1887

Abstract

Gene expression is a fundamental process that is highly conserved from humans to bacteria. The first step in gene expression, transcription, is performed by structurally conserved DNA-dependent RNA polymerases (RNAPs), which results in the synthesis of an RNA molecule from a DNA template. In bacteria, a single species of RNAP is responsible for transcribing both stable RNA (i.e. t- and rRNA) and protein-encoding genes (i.e. mRNA), unlike eukaryotic systems, which use three distinct RNAP species to transcribe the different gene classes (RNAP I transcribes most rRNA, RNAP II transcribes mRNA, and RNAP III transcribes tRNA and 5S rRNA). The versatility of bacterial RNAP is dependent on both dynamic interactions with co-factors and the coding sequence of the template DNA, which allows RNAP to respond appropriately to the transcriptional needs of the cell. Although the majority of the research on gene expression has focused on the initiation stage, regulation of the elongation phase is essential for cell viability and represents an important topic for study. The elongation factors that associate with RNAP are unique and highly conserved among prokaryotes, making disruption of their interactions a potentially important target for antibiotic development. One of the most significant advances in molecular biology over the last decade has been the use of green fluorescent protein (GFP) and its spectral variants to observe the subcellular localization of proteins in live intact cells. This review discusses transcription dynamics with respect to RNAP and its associated transcription elongation factors in the two best-studied prokaryotes, and .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/018549-0
2008-07-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/7/1837.html?itemId=/content/journal/micro/10.1099/mic.0.2008/018549-0&mimeType=html&fmt=ahah

References

  1. Borukhov, S. & Nudler, E. ( 2008; ). RNA polymerase: the vehicle of transcription. Trends Microbiol 16, 126–134.[CrossRef]
    [Google Scholar]
  2. Borukhov, S., Sagitov, V. & Goldfarb, A. ( 1993; ). Transcript cleavage factors from E. coli. Cell 72, 459–466.[CrossRef]
    [Google Scholar]
  3. Borukhov, S., Lee, J. & Laptenko, O. ( 2005; ). Bacterial transcription elongation factors: new insights into molecular mechanism of action. Mol Microbiol 55, 1315–1324.
    [Google Scholar]
  4. Burns, C. M., Richardson, L. V. & Richardson, J. P. ( 1998; ). Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli. J Mol Biol 278, 307–316.[CrossRef]
    [Google Scholar]
  5. Cabrera, J. E. & Jin, D. J. ( 2003; ). The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues. Mol Microbiol 50, 1493–1505.[CrossRef]
    [Google Scholar]
  6. Cabrera, J. E. & Jin, D. J. ( 2006; ). Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J Struct Biol 156, 284–291.[CrossRef]
    [Google Scholar]
  7. Chatterji, D., Ogawa, Y., Shimada, T. & Ishihama, A. ( 2007; ). The role of the omega subunit of RNA polymerase in expression of the relA gene in Escherichia coli. FEMS Microbiol Lett 267, 51–55.[CrossRef]
    [Google Scholar]
  8. Condon, C., Squires, C. & Squires, C. L. ( 1995; ). Control of rRNA transcription in Escherichia coli. Microbiol Rev 59, 623–645.
    [Google Scholar]
  9. Couturier, E. & Rocha, E. P. C. ( 2006; ). Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol Microbiol 59, 1506–1518.[CrossRef]
    [Google Scholar]
  10. Cramer, P., Bushnell, D. A. & Kornberg, R. D. ( 2001; ). Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292, 1863–1876.[CrossRef]
    [Google Scholar]
  11. Davies, K. M. & Lewis, P. J. ( 2003; ). Localization of rRNA synthesis in Bacillus subtilis: characterization of loci involved in transcription focus formation. J Bacteriol 185, 2346–2353.[CrossRef]
    [Google Scholar]
  12. Davies, K. M., Dedman, A. J., van Hork, S. & Lewis, P. J. ( 2005; ). The NusA : RNA polymerase ratio is increased at sites of rRNA synthesis in Bacillus subtilis. Mol Microbiol 57, 366–379.[CrossRef]
    [Google Scholar]
  13. Doherty, G. P., Meredith, D. H. & Lewis, P. J. ( 2006; ). Subcellular partitioning of transcription factors in Bacillus subtilis. J Bacteriol 188, 4101–4110.[CrossRef]
    [Google Scholar]
  14. Erie, D. A., Hgaseyedjavadi, O., Young, M. C. & von Hippel, P. H. ( 1993; ). Multiple RNA polymerase conformations and GreA control of fidelity of transcription. Science 262, 867–873.[CrossRef]
    [Google Scholar]
  15. Greive, S. J., Lins, A. F. & von Hippel, P. H. ( 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.[CrossRef]
    [Google Scholar]
  16. Gruber, T. M. & Gross, C. A. ( 2003; ). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57, 441–466.[CrossRef]
    [Google Scholar]
  17. Gusarov, I. & Nudler, E. ( 2001; ). Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell 107, 437–449.[CrossRef]
    [Google Scholar]
  18. Hirata, A., Klein, B. J. & Murakami, K. S. ( 2008; ). The X-ray crystal structure of RNA polymerase from Archaea. Nature 451, 851–854.[CrossRef]
    [Google Scholar]
  19. Hsu, L. M., Vo, N. V. & Chamberlin, M. J. ( 1995; ). Escherichia coli transcript cleavage factors GreA and GreB stimulate promoter escape and gene expression in vivo and in vitro. Proc Natl Acad Sci U S A 92, 11588–11592.[CrossRef]
    [Google Scholar]
  20. Ingham, C. J., Dennis, J. & Furneaux, P. A. ( 1999; ). Autogenous regulation of transcription termination factor Rho and the requirements for Nus factors in Bacillus subtilis. Mol Microbiol 31, 651–663.[CrossRef]
    [Google Scholar]
  21. Kazmierczak, M. J., Wiedmann, M. & Boor, K. J. ( 2005; ). Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev 69, 527–543.[CrossRef]
    [Google Scholar]
  22. Kolesov, G., Wunderlich, Z., Laikova, O. N., Mikhail, S., Gelfand, M. S. & Mirny, L. A. ( 2007; ). How gene order is influenced by the biophysics of transcription regulation. Proc Natl Acad Sci U S A 104, 13948–13953.[CrossRef]
    [Google Scholar]
  23. Koulich, D., Nikiforov, V. & Borukhov, S. ( 1998; ). Distinct functions of N and C-terminal domains of GreA, an Escherichia coli transcript cleavage factor. J Mol Biol 276, 379–389.[CrossRef]
    [Google Scholar]
  24. Landick, R., Turnbough, C., Jr & Yanofsky, C. ( 1996; ). Transcription attenuation. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 1263–1286. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  25. Leake, M. C., Chandler, J. H., Wadhams, G. H., Bai, F., Berry, R. M. & Armitage, J. P. ( 2006; ). Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443, 355–358.[CrossRef]
    [Google Scholar]
  26. Lewis, P. ( 2007; ). The organisation of transcription and translation. In Bacillus: Cellular and Molecular Biology, pp. 135–166. Edited by P. Graumann. Norwich, UK: Horizon Press.
  27. Lewis, P. J. & Marston, A. L. ( 1999; ). GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227, 101–109.[CrossRef]
    [Google Scholar]
  28. Lewis, P. J., Thaker, S. D. & Errington, J. ( 2000; ). Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19, 710–718.[CrossRef]
    [Google Scholar]
  29. Li, J., Mason, S. W. & Greenblatt, J. ( 1993; ). Elongation factor NusG interacts with termination factor Rho to regulate termination and antitermination of transcription. Genes Dev 7, 161–172.[CrossRef]
    [Google Scholar]
  30. Minakhin, L., Bhagat, S., Brunning, A., Campbell, E. A., Darst, S. A., Ebright, R. H. & Severinov, K. ( 2001; ). Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. Proc Natl Acad Sci U S A 98, 892–897.[CrossRef]
    [Google Scholar]
  31. Mukherjee, K., Nagai, H., Shimamoto, N. & Chatterji, D. ( 1999; ). GroEL is involved in activation of Escherichia coli RNA polymerase devoid of the omega subunit in vivo. Eur J Biochem 266, 228–235.[CrossRef]
    [Google Scholar]
  32. Opalka, N., Chlenov, M., Chacon, P., Rice, W. J., Wriggers, W. & Darst, S. A. ( 2003; ). Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 114, 335–345.[CrossRef]
    [Google Scholar]
  33. Orlova, M., Newlands, J., Das, A., Goldfarb, A. & Borukhov, S. ( 1995; ). Intrinsic transcript cleavage activity of RNA polymerase. Proc Natl Acad Sci U S A 92, 4596–4600.[CrossRef]
    [Google Scholar]
  34. Pasman, Z. & von Hippel, P. H. ( 2000; ). Regulation of Rho-dependent transcription termination by NusG is specific to the Escherichia coli elongation complex. Biochemistry 39, 5573–5585.[CrossRef]
    [Google Scholar]
  35. Potrykus, K., Vinella, D., Murphy, H., Szalweska-Palasz, A., D'Ari, R. & Cashel, M. ( 2006; ). Antagonistic regulation of Escherichia coli ribosomal RNA rrnB P1 promoter activity by GreA and DksA. J Biol Chem 281, 15238–15248.[CrossRef]
    [Google Scholar]
  36. Reyes-Lamothe, R., Possoz, C., Danilova, O. & Sherratt, D. J. ( 2008; ). Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133, 90–102.[CrossRef]
    [Google Scholar]
  37. Richardson, J. P. & Greenblatt, J. ( 1996; ). Control of RNA chain elongation and termination. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 822–848. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  38. Stepanova, E., Lee, J., Ozerova, M., Semenova, E., Datsenko, K., Wanner, B. L., Severinov, K. & Borukhov, S. ( 2007; ). Analysis of promoter targets for Escherichia coli transcription elongation factor GreA in vivo and in vitro. J Bacteriol 189, 8772–8785.[CrossRef]
    [Google Scholar]
  39. Torres, M., Balada, J.-M., Zellars, M., Squires, C. & Squires, C. L. ( 2004; ). In vivo effect of NusB and NusG on rRNA transcription antitermination. J Bacteriol 186, 1304–1310.[CrossRef]
    [Google Scholar]
  40. Vogel, U. & Jensen, K. F. ( 1994; ). The RNA chain elongation rate in Escherichia coli depends on the growth rate. J Bacteriol 176, 2807–2813.
    [Google Scholar]
  41. Vrentas, C. E., Gaal, T., Ross, W., Ebright, R. H. & Gourse, R. L. ( 2005; ). Response of RNA polymerase to ppGpp: requirement for the omega subunit and relief of this requirement by DksA. Genes Dev 19, 2378–2387.[CrossRef]
    [Google Scholar]
  42. Zellars, M. & Squires, C. L. ( 1999; ). Antiterminator-dependent modulation of transcription elongation rates by NusB and NusG. Mol Microbiol 32, 1296–1304.[CrossRef]
    [Google Scholar]
  43. Zhang, G., Campbell, E. A., Minakhin, L., Richter, C., Severinov, K. & Darst, S. A. ( 1999; ). Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell 98, 811–824.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/018549-0
Loading
/content/journal/micro/10.1099/mic.0.2008/018549-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error