Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli

Journal of Molecular Biology

Volumn 278, Issue 2, 1998, Pages 307-316

  Burns, Christopher M ^a,b   Richardson, Lislott V ^a   Richardson, John P ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Kinetic coupling; NusA; NusG; Rho dependent transcription termination; RNA polymerase

Indexed keywords

ELONGATION FACTOR; RHO FACTOR; RNA POLYMERASE; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION TERMINATION;

ESCHERICHIA COLI;

EID: 0032079954     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1691     Document Type: Article

References (46)

1. Burns, C. M. & Richardson, J. P. (1995). NusG is required to overcome a kinetic limitation to Rho function at an intragenic terminator. Proc. Natl Acad. Sci. USA, 92, 4738-4742.
2. Burova, E., Hung, S. C., Sagitov, V., Stitt, B. L. & Gottesman, M. E. (1995). Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro. J. Bacteriol. 177, 1388-1392.
3. Chan, C. L. & Landick, R. (1989). The Salmonella typhimurium his operon leader reagion contains an RNA hairpin-dependent transcription pause site. J. Biol. Chem. 264, 20796-20804.
4. Farnham, P. J., Greenblatt, J. & Platt, T. (1982). Effects of NusA protein on transcription termination in the tryptophan operon of Escherichia coli. Cell, 29, 945-951.
5. Fisher, R. F. & Yanofsky, C. (1983). A complementary DNA oligomer releases a transcription pause complex. J. Biol. Chem. 258, 9208-9212.
6. Fraser, C. M., Gocayne, J. D. & White, O. (1995). The minimal gene complement of Mycoplasma genitalium. Science, 270, 397-445.
7. 70 and NusA proteins I. Binding interactions with core RNA polymerase in solution and within the transcription complex. J. Mol. Biol. 220, 307-324.
8. Greenblatt, J. & Li, J. (1981). Interaction of the sigma factor and the nusA gene protein of E. coli with RNA polymerase in the initiation-termination cycle of transcription. Cell, 24, 421-428.
9. Greenblatt, J., McLimont, M. & Hanly, S. (1981). Termination of transcription by nusA gene protein of Escherichia coli. Nature, 292, 215-220.
10. Jin, D. J., Burgess, R. R., Richardson, J. P. & Gross, C. A. (1992). Termination efficiency at rho-dependent terminators depends on kinetic coupling between RNA polymerase and rho. Proc. Natl Acad. Sci. USA, 89, 1453-1457.
11. Kassavetis, G. A. & Chamberlin, M. J. (1981). Pausing and termination of transcription within the early region of bacteriophage T7 DNA in vitro. J. Biol. Chem. 256, 2777-2786.
12. Kingston, R. E., Nierman, W. C. & Chamberlin, M. J. (1981). A direct effect of guanosine tetraphosphate on pausing of E. coli RNA polymerase during RNA chain elongation. J. Biol. Chem. 256, 2787-2797.
13. Komisarrova, N. & Kashlev, M. (1997). Arrest of transcription: E. coli RNA polymerase translocates backward leaving the 3′ end of the RNA intact and extruded. Proc. Natl Acad. Sci. USA, 94, 1755-1760.
14. Landick, R. & Yanofsky, C. (1984). Stability of an RNA secondary structure affects in vitro transcription pausing in the trp operon leader region. J. Biol. Chem. 259, 11550-11555.
15. Lau, L. F., Roberts, J. W. & Wu, R. (1982). Transcription terminates at λtR1 in three clusters. Proc. Natl Acad. Sci. USA, 79, 6171-6175.
16. R1 terminator in vitro. J. Biol. Chem. 258, 9391-9397.
17. Levin, J. R., Krummel, B. & Chamberlin, M. J. (1987). Isolation and properties of transcribing ternary complexes of Escherichia coli RNA polymerase positioned at a single template base. J. Mol. Biol. 196, 85-100.
18. Li, J., Horwitz, R., McCracken, S. & Greenblatt, J. (1992). NusG, a new Escherichia coli elongation factor involved in transcription antitermination by the N protein of phage λ. J. Biol. Chem. 267, 6012-6019.
19. Li, J., Mason, S. W. & Greenblatt, J. (1993). Elongation factor NusG interacts with termination factor p to regulate termination and antitermination of transcription. Genes Dev. 7, 161-172.
20. Linn, T. & Greenblatt, J. (1992). The NusA and NusG proteins of Escherichia coli increase the in vitro read-through frequency of a transcriptional attenuator preceding the gene for the β subunit of RNA polymerase. J. Biol. Chem. 267, 1449-1454.
21. Liu, K. & Hanna, M. M. (1995a). NusA contacts nascent RNA in E. coli transcription complexes. J. Mol. Biol. 247, 547-558.
22. Liu, K. & Hanna, M. M. (1995b). NusA interferes with interactions between the nascent RNA and the C-terminal domain of the alpha subunit of E. coli transcription complexes. Proc. Natl Acad. Sci. USA, 92, 5012-5016.
23. Liu, K., Zhang, Y., Severinov, K., Das, A. & Hanna, M. M. (1996). Role of Escherichia coli RNA polymerase alpha subunit in modulation of pausing, termination and anti-termination by the transcription elongation factor NusA. EMBO J. 15, 150-161.
24. Mason, S. W., Li, J. & Greenblatt, J. (1992). Host factor requirements for processive antitermination of transcription and suppression of pausing by the N protein of bacteriophage λ. J. Biol. Chem. 267, 19418-19426.
25. Matthews, C. (1972). Biochemistry of deoxyribonucleic acid-defective amber mutants of bacteriophage T4. J. Biol. Chem. 247, 7430-7438.
26. R promoter. J. Biol. Chem. 258, 9565-9574.
27. Mosteller, R. D. & Yanofsky, C. (1970). Transcription of the tryptophan operon in Escherichia coli: rifampicin as an inhibitor of initiation. J. Mol. Biol. 48, 525-531.
28. Nehrke, K. W., Zalatan, F. & Platt, T. (1993). NusG alters rho-dependent termination of transcription in vitro independent of kinetic coupling. Gene Expression, 3, 119-133.
29. Nowatzke, W. L., Richardson, L. V. & Richardson, J. P. (1996). Purification of transcription termination factor Rho from Escherichia coli and Micrococcus luteus. Methods Enzymol. 274, 353-363.
30. Nudler, E., Mustaev, A., Lukhtanov, E. & Godlfarb, A. (1997). The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell, 89, 33-41.
31. Primakoff, P. & Artz, S. W. (1979). Positive control of lac operon expression in vitro by guanosine 5′-diphosphate 3′-diphosphate. Proc. Natl Acad. Sci. USA, 76, 1726-1730.
32. Richardson, L. V. & Richardson, J. P. (1996). Rho-dependent termination of transcription is governed primarily by the upstream Rho utilization (rut) sequences of a terminator. J. Biol. Chem. 271, 21597-21603.
33. Ruteshouser, E. C. & Richardson, J. P. (1989). Identification and characterization of transcription termination sites in the Escherichia coli lacZ gene. J. Mol. Biol. 208, 23-43.
34. Schmidt, M. C. & Chamberlin, M. J. (1984). Binding of rho factor to Escherichia coli RNA polymerase mediated by NusA protein. J. Biol. Chem. 259, 15000-15002.
35. Schmidt, M. C. & Chamberlin, M. J. (1987). nus A protein of Escherichia coli is an efficient transcription terminator factor for certain termination sites. J. Mol. Biol. 195, 809-818.
36. Sigmund, C. D. & Morgan, E. A. (1988). NusA protein affects transcriptional pausing and termination in vitro by binding to different site on the transcription complex. Biochemistry, 27, 5622-5627.
37. Sullivan, S. L. & Gottesman, M. E. (1992). Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell, 68, 989-994.
38. Sullivan, S. L., Ward, D. F. & Gottesman, M. E. (1992). Effect of Escherichia coli nusG function λ N-mediated transcription antitermination. J. Bacteriol. 174, 1339-1344.
39. Vogel, U. & Jensen, K. F. (1994a). Effects of guanosine 3′,5′-bisdiphosphate (ppGpp) on rate of transcription elongation in Isoleucine-starved Escherichia coli. J. Biol. Chem. 269, 16236-16241.
40. Vogel, U. & Jensen, K. F. (1994b). The RNA chain elongation rate in Escherichia coli depends on the growth rate. J. Bacteriol. 176, 2807-2813.
41. Vogel, U. & Jensen, K. F. (1997). NusA is required for ribosomal antitermination and for modulation of the transcription elongation rate of both antiterminated RNA and mRNA. J. Biol. Chem. 272, 12265-12271.
42. Wang, D., Meier, T., Chan, C. L., Feng, G., Lee, D. N. & Landick, R. (1995). Discontinuous movements of DNA, and RNA in E. coli RNA polymerase trigger formation of a paused transcription complex. Cell, 81, 341-350.
43. Whalen, W., Ghosh, B. & Das, A. (1988). NusA protein is necessary and sufficient in vitro for phage λ N gene product to suppress a p-independent terminator placed downstream of nutL. Proc. Natl Acad. Sci. USA, 85, 2494-2498.
44. Winston, S. E., Fuller, S. A. & Hurrell, J. G. R. (1989). Enzyme-linked immunosorbent assays (ELISA) for detecting antigens. In Current Protocols in Molecular Biology (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K., eds), pp. 11.2.1-11.2.9, J. Wiley & Son, New York, NY.
45. Zalenskaya, K., Lee, J., Gujuluva, C. N., Shin, Y. K., Slutsky, M. & Goldfarb, A. (1990). Recombinant RNA polymerase: inducible overexpression, purification and assembly of Escherichia coli rpo gene products. Gene, 89, 7-12.
46. Zheng, C. & Friedman, D. I. (1994). Reduced Rho-dependent transcription termination permits NusA-independent growth of Escherichia coli. Proc. Natl Acad. Sci. USA, 91, 7543-7547.