Studies on the NusB protein of Escherichia coli expression and determination of secondary-structure elements by multinuclear NMR spectroscopy

European Journal of Biochemistry

Volumn 248, Issue 2, 1997, Pages 338-346

  Berglechner, Fabian ^a   Richter, Gerald ^a   Fischer, Markus ^a   Bacher, Adelbert ^a   Gschwind, Ruth M ^a   Huenges, Martin ^a   Gemmecker, Gerd ^a   Kessler, Horst ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Antitermination; N utilization protein; NMR; NusB protein; Secondary structure

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; ESCHERICHIA COLI; GENE CONSTRUCT; GENE EXPRESSION; GENE OVEREXPRESSION; MUTANT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TRANSCRIPTION TERMINATION;

BACTERIA (MICROORGANISMS); BACTERIOPHAGE LAMBDA; ESCHERICHIA COLI; EUKARYOTA; HUMAN IMMUNODEFICIENCY VIRUS;

EID: 0030931961     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00338.x     Document Type: Article

References (72)

1. Bax, A. & Pochapsky, S. (1992) Optimized recording of heteronuclear multidimensional NMR spectra using pulsed field gradients, J. Magn. Reson. 99, 638-643.
2. Bax, A., Ikura, M., Kay, L. E., Torchia, D. A. & Tschudin, R. (1990) Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins, J. Magn. Reson. 86, 304-318.
3. Berg, K. L., Squires, C. & Squires, C. L. (1989) Ribosomal RNA operon anti-termination. Function of leader and spacer region box B-Box A sequences and their conservation in diverse microorganisms, J. Mol. Biol. 209, 345-358.
4. Bujard, H., Gentz, R., Lanzer, M., Stueber, D., Mueller, M., Ibrahimi, I., Haeuptle, M.-T. & Dobberstein, B. (1987) A T5 promoter-based transcription-translation system for the analysis of proteins in vitro and in vivo, Methods Enzymol. 155, 416-433.
5. Bullock, W. O., Fernandez, J. M. & Short, J. M. (1987) XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection, Biotechniques 5, 376-379.
6. Calnan, B. J., Tidor, B., Biancalana, S., Hudson, D., Frankel, A. D. (1991) Arginine-mediated RNA recognition: the arginine fork, Science 252, 1167-1171.
7. Chattopadhyay, S., Garcia-Mena, J., DeVito, J., Wolska, K. & Das, A. (1995) Bipartite function of a small RNA hairpin in transcription antitermination in bacteriophage λ, Proc. Natl Acad. Sci. USA 92, 4061-4065.
8. Cheng, S-W, C., Lynch, E. C., Leason, K. R., Court, D. L., Shapiro, B. A. & Friedman, D. I. (1991) Functional importance of sequence in the stem-loop of a transcription terminator, Science 254, 1205-1207.
9. 13C-labelled proteins, J. Biomol. NMR 2, 203-210.
10. Condon, C., Squires, C. & Squires, C. L. (1995) Control of rRNA transcription in Escherichia coli, Microbiol. Reviews 59, 623-645.
11. Court, D. L., Patterson, T. A., Baker, T., Costantino, N., Mao X. & Friedman, D. I. (1995) Structural and functional analyses of the transcription-translation proteins NusB and NusE, J. Bacteriol. 177, 2589-2591.
12. Das, A. (1992) How the phage lambda N gene product suppresses transcription termination: communication of RNA polymerase with regulatory proteins mediated by signals in nascent RNA, J. Bacteriol. 174, 6711-6716.
13. Das, A. (1993) Control of transcription termination by RNA-binding proteins, Annu. Rev. Biochem. 62, 893-930.
14. Das, A., Pal, M., Mena, J. G., Whalen, W., Wolska, K., Crossley, R., Rees, W., von Hippel, P. H., Costantino, N., Court, D., Mazzulla, M., Altieri, A. S., Byrd, R. A., Chattopadhyay, S., DeVito, J. & Ghosh, B. (1996) Components of multiprotein-RNA complex that controls transcription elongation in Escherichia coli phage λ, Methods Enzymol. 274, 374-402.
15. DeVito, J. & Das, A. (1994) Control of transcription 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.
16. 13C resonanes in perdeuterated proteins, J. Am. Chem. Soc. 117, 4187-4188.
17. Fleischmann, R. D., Adams, M. D., White, O., Clayton, R. A., Kirkness, E. F., Kerlavage, A. R., Bult, C. J., Tomb, J.-F., Dougherty, B. A., Merrick, J. M. McKenney, K., Sutton, G., FitzHugh, W., Fields, C., Gocayne, J. D., Scott, J., Shirley, R., Liu, L.-I., Glodek, A., Kelley, J. M., Weidman, J. F., Phillips, C. A., Spriggs, T., Hedblom, E., Cotton, M. D., Utterback, T. R., Hanna, M. C., Nguyen, D. T., Saudek, D. M., Brandon, R. C., Fine, L. D., Fritchman, J. L., Fuhrmann, J. L., Geoghagen, N. S. M., Gnehm, C. L., McDonald, L. A., Small, K. V. Fraser, C. M., Smith, H. O. & Venter, J. C. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd., Science 269, 496-512.
18. Friedman, D. I. (1992) Interaction between bacteriophage λ and its Escherichia coli host, Curr. Opin. Gen. Genet. 2, 727-738.
19. Friedman, D. I. & Court, D. L. (1995) Transcription antitermination: the λ paradigm updated, Mol. Microbiol. 18, 191-200.
20. Gemmecker, G., Jahnke, W. & Kessler, H. (1993) Measurement of fast proton exchange rates in isotopically labeled compounds, J. Am. Chem. Soc. 115, 11620-11621.
21. Ghosh, B. & Das, A. (1984) NusB: a protein factor necessary for transcription antitermination in vitro by phage λ N gene product, Proc. Natl Acad. Sci. USA 81, 6305-6309.
22. Greenblatt, J., Nodwell, J. R. & Mason, S. W. (1993) Transcriptional antitermination, Nature 364, 401-406.
23. Harada, K., Martin, S. S. & Frankel, A. D. (1996) Selection of RNA-binding peptides in vivo, Nature 380, 175-179.
24. Henkin, T. M. (1996) Control of transcription termination in prokaryotes, Annu. Rev. Genet. 30, 35-57
25. 13C-labelled protein, J. Magn. Reson. 86, 204-209.
26. Jahnke, W. & Kessler, H. (1995) Modified triple-resonance NMR experiments with optimized sensitivity for rapidly exchanging protons, Angew. Chem. Int. Ed. Engl. 34, 469-471.
27. Karn, J. & Graeble, A. (1992) New insights into the mechanism of HIV-1 trans-activation, Trends Genet. 8, 365-368.
28. Kay, L. E., Ikura, M., Tschudin, R. & Bax, A. (1990) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins, J. Magn. Reson. 89, 496-514.
29. Kay, L. E., Keifer, P. & Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
30. 2O samples of proteins, J. Magn. Reson. B 101, 333-337.
31. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
32. Lanzer, M. & Bujard, H. (1988) Promoters largely determine the efficiency of repressor action, Proc. Natl Acad. Sci. USA 85, 8973-8977.
33. Laue, T. M., Shah, B. D., Ridgeway, T. M. & Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins; in Analytical ultracentrifugation in biochemistry and polymer science (Harding, S. E., Rowe, A. J. & Horton, J. C., eds) pp. 90-125, The Royal Society of Chemistry, Cambridge.
34. Maekawa, T., Nagase, T., Imamoto, F. & Ishii, S. (1985) Purification of the NusB gene product of Escherichia coli K12. Mol. Gen. Genet. 200, 14-20.
35. Marion, D., Ikura, M., Tschudin, R. & Bax, A. (1989) Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins, J. Magn. Reson. 85, 393-399.
36. Mason, S. W., Li, J. & Greenblatt, J. (1992) Direct interaction between two Escherichia coli transcription antitermination factors, NusB and ribosomal protein S10, J. Mol. Biol. 223, 55-66.
37. Mogridge, J., Mah, T.-F. & 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, 2831-2844.
38. Mörtl, S., Fischer, M., Richter, G., Tack, J., Weinkauf, S. & Bacher, A. (1996) Biosynthesis of riboflavin. Lumazine synthase of Escherichia coli. J. Biol. Chem. 271, 33201-33207.
39. Nietlispach, D., Clowes, R. T., Broadhurst, R. W., Ito, Y., Keeler, J., Kelly, M., Ashurst, J., Oschkinat, H., Domaille, P. J. & Laue, E. D. (1996) An approach to the structure determination of larger proteins using triple resonance NMR experiments in conjunction with random fractional deuteration, J. Am. Chem. Soc. 118, 407-415.
40. Nodwell, J. R. & 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.
41. Nodwell, J. R. & Greenblatt, J. (1993) Recognition of boxA antiterminator RNA by the E. coli antitermination factors NusB and ribosomal protein S10, Cell 72, 261-268.
42. Obuchowski, M., Wegrzyn, A., Szalewska-Palasz, A., Thomas M. S. & Wegrzyn, G. (1997) An RNA polymerase α subunit mutant impairs N-dependent transcriptional antitermination in Escherichia coli, Mol. Microbiol. 23, 211-222.
43. Palmer, A. G. III, Cavanagh, J., Wright, P. E. & Rance, M. (1991) Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy, J. Magn. Reson. 93, 151-170.
44. Patterson, T. A., Zhang, Z., Baker, T., Johnson, L. J., Fiedman, D. I. & Court, D. L. (1994) Bacteriophage lambda N-dependent transcription antitermination. Competition for an RNA site may regulate antitermination, J. Mol. Biol. 236, 217-228.
45. 15N-enriched proteins using constant-time evolution, J. Magn. Reson. 94, 209-213.
46. Rees, W. A., Weitzel, S. E., Yager, T. D., Das, A. & von Hippel, P. H. (1996) Bacteriophage λ N protein alone can induce transcription antitermination in vitro, Proc. Natl Acad. Sci. USA 93, 342-346.
47. Richardson, J. P. & Greenblatt, J. (1996) Control of RNA chain elongation and termination; in Escherichia coli and Salmonella typhimurium: cellular and molcular biology (Neidhardt, F. C., Ingraham, J. L., Low, K. B., Magasanik, B., Schaechter, M. & Umbarger, H. E., eds) vol. 2, pp. 822-848. American Society for Microbiology, Washington.
48. Richter, G., Fischer, M., Krieger, C., Eberhardt, S., Lüttgen, H., Gerstenschläger, I. & Bacher, A. (1997) Biosynthesis of riboflavin: characterization of the bifunctional deaminase-reductase of Escherichia coli and Bacillus subtilis, J. Bacteriol. 179, 2022-2028.
49. Sanger, F., Nicklen, S. & Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors Proc. Natl Acad. Sci. USA 74, 5463-5467.
50. Sattler, M. & Fesik, S. W. (1996) Use of deuterium labeling in NMR: overcoming a sizeable problem, Structure (Lond.) 4, 1245-1249.
51. Schägger, H. & von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
52. Schägger, H. & von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form, Anal. Biochem. 199, 223-231.
53. Schauer, A. T., Cheng, S.-W. C., Zheng, C., St Pierre, L., Alessi, D., Hidayetoglu, D. L., Costantino, N., Court, D. L. & Friedman, D. I. (1996) The alpha subunit of RNA polymerase and transcription antitermination, Mol. Microbiol. 21, 839-851.
54. Schleucher, J., Sattler, M. & Griesinger, C. (1993). Coherence selecion by gradients without signal attenuation - application to the three-dimensional HNCO experiment. Angew. Chem. Int. Ed. Engl. 32, 1489-1491.
55. 15N and Hα protons (HN(CA)H) in isotopically enriched proteins, J. Magn. Reson. 100, 406-410.
56. 2H labelled 64 kDa trp repressor-operator complex using triple-resonance NMR spectroscopy and 2H-decoupling, J. Am. Chem. Soc. 118, 6570-6579.
57. 13C nuclear magnetic resonance chemical shifts, J. Am. Chem. Soc. 113, 5490-5492.
58. Squires, C. L., Greenblatt, J., Li, J. Condon, C. & Squires, C. L. (1993) Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentified cellular components, Proc. Natl Acad. Sci. USA 90, 970-974.
59. Stüber, D., Matile, H. & Garotta, G. (1990) System for high-level production in Escherichia coli and rapid purification of recombinant proteins: application to epitope mapping, preparation of antibodies, and structure-function analysis, Immun. Methods 4, 121-152.
60. Swindle, J., Zylicz, M., Georgopoulos, C., Li, J. & Greenblatt, J. (1988) Purification and properties of the NusB protein of Escherichia coli, J. Biol. Chem. 263, 10229-10235.
61. Taura, T., Ueguchi, C., Shiba, K. & 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.
62. Van Gilst, M. R., Rees, W. A., Das, A. & 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.
63. 15N-enriched proteins, J. Am. Chem. Soc. 115, 7772-7777.
64. Wishart, D. S., Sykes, B. D. & Richards, F. M. (1991) Relationship between nuclear-magnetic-resonance chemical-shift and protein secondary structure, J. Mol. Biol. 222, 311-333.
65. 13C chemical-shift data, J. Biomol. NMR 4, 171-180.
66. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects, J. Biomol. NMR 5, 67-81.
67. 15N chemical shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
68. Wüthrich, K. (1986) NMR of proteins and nucleic acids, Wiley. New York, NY.
69. 2H labelled proteins with high sensitivity, J. Am. Chem. Soc. 116, 11655-11666.
70. 2H-labelled proteins: application to a 37-kDa Trp repressor-DNA complex, J. Am. Chem. Soc. 116, 6464-6465.
71. Zamenhof, P. J., & Villarejo, M. (1972) Construction and properties of Escherichia coli strains exhibiting α-complementation of β-galactosidase fragments in vivo, J. Bacteriol. 110, 171-178.
72. 13C-labelled proteins for the NMR assignment and structure determination of larger molecules, J. Magn. Reson. 86, 210-216.