Context and conformation dictate function of a transcription antitermination switch

Nature Structural Biology

Volumn 10, Issue 10, 2003, Pages 812-819

  Xia, Tianbing ^a   Frankel, Adam ^a   Takahashi, Terry T ^a   Ren, Jinsong ^b   Roberts, Richard W ^a  

^a California Institute of Technology   (United States)

^b CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BOXB RNA; CIS ACTING ELEMENT; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; RNA POLYMERASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE LAMBDA; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; KINETICS; PEPTIDE ELONGATION FACTORS; PEPTIDES; PROTEIN CONFORMATION; RNA; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACTERIOPHAGE LAMBDA; UNIDENTIFIED BACTERIOPHAGE;

EID: 0141730393     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb983     Document Type: Article

References (49)

1. von Hippel, P.H. An integrated model of the transcription complex in elongation, termination, and editing. Science 281, 660-665 (1998).
2. Yarnell, W.S. & Roberts, J.W. Mechanism of intrinsic transcription termination and antitermination. Science 284. 611-615 (1999).
3. Uptain, S.M., Kane, C.M. & Chamberlin, M.J. Basic mechanisms of transcript elongation and its regulation. Annu. Rev. Biochem. 66. 117-172 (1997).
4. Zorio, D.A. & Bentley, D.L. Transcription elongation: the 'Foggy' is lifting... Curr. Biol. 11, R144-R146 (2001).
5. Maniatis, T. & Reed, R. An extensive network of coupling among gene expression machines. Nature 416, 499-506 (2002).
6. Roberts, J.W. Termination factor for RNA synthesis. Nature 224, 1168-1174 (1969).
7. Greenblatt, J. Positive control of endolysin synthesis in vitro by the gene N protein of phage λ. Proc. Natl. Acad. Sci. USA 69, 3606-3610 (1972).
8. -: a unique class of mutants defective in the site of gene N product utilization for antitermination of leftward transcription. J. Mol. Biol. 124, 195-221 (1978).
9. Greenblatt, J., Nodwell, J.R. & Mason, S.W. Transcriptional antitermination. Nature 364, 401-406 (1993).
10. Friedman, D.I. & Court, D.L. Transcription antitermination: the lambda paradigm updated. Mol. Microbiol. 18, 191-200 (1995).
11. Weisberg, R.A. & Gottesman, M.E. Processive antitermination. J. Bacteriol. 181, 359-367 (1999).
12. Van Gilst, M.R. & von Hippel, P.H. Assembly of the N-dependent antitermination complex of phage lambda: NusA and RNA bind independently to different unfolded domains of the N protein. J. Mol. Biol. 274, 160-173 (1997).
13. Mogridge, J., Mah, T.F. & Greenblatt, J. A protein-RNA interaction network facilitates the template-independent cooperative assembly on RNA polymerase of a stable antitermination complex containing the lambda N protein. Genes Dev. 9, 2831-2845 (1995).
14. Zhou, Y. et al. 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 (2001).
15. Murakami, K.S., Masuda, S., Campbell, E.A., Muzzin, O. & Darst, S.A. Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science 296, 1285-1290 (2002).
16. Gusarov, I. & Nudler, E. Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell 107, 437-449 (2001).
17. Legault, P., Li, J., Mogridge, J., Kay, L.E. & Greenblatt, J. NMR structure of the bacteriophage lambda N peptide/boxB RNA complex: recognition of a GNRA fold by an arginine-rich motif. Cell 93, 289-299 (1998).
18. Scharpf, M. et al. Antitermination in bacteriophage lambda. The structure of the N36 peptide-boxB RNA complex. Eur. J. Biochem. 267, 2397-2408 (2000).
19. Su, L. et al. RNA recognition by a bent alpha-helix regulates transcriptional antitermination in phage lambda. Biochemistry 36, 12722-12732 (1997).
20. Jucker, F.M., Heus, H.A., Yip, P.F., Moors, E.H. & Pardi, A. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 264, 968-980 (1996).
21. Heus, H.A. & Pardi, A. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science 253, 191-194 (1991).
22. Franklin, N.C. Clustered arginine residues of bacteriophage lambda N protein are essential to antitermination of transcription, but their locale cannot compensate for boxB loop defects. J. Mol. Biol. 231, 343-360 (1993).
23. Barrick, J.E., Takahashi, T.T., Ren, J., Xia, T. & Roberts, R.W. Large libraries reveal diverse solutions to an RNA recognition problem. Proc. Natl. Acad. Sci. USA 98, 12374-12378 (2001).
24. Barrick, J.E., Takahashi, T.T., Balakin, A. & Roberts, R.W. Selection of RNA-binding peptides using mRNA-peptide fusions. Methods 23, 287-293 (2001).
25. Barrick, J.E. & Roberts. R.W. Sequence analysis of an artificial family of RNA-binding peptides. Protein Sci. 11, 2688-2696 (2002).
26. Xia, T. et al. The RNA-protein complex: direct probing of the interfacial recognition dynamics and its correlation with biological functions. Proc. Natl. Acad. Sci. USA 100, 8119-8123 (2003).
27. Cai, Z. et al. Solution structure of P22 transcriptional antitermination N peptide-boxB RNA complex. Nat. Struct. Biol. 5, 203-212 (1998).
28. Harada, K., Martin, S.S. & Frankel, A.D. Selection of RNA-binding peptides in vivo. Nature 380, 175-179 (1996).
29. Doelling, J.H. & Franklin, N.C. Effects of all single base substitutions in the loop of boxB on antitermination of transcription by bacteriophage lambda's N protein. Nucleic Acids Res. 17, 5565-5577 (1989).
30. Das, A. et al. Components of multiprotein-RNA complex that controls transcription elongation in Escherichia coli phage lambda. Methods Enzymol. 274, 374-402 (1996).
31. Friedman, D.I. In The Bacteriophages vol. 2 (ed. Calendar, R.) 263-318 (Plenum, New York, 1988).
32. Whalen, W., Ghosh, B. & Das, A. NusA protein is necessary and sufficient in vitro for phage lambda N gene product to suppress a rho-independent terminator placed downstream of nutL. Proc. Natl. Acad. Sci. USA 85, 2494-2498 (1988).
33. Gill, S.C., Weitzel, S.E. & von Hippel, P.H. Escherichia coli sigma 70 and NusA proteins. I. Binding interactions with core RNA polymerase in solution and within the transcription complex. J. Mol. Biol. 220, 307-324 (1991).
34. Mason, S.W., Li, J. & Greenblatt, J. 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 (1992).
35. Rees, W.A., Weitzel, S.E., Yager, T.D., Das, A. & von Hippel, P.H. Bacteriophage lambda N protein alone can induce transcription antitermination in vitro. Proc. Natl. Acad. Sci. USA 93, 342-346 (1996).
36. Chattopadhyay, S., Garcia-Mena, J., DeVito, J., Wolska, K. & Das, A. Bipartite function of a small RNA hairpin in transcription antitermination in bacteriophage lambda. Proc. Natl. Acad. Sci. USA 92, 4061-4065 (1995).
37. Mogridge, J. et al. Independent ligand-induced folding of the RNA-binding domain and two functionally distinct antitermination regions in the phage lambda N protein. Mol. Cell. 1, 265-275 (1998).
38. Barik, S., Ghosh, B., Whalen, W., Lazinski, D. & Das, A. An antitermination protein engages the elongating transcription apparatus at a promoter-proximal recognition site. Cell 50, 885-899 (1987).
39. Mason, S.W. & Greenblatt, J. 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 (1991).
40. Toulokhonov, I., Artsimovitch, I. & Landick, R. Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science 292, 730-733 (2001).
41. Marciniak, R.A., Calnan, B.J., Frankel, A.D. & Sharp, P.A. HIV-1 Tat protein transactivates transcription in vitro. Cell 63, 791-802 (1990).
42. Richter, S., Ping, Y.H. & Rana, T.M. TAR RNA loop: a scaffold for the assembly of a regulatory switch in HIV replication. Proc. Natl. Acad. Sci. USA 99, 7928-7933 (2002).
43. Steinmetz, E.J. & Brow, D.A. Repression of gene expression by an exogenous sequence element acting in concert with a heterogeneous nuclear ribonucleoprotein-like protein, Nrd1, and the putative helicase Sen1. Mol. Cell. Biol. 6, 6993-7003 (1996).
44. Steinmetz, E.J. & Brow, D.A. Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc. Natl. Acad. Sci. USA 95, 6699-6704 (1998).
45. Steinmetz, E.J., Conrad, N.K., Brow, D.A. & Corden, J.L. RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413, 327-331 (2001).
46. Austin, R.J., Xia, T., Ren, J., Takahashi, T.T. & Roberts, R.W. Designed arginine-rich RNA-binding peptides with picomolar affinity. J. Am. Chem. Soc. 124, 10966-10967 (2002).
47. Milligan, J.F., Groebe, D.R., Witherell, G.W. & Uhlenbeck, O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15, 8783-8798 (1987).
48. Rees, W.A., Weitzel, S.E., Das, A. & von Hippel, P.H. Regulation of the elongation-termination decision at intrinsic terminators by antitermination protein N of phage lambda. J. Mol. Biol. 273, 797-813 (1997).
49. Peled-Zehavi, H., Smith, C.A., Harada, K. & Frankel, A.D. Screening RNA-binding libraries by transcriptional antitermination in bacteria. Methods Enzymol. 318, 297-308 (2000).