 175-179.
27. Hoffmann,D.W., Query,C.C., Golden,B.L., White,S.W. and Keene,J.D. (1991) RNA-binding domain of the A protein component of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins. Proc. Natl Acad. Sci. USA, 83, 2495-2499.
28. Holm,L. and Sander,C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
29. 13C-labelled protein. J. Magn. Resonance, 86, 204-209.
30. Kang,C.-H,. Chan,R, Berger,I., Lockshin,C., Green,L., Gold,L. and Rich,A. (1995) Crystal structure of the T4 regA translational regulator protein at 1.9 Å resolution. Science, 268, 1170-1173.
31. Karn,J. and Graeble,A. (1992) New insights into the mechanism of HIV- 1 trans-activation. Trends Genet., 8, 365-368.
32. Kay,L.E., Clore,G.M., Bax,A. and Gronenborn,A.M. (1990) Four-dimensional heteronuclear triple-resonance NMR-spectroscopy of interleukin-1β in solution. Science, 249, 411-414.
33. Keener,J. and Nomura,M. (1996) Regulation of ribosome synthesis. In Neidhurdt,F.C., Ingraham,J.L., Low,K.B., Magasanik,B., Schaecher,M. and Umbarger,H.E. (eds), Cellular and Molecular Biology. American Society for Microbiology, Washington, DC, pp. 822-848.
34. Kharrat,A., Macias,M.J., Gibson,T.J., Nilges,M. and Pastore,A. (1995) Structure of the dsRNA binding domain of E.coli RNase III. EMBO J., 14, 3572-3584.
35. Lazinski,D., Grzadienska,E. and Das,A. (1989) Sequence-specific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif. Cell, 59, 207-218.
36. Laskowski,R.A., Rullmann,J.A.C., MacArthur,M.W., Kaptein,R. and Thornton,J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
37. Liljas,A. and Garber,M. (1995) Ribosomal proteins and elongation factors. Curr. Opin. Struct. Biol., 5, 721-727.
38. 2NCO-E.COSY. a simple method for the stereospecific assignment of side-chain amide protons in proteins. J. Magn. Resonance, 124, 255-258.
39. Markus,M.A., Hinck,A.R, Huang,S. and Draper,D.E. (1997) High resolution solution structure of ribosomal protein L11-C76, a helical protein with a flexible loop that becomes structured upon binding to RNA. Nature Struct. Biol., 4, 70-77.
40. Mason,S., Li,J. an Greenblatt,J. (1992) A direct interaction between two Escherichia coli transcription antitermination factors. NusB and ribosomal protein S10. J. Mol. Biol., 223, 55-66.
41. Mogridge,J., Mah,T.-F. and Greenblatt,J. (1995). A protein-RNA interaction network facilitates the template-independent cooperative assembly on RNA polymerase of a stable antitermination complex containing the λ N protein. Genes Dev., 9, 2831-2841.
42. Musco,G., Stier,G., Joseph,C., Castiglione Morelli,M.A., Nilges,M., Gibson,T.J. and Pastore,A. (1996) Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell, 85, 237-245.
43. Nagai,K. (1996) RNA-protein complexes. Curr. Opin. Struct. Biol., 6, 53-61.
44. Nagai,K., Oubridge,C., Jessen,T.H., Li,J. and Evans,P.R. (1990) Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature, 348, 515-520.
45. 13C-labeling. Biochemistry, 28, 7510-7516.
46. Nilges,M., dore,G.M. and Gronenborn,A.M. (1988) Determination of three-dimensional structures of proteins from interproton distance data by dynamic simulated annealing from a random array of atoms. FEBS Lett., 239, 129-136.
47. Nilges,M., Kuszewski,J. and Brünger,A.T. (1991) Sampling properties of simulated annealing and distance geometry. In Hoch,J.C., Poulsen,F.M. and Redfield,C. (eds), Computational Aspects of the Study of Biological Macromolecules by Nuclear Magnetic Resonance Spectroscopy. Plenum Press, New York, NY, pp. 451-456.
48. Nodwell,J.R. and Greenblatt,J. (1991) The nut site of bacteriophage λ is made of RNA and is bound by transcription antitermination factors on the surface of RNA polymerase. Genes Dev., 5, 2141-2151.
49. Nodwell,J.R. and Greenblatt,J. (1993) Recognition of boxA antiterminator RNA by the E.coli antitermination factors NusB and ribosomal protein S10. Cell, 72, 261-268.
50. Puglisi,J.D., Chen,L., Blanchard,S. and Frankel,A.D. (1995) Solution structure of a bovine immunodeficency virus Tat-TAR peptide RNA complex. Science, 270, 1200-1203.
51. Richardson,J.P. and Greenblatt,J. (1996) Control of RNA chain elongation and termination in Eschericha coli and Salmonella typhimurium. In Neidhardt,F.C., Ingraham,J.L., Low,K.B., Magasanik,B., Schaecher,M. and Umbarger,H.E. (eds), Cellular and Molecular Biology. American Society for Microbiology, Washington, DC, pp. 822-848.
52. Su,L. Radek,J.T., Hallenga,K., Hermanto,P., Chan,G., Labeots,L.A. and Weiss,M.A. (1997a) RNA recognition by a bent ex-helix regulates transcriptional antitermination in phage λ. Biochemistry, 36, 12722-12732.
53. Su,L. et al. (1997b) An RNA enhancer in a phage transcriptional antitermination complex functions as a structural switch. Genes Dev., 11, 2214-2226.
54. Taura,R., Ueguchi,C., Shiba,K. and Ito,K. (1992) Insertional disruption of the nusB (ssyB) gene leads to cold-sensitive growth of Escherichia coli and suppression of the secY24 mutation. Mol. Gen. Genet., 234, 429-432.
55. Torchia,D.A., Sparks,S.W. and Bax,A. (1988) Delineation of α-helical domains in deuterated staphyloccal nuclease by 2D NOE NMR spectroscopy. J. Am. Chem. Soc., 110, 2320-2321.
56. Van Gilst,M.R., Rees,W.A., Das,A. and von Hippel,P.H. (1997) Complexes of N antitermination protein of phage λ with specific and nonspecific RNA target sites on the nascent transcript. Biochemistry, 36, 1514-1524.
57. Varani,G. (1997) RNA-protein intermolecular recognition. Acc. Chem. Res., 5, 189-195.
58. N NOEs to determine protein global folds in perdeuterated proteins. J. Am. Chem. Soc., 117, 9592-9593.
59. 15N-enriched proteins, J. Am. Chem. Soc., 115, 7772-7777.
60. Wolberger,C. (1996) Homeodomain interactions. Curr. Opin. Struct. Biol., 6, 62-68.
61. Xing,Y., Guha Thakurta,D. and Draper,D.E. (1997) The RNA-binding domain of ribosomal protein L11 is structurally similar to homeodomains. Nature Struct. Biol., 4, 24-27.
62. Ye,X., Kumar,R. and Patel,D.J. (1995) Molecular recognition in the bovine immunodeficiency virus Tat peptide-TAR RNA complex. Chem. Biol., 2, 827-840.
63. Ye,X., Gorin,A., Ellington,A.D. and Patel,J.D. (1996) Deep penetration of an α-helix into a widened RNA major groove in the HIV-1 rev peptide-RNA aptamer complex. Nature Struct. Biol., 3, 1026-1033.
64. 13C-labelled proteins for the NMR assignment and structure determination of larger molecules, J. Magn. Resonance, 86, 210-216.
65. Zwahlen,C., Legault,P., Vincent,S.J.F., Greenblatt,J., Konrat,R. and Kay,L.E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N peptide/boxB RNA complex. J. Am. Chem. Soc., 119, 6711-6721.