RNA Polymerase Pausing Regulates Translation Initiation by Providing Additional Time for TRAP-RNA Interaction

Molecular Cell

Volumn 24, Issue 4, 2006, Pages 547-557

  Yakhnin, Alexander V ^a   Yakhnin, Helen ^a   Babitzke, Paul ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

DNA; RNA

Indexed keywords

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; CELLS, CULTURED; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, BIOLOGICAL; OPERON; PROKARYOTIC INITIATION FACTORS; PROTEIN BINDING; RNA, MESSENGER; RNA-BINDING PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRYPTOPHAN;

BACILLUS SUBTILIS; PROKARYOTA;

EID: 33750972017     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.09.018     Document Type: Article

References (35)

1. Armache K.-J., Kettenberger H., and Cramer P. The dynamic machinery of mRNA elongation. Curr. Opin. Struct. Biol. 15 (2005) 197-203
2. Artsimovitch I., and Landick R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl. Acad. Sci. USA 97 (2000) 7090-7095
3. Artsimovitch I., and Landick R. Interaction of a nascent RNA structure with RNA polymerase is required for hairpin-dependent transcriptional pausing but not for transcript release. Genes Dev. 12 (2000) 3110-3122
4. Artsimovitch I., Svetlov V., Anthony L., Burgess R.R., and Landick R. RNA polymerases from Bacillus subtilis and Escherichia coli differ in recognition of regulatory signals in vitro. J. Bacteriol. 182 (2000) 6027-6035
5. Babitzke P. Regulation of transcription attenuation and translation initiation by allosteric control of an RNA-binding protein: the Bacillus subtilis TRAP protein. Curr. Opin. Microbiol. 7 (2004) 132-139
6. Du H., and Babitzke P. trp RNA-binding attenuation protein-mediated long distance RNA refolding regulates translation of trpE in Bacillus subtilis. J. Biol. Chem. 273 (1998) 20494-20503
7. Gollnick P., and Babitzke P. Transcription attenuation. Biochim. Biophys. Acta 1577 (2002) 240-250
8. Gollnick P., Ishino S., Kuroda M.I., Henner D.J., and Yanofsky C. The mtr locus is a two-gene operon required for transcription attenuation in the trp operon of Bacillus subtilis. Proc. Natl. Acad. Sci. USA 87 (1990) 8726-8730
9. Gollnick P., Babitzke P., Antson A., and Yanofsky C. Complexity in Regulation of Tryptophan Biosynthesis in Bacillus subtilis. Annu. Rev. Genet. 39 (2005) 47-68
10. Gong F., and Yanofsky C. A transcriptional pause synchronizes translation with transcription in the tryptophanase operon leader region. J. Bacteriol. 185 (2003) 6472-6476
11. Grundy F.J., and Henkin T.M. Kinetic analysis of tRNA-directed transcription antitermination of the Bacillus subtilis glyQS gene in vitro. J. Bacteriol. 186 (2004) 5392-5399
12. Henkin T.M., and Yanofsky C. Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. Bioessays 24 (2002) 700-707
13. Hoffman R.J., and Gollnick P. The mtrB gene of Bacillus pumilus encodes a protein with sequence and functional homology to the trp RNA-binding attenuation protein (TRAP) of Bacillus subtilis. J. Bacteriol. 177 (1995) 839-842
14. Kainz M., and Roberts J. Kinetics of RNA polymerase initiation and pausing at the lambda late gene promoter in vivo. J. Mol. Biol. 254 (1995) 808-814
15. Landick R. RNA polymerase slides home: pause and termination site recognition. Cell 88 (1997) 741-744
16. Landick R. Active-site dynamics in RNA polymerases. Cell 116 (2004) 351-353
17. Landick R., Carey J., and Yanofsky C. Detection of transcription-pausing in vivo in the trp operon leader region. Proc. Natl. Acad. Sci. USA 84 (1987) 1507-1511
18. Marr M.T., and Roberts J.W. Function of transcription cleavage factors GreA and GreB at a regulatory pause site. Mol. Cell 6 (2000) 1275-1285
19. Merino E., Babitzke P., and Yanofsky C. trp RNA-binding attenuation protein (TRAP)-trp leader RNA interactions mediate translational as well as transcriptional regulation of the Bacillus subtilis trp operon. J. Bacteriol. 177 (1995) 6362-6370
20. Mironov A.S., Gusarov I., Rafikov R., Lopez L.E., Shatalin K., Kreneva R.A., Perumov D.A., and Nudler E. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111 (2002) 747-756
21. Mooney R.A., Artsimovitch I., and Landick R. Information processing by RNA polymerase: recognition of regulatory signals during RNA chain elongation. J. Bacteriol. 180 (1998) 3265-3275
22. Palangat M., Meier T.I., Keene R.G., and Landick R. Transcriptional pausing at +62 of the HIV-1 nascent RNA modulates formation of the TAR RNA structure. Mol. Cell 1 (1998) 1033-1042
23. Qi Y., and Hulett F.M. PhoP-P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP-P activator sites within the coding region stimulate transcription in vitro. Mol. Microbiol. 28 (1998) 1187-1197
24. Rasmussen E.B., and Lis J.T. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl. Acad. Sci. USA 90 (1993) 7923-7927
25. Sambrook J., and Russell D.W. Molecular Cloning: A Laboratory Manual. Third Edition (2001), Cold Spring Harbor Laboratory Press, New York
26. Sasse-Dwight S., and Gralla J.D. KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo. J. Biol. Chem. 264 (1989) 8074-8081
27. Sha Y., Lindahl L., and Zengel J.M. Role of NusA in L4-mediated attenuation control of the S10 r-protein operon of Escherichia coli. J. Mol. Biol. 245 (1995) 474-485
28. Toulokhonov I., and Landick R. The flap domain is required for pause RNA hairpin inhibition of catalysis by RNA polymerase and can modulate intrinsic termination. Mol. Cell 12 (2003) 1125-1136
29. Valbuzzi A., Gollnick P., Babitzke P., and Yanofsky C. The anti-trp RNA-binding attenuation protein (Anti-TRAP), AT, recognizes the tryptophan-activated RNA binding domain of the TRAP regulatory protein. J. Biol. Chem. 277 (2002) 10608-10613
30. Winkler M.E., and Yanofsky C. Pausing of RNA polymerase during in vitro transcription of the tryptophan operon leader region. Biochemistry 20 (1981) 3738-3744
31. Winkler W., Nahvi A., and Breaker R.R. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419 (2002) 952-956
32. Yakhnin A.V., and Babitzke P. NusA-stimulated RNA polymerase pausing and termination participates in the Bacillus subtilis trp operon attenuation mechanism in vitro. Proc. Natl. Acad. Sci. USA 99 (2002) 11067-11072
33. Yakhnin H., Zhang H., Yakhnin A.V., and Babitzke P. The trp RNA-binding attenuation protein of Bacillus subtilis regulates translation of the tryptophan transport gene trpP (yhaG) by blocking ribosome binding. J. Bacteriol. 186 (2004) 278-286
34. Yang W.J., and Yanofsky C. Effects of tryptophan starvation on levels of the trp RNA-binding attenuation protein (TRAP) and anti-TRAP regulatory protein and their influence on trp operon expression in Bacillus subtilis. J. Bacteriol. 187 (2005) 1884-1891
35. Zhang H., Jorgensen C.M., and Switzer R.L. Mutations affecting transcription pausing in the Bacillus subtilis pyr operon. Arch. Microbiol. 184 (2005) 101-107