Evolutionary comparison of ribosomal operon antitermination function

Journal of Bacteriology

Volumn 190, Issue 21, 2008, Pages 7251-7257

  Arnvig, Kristine B ^a   Zeng, Shirley ^b   Quan, Selwyn ^b,c   Papageorge, Alexander ^b   Zhang, Ning ^b   Villapakkam, Anuradha C ^c   Squires, Catherine L ^b,c  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN NUSB; RNA POLYMERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CAULOBACTER CRESCENTUS; CONTROLLED STUDY; ESCHERICHIA COLI; EVOLUTION; GENE SEQUENCE; GENETIC TRANSCRIPTION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PSEUDOMONAS AERUGINOSA; RIBOSOME; THERMOTOGA MARITIMA; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PSEUDOMONAS AERUGINOSA; RNA, RIBOSOMAL; SPECIES SPECIFICITY; TERMINATOR REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS; CAULOBACTER VIBRIOIDES; ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; PSEUDOMONAS AERUGINOSA; THERMOTOGA MARITIMA;

EID: 55749106800     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00760-08     Document Type: Article

References (53)

1. Albrechtsen, B., C. L. Squires, S. Li, and C. Squires. 1990. Antitermination of characterized transcriptional terminators by the Escherichia coli rrnG leader region. J. Mol. Biol. 213:123-134.
2. Angelini, G., N. Tanigaki, R. Tosi, and G. B. Ferrara. 1986. Southern blot and micro fingerprinting analysis of two DR7 haplotypes. Immunogenetics 24:63-67.
3. Arnvig, K. B., S. Pennell, B. Gopal, and M. J. Colston. 2004. A high-affinity interaction between NusA and the rrn nut site in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 101:8325-8330.
4. Berg, K. L., C. Squires, and C. L. Squires. 1989. Ribosomal RNA operon anti-termination. Function of leader and spacer region box B-box A sequences and their conservation in diverse micro-organisms. J. Mol. Biol. 209:345-358.
5. Beuth, B., S. Pennell, K. B. Arnvig, S. R. Martin, and I. A. Taylor. 2005. Structure of a Mycobacterium tuberculosis NusA-RNA complex. EMBO J. 24:3576-3587.
6. Blattner, F. R., G. Plunkett, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
7. Bonin, I., R. Robelek, H. Benecke, H. Urlaub, A. Bacher, G. Richter, and M. C. Wahl. 2004. Crystal structures of the antitermination factor NusB from Thermotoga maritima and implications for RNA binding. Biochem. J. 383:419-428.
8. Bubunenko, M., T. Baker, and D. L. Court. 2007. Essentiality of ribosomal and transcription antitermination proteins analyzed by systematic gene replacement in Escherichia coli. J. Bacteriol. 189:2844-2853.
9. Cardinale, C. J., R. S. Washburn, V. R. Tadigotla, L. M. Brown, M. E. Gottesman, and E. Nudler. 2008. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320:935-938.
10. Cheeran, A., N. R. Kolli, and R. Sen. 2007. The site of action of the anti-terminator protein N from the lambdoid phage H-19B. J. Biol. Chem. 282:30997-31007.
11. Cheeran, A., R. B. Suganthan, G. Swapna, I. Bandey, M. S. Achary, H. A. Nagarajaram, and R. Sen. 2005. Escherichia coli RNA polymerase mutations located near the upstream edge of an RNA:DNA hybrid and the beginning of the RNA-exit channel are defective for transcription antitermination by the N protein from lambdoid phage H-19B. J. Mol. Biol. 352:28-43.
12. Condon, C., C. Squires, and C. L. Squires. 1995. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59:623-645.
13. Court, D. L., T. A. Patterson, T. Baker, N. Costantino, X. Mao, and D. I. Friedman. 1995. Structural and functional analyses of the transcription-translation proteins NusB and NusE. J. Bacteriol. 177:2589-2591.
14. Das, R., S. Loss, J. Li, D. S. Waugh, S. Tarasov, P. T. Wingfield, R. A. Byrd, and A. S. Altieri. 2008. Structural biophysics of the NusB:NusE antitermination complex. J. Mol. Biol. 376:705-720.
15. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
16. Davies, K. M., A. J. Dedman, S. van Horck, and P. J. Lewis. 2005. The NusA:RNA polymerase ratio is increased at sites of rRNA synthesis in Bacillus subtilis. Mol. Microbiol. 57:366-379.
17. Doherty, G. P., D. H. Meredith, and P. J. Lewis. 2006. Subcellular partitioning of transcription factors in Bacillus subtilis. J. Bacteriol. 188:4101-4110.
18. Downing, W. L., S. L. Sullivan, M. E. Gottesman, and P. P. Dennis. 1990. Sequence and transcriptional pattern of the essential Escherichia coli secEnusG operon. J. Bacteriol. 172:1621-1627.
19. Friedman, D. I., and E. R. Olson. 1983. Evidence that a nucleotide sequence, "boxA," is involved in the action of the NusA protein. Cell 34:143-149.
20. Gopal, B., L. F. Haire, R. A. Cox, M. J. Colston, S. Major, J. A. Brannigan, S. J. Smerdon, and G. Dodson. 2000. The crystal structure of NusB from Mycobacterium tuberculosis. Nat. Struct. Biol. 7:475-478.
21. Gopal, B., K. G. Papavinasasundaram, G. Dodson, M. J. Colston, S. A. Major, and A. N. Lane. 2001. Spectroscopic and thermodynamic characterization of the transcription antitermination factor NusE and its interaction with NusB from Mycobacterium tuberculosis. Biochemistry 40:920-928.
22. Greenblatt, J., J. R. Nodwell, and S. W. Mason. 1993. Transcriptional antitermination. Nature 364:401-406.
23. Greive, S. J., A. F. Lins, and P. H. von Hippel. 2005. Assembly of an RNA-protein complex. Binding of NusB and NusE (S10) proteins to boxA RNA nucleates the formation of the antitermination complex involved in controlling rRNA transcription in Escherichia coli. J. Biol. Chem. 280:36397-36408.
24. Heinrich, T., C. Condon, T. Pfeiffer, and R. K. Hartmann. 1995. Point mutations in the leader boxA of a plasmid-encoded Escherichia coli rrnB operon cause defective antitermination in vivo. J. Bacteriol. 177:3793-3800.
25. Herbert, K. M., A. L. Porta, B. J. Wong, R. A. Mooney, K. C. Neuman, R. Landick, and S. M. Block. 2006. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 125:1083-1094.
26. Ingham, C. J., J. Dennis, and P. A. Furneaux. 1999. Autogenous regulation of transcription termination factor Rho and the requirement for Nus factors in Bacillus subtilis. Mol. Microbiol. 31:651-663.
27. Klotsky, R. A., and I. Schwartz. 1987. Measurement of cat expression from growth-rate-regulated promoters employing beta-lactamase activity as an indicator of plasmid copy number. Gene 55:141-146.
28. Li, J., R. Horwitz, S. McCracken, and J. Greenblatt. 1992. NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage lambda. J. Biol. Chem. 267:6012-6019.
29. Li, S. C., C. L. Squires, and C. Squires. 1984. Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences. Cell 38:851-860.
30. Li, Z., G. Stahl, and P. J. Farabaugh. 2001. Programmed +1 frameshifting stimulated by complementarity between a downstream mRNA sequence and an error-correcting region of rRNA. RNA 7:275-284.
31. Lttgen, H., R. Robelek, R. Mhlberger, T. Diercks, S. C. Schuster, P. Khler, H. Kessler, A. Bacher, and G. Richter. 2002. Transcriptional regulation by antitermination. Interaction of RNA with NusB protein and NusB/NusE protein complex of Escherichia coli. J. Mol. Biol. 316:875-885.
32. Mah, T. F., K. Kuznedelov, A. Mushegian, K. Severinov, and J. Greenblatt. 2000. The alpha subunit of E. coli RNA polymerase activates RNA binding by NusA. Genes Dev. 14:2664-2675.
33. Mah, T. F., J. Li, A. R. Davidson, and J. Greenblatt. 1999. Functional importance of regions in Escherichia coli elongation factor NusA that interact with RNA polymerase, the bacteriophage lambda N protein and RNA. Mol. Microbiol. 34:523-537.
34. Mason, S. W., and J. Greenblatt. 1991. Assembly of transcription elongation complexes containing the N protein of phage lambda and the Escherichia coli elongation factors NusA, NusB, NusG, and S10. Genes Dev. 5:1504-1512.
35. Mason, S. W., J. Li, and J. Greenblatt. 1992. Host factor requirements for processive antitermination of transcription and suppression of pausing by the N protein of bacteriophage lambda. J. Biol. Chem. 267:19418-19426.
36. Mathews, D. H., J. Sabina, M. Zuker, and D. H. Turner. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288:911-940.
37. Nodwell, J. R., and J. Greenblatt. 1993. Recognition of boxA antiterminator RNA by the E. coli antitermination factors NusB and ribosomal protein S10. Cell 72:261-268.
38. Pfeiffer, T., and R. K. Hartmann. 1997. Role of the spacer boxA of Escherichia coli ribosomal RNA operons in efficient 23 S rRNA synthesis in vivo. J. Mol. Biol. 265:385-393.
39. Quan, S., N. Zhang, S. French, and C. L. Squires. 2005. Transcriptional polarity in rRNA operons of Escherichia coli nusA and nusB mutant strains. J. Bacteriol. 187:1632-1638.
40. Schäferkordt, J., and R. Wagner. 2001. Effects of base change mutations within an Escherichia coli ribosomal RNA leader region on rRNA maturation and ribosome formation. Nucleic Acids Res. 29:3394-3403.
41. Sharrock, R. A., R. L. Gourse, and M. Nomura. 1985. Defective antitermination of rRNA transcription and derepression of rRNA and tRNA synthesis in the nusB5 mutant of Escherichia coli. Proc. Natl. Acad. Sci. USA 82:5275-5279.
42. Shin, D. H., H. H. Nguyen, J. Jancarik, H. Yokota, R. Kim, and S.-H. Kim. 2003. Crystal structure of NusA from Thermotoga maritima and functional implication of the N-terminal domain. Biochemistry 42:13429-13437.
43. Squires, C. L., C. Condon, and H.-K. Seoh. 2003. Assay of antitermination of ribosomal RNA transcription. Methods Enzymol. 371:472-487.
44. Squires, C. L., J. Greenblatt, J. Li, C. Condon, and C. L. Squires. 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.
45. Taura, T., C. Ueguchi, K. Shiba, and K. Ito. 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.
46. Torres, M., J.-M. Balada, M. Zellars, C. Squires, and C. L. Squires. 2004. In vivo effect of NusB and NusG on rRNA transcription antitermination. J. Bacteriol. 186:1304-1310.
47. Torres, M., C. Condon, J. M. Balada, C. Squires, and C. L. Squires. 2001. Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J. 20:3811-3820.
48. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218:97-106.
49. Vogel, U., and K. F. Jensen. 1995. Effects of the antiterminator BoxA on transcription elongation kinetics and ppGpp inhibition of transcription elongation in Escherichia coli. J. Biol. Chem. 270:18335-18340.
50. Vogel, U., and K. F. Jensen. 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.
51. Zellars, M., and C. L. Squires. 1999. Antiterminator-dependent modulation of transcription elongation rates by NusB and NusG. Mol. Microbiol. 32:1296-1304.
52. Zhou, Y., T. F. Mah, Y. T. Yu, J. Mogridge, E. R. Olson, J. Greenblatt, and D. I. Friedman. 2001. Interactions of an Arg-rich region of transcription elongation protein NusA with NUT RNA: implications for the order of assembly of the lambda N antitermination complex in vivo. J. Mol. Biol. 310:33-49.
53. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.