Tethering σ70 to RNA polymerase reveals high in vivo activity of σ factors and σ70-dependent pausing at promoter-distal locations

Genes and Development

Volumn 17, Issue 22, 2003, Pages 2839-2851

  Mooney, Rachel Anne ^a   Landick, Robert ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

factor; E. coli; Pausing; RNA polymerase; Transcriptional regulation

Indexed keywords

DNA; ELONGATION FACTOR; PROTEIN; PROTEIN RPOC; PROTEIN RPOD; PROTEIN SIGMA 70; RNA POLYMERASE; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; DNA DIRECTED RNA POLYMERASE; RNA POLYMERASE SIGMA 70; SIGMA FACTOR;

ARTICLE; BACTERIAL STRAIN; BETA CHAIN; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA SEQUENCE; ENZYME RELEASE; ESCHERICHIA COLI; GENE FUSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; THERMODYNAMICS; COMPARATIVE STUDY; ENZYMOLOGY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HEAT; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; SIGMA FACTOR; TRANSCRIPTION, GENETIC;

EID: 0344011547     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1142203     Document Type: Article

References (61)

1. Arndt, K.M. and Chamberlin, M.J. 1988. Transcription termination in Escherichia coli. Measurement of the rate of enzyme release from Rho-independent terminators. J. Mol. Biol. 202: 271-285.
2. Artsimovitch, I. and Landick, R. 2002. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109: 193-203.
3. 70-retaining transcription elongation complexes from Escherichia coli. Cell 106: 443-451.
4. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Quail, M.A., Kieser, H., Harper, D., et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
5. Bremer, H. and Dennis, P. 1996. Modulation of cell parameters by growth rate. In Escherichia coli and Salmonella: Cellular and molecular biology, 2nd ed. (eds. F. Neidhardt et al.), pp. 1553-1569. ASM press, Washington, DC.
6. Burgess, R.R., Travers, A.A., Dunn, J.J., and Bautz, E.K. 1969. Factor stimulating transcription by RNA polymerase. Nature 221: 43-46.
7. Cantor, C.R. and Schimmel, P.R. 1980. Biophysical chemistry. Freeman, New York.
8. Cayley, S., Lewis, B.A., Guttman, H.J., and Record Jr., M.T. 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. J. Mol. Biol. 222: 281-300.
9. Chamberlin, M. 1976. RNA polymerase-An overview. In RNA polymerase (eds. R. Losick and M. Chamberlin), pp. 17-68. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
10. Chan, C. and Landick, R. 1989. The Salmonella typhimurium his operon leader region contains an RNA hairpin-dependent transcription pause site. J. Biol. Chem. 264: 20796-20804.
11. 70 within the transcription elongation complex. Proc. Natl. Acad. Sci. 96:8390-8395.
12. De Las Penas, A., Connolly, L., and Gross, C.A. 1997. σE is an essential σ factor in Escherichia coli. J. Bacteriol. 179: 6862-6864.
13. Ellis, R.J. 2001. Macromolecular crowding: Obvious but under-appreciated. Trends Biochem Sci. 26: 597-604.
14. Farewell, A., Kvint, K., and Nystrom, T. 1998. Negative regulation by RpoS: A case of σ factor competition. Mol. Microbiol. 29: 1039-1051.
15. Flory, P. 1969. Statistical mechanics of chain molecules. Interscience, London.
16. Friedman, D.I., Baumann, M., and Baron, L.S. 1976. Cooperative effects of bacterial mutations affecting λ N gene expression. I. Isolation and characterization of a nusB mutant. Virology 73: 119-127.
17. Fujita, M. and Sadaie, Y. 1998. Promoter selectivity of the Bacillus subtilis RNA polymerase σA and σH holoenzymes. J. Biochem. (Tokyo) 124: 89-97.
18. Gill, S.C., Weitzel, S.E., and von Hippel, P.H. 1991. Escherichia coli σ 70 and NusA proteins. I. Binding interactions with core RNA polymerase in solution and within the transcription complex. J. Mol. Biol. 220: 307-324.
19. Gross, C.A., Chan, C., Dombroski, A., Gruber, T., Sharp, M., Tupy, J., and Young, B. 1998. The functional and regulatory roles of σ factors in transcription. Cold Spring Harb. Symp. Quant. Biol. 63: 141-155.
20. Hicks, K.A. and Grossman, A.D. 1996. Altering the level and regulation of the major σ subunit of RNA polymerase affects gene expression and development in Bacillus subtilis. Mol. Microbiol. 20: 201-212.
21. Hoopes, B.C. and McClure, W.R. 1981. Studies on the selectivity of DNA precipitation by spermine. Nucleic Acids Res. 9: 5493-5504.
22. Ishihama, A. 2000. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 54: 499-518.
23. Jishage, M. and Ishihama, A. 1995. Regulation of RNA polymerase σ subunit synthesis in Escherichia coli: Intracellular levels of σ 70 and σ 38. J. Bacteriol. 177: 6832-6835.
24. Jishage, M., Kvint, K., Shingler, V., and Nystrom, T. 2002. Regulation of σ factor competition by the alarmone ppGpp. Genes & Dev. 16: 1260-1270.
25. Kimura, H., Sugaya, K., and Cook, P.R. 2002. The transcription cycle of RNA polymerase II in living cells. J. Cell Biol. 159: 777-782.
26. Kolesky, S., Ouhammouch, M., Brody, E.N., and Geiduschek, E.P. 1999. σ competition: The contest between bacteriophage T4 middle and late transcription. J. Mol. Biol. 291: 267-281.
27. Krummel, B. and Chamberlin, M.J. 1989. RNA chain initiation by Escherichia coli RNA polymerase. Structural transition of the enzyme in early ternary complexes. Biochemistry 28: 7829-7842.
28. Kumar, A., Grimes, B., Logan, M., Wedgwood, S., Williamson, H., and Hayward, R.S. 1995. A hybrid σ subunit directs RNA polymerase to a hybrid promoter in Escherichia coli. J. Mol. Biol. 246: 563-571.
29. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., Bertero, M.G., Bessieres, P., Bolotin, A., Borchert, S., et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
30. Law, S.M., Bellomy, G.R., Schlax, P.J., and Record Jr., M.T. 1993. In vivo thermodynamic analysis of repression with and without looping in lac constructs, Estimates of free and local lac repressor concentrations and of physical properties of a region of supercoiled plasmid DNA in vivo. J. Mol. Biol. 230: 161-173.
31. Lonetto, M.A., Rhodius, V., Lamberg, K., Kiley, P., Busby, S., and Gross, C. 1998. Identification of a contact site for different transcription activators in region 4 of the Escherichia coli RNA polymerase σ70 subunit. J. Mol. Biol. 284: 1353-1365.
32. Lord, M., Barilla, D., and Yudkin, M.D. 1999. Replacement of vegetative σA by sporulation-specific σF as a component of the RNA polymerase holoenzyme in sporulating Bacillus subtilis. J. Bacteriol. 181: 2346-2350.
33. Maeda, H., Fujita, N., and Ishihama, A. 2000. Competition among seven Escherichia coli σ subunits: Relative binding affinities to the core RNA polymerase. Nucleic Acids Res. 28: 3497-3503.
34. Marr, M.T. and Roberts, J.W. 2000. Function of transcription cleavage factors GreA and GreB at a regulatory pause site. Mol. Cell 6: 1275-1285.
35. Marr, M.T., Datwyler, S.A., Meares, C.F., and Roberts, J.W. 2001. Restructuring of an RNA polymerase holoenzyme elongation complex by lambdoid phage Q proteins. Proc. Natl. Acad. Sci. 98: 8972-8978.
36. McClure, W.R. 1980. Rate-limiting steps in RNA chain initiation. Proc. Natl. Acad. Sci. 77: 5634-5638.
37. Mekler, V., Kortkhonjia, E., Mukhopadhyay, J., Knight, J., Revyakin, A., Kapanidis, A.N., Niu, W., Ebright, Y.W., Levy, R., and Ebright, R.H. 2002. Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell 108: 599-614.
38. 70 with RNA polymerase during transcription: Fluorescence resonance energy transfer assay for movement relative to DNA. Cell 106: 453-463.
39. Murakami, K.S., Masuda, S., Campbell, E.A., Muzzin, O., and Darst, S. 2002. Structural basis of transcription initiation: An RNA polymerase holoenzyme/DNA complex. Science 296: 1285-1290.
40. Pokholok, D.K., Hannett, N.M., and Young, R.A. 2002. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9: 799-809.
41. Raag, R. and Whitlow, M. 1995. Single-chain Fvs. FASEB J. 9: 73-80.
42. Record Jr., M.T., Courtenay, E.S., Cayley, S., and Guttman, H.J. 1998. Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem. Sci. 23: 190-194.
43. 70 in promoter-proximal pausing. Cell 86: 485-493.
44. Robinson, C.R. and Sauer, R.T. 1998. Optimizing the stability of single-chain proteins by linker length and composition mutagenesis. Proc. Natl. Acad. Sci. 95: 5929-5934.
45. Rollenhagen, C., Antelmann, H., Kirstein, J., Delumeau, O., Hecker, M., and Yudkin, M.D. 2003. Binding of σ(A) and σ(B) to core RNA polymerase after environmental stress in Bacillus subtilis. J. Bacteriol. 185: 35-40.
46. R promoter: Large scale conformational changes in forming kinetically significant intermediates. J. Mol. Biol. 319: 649-671.
47. Severinov, K., Mooney, R., Darst, S., and Landick, R. 1997. Tethering of the large subunits of Escherichia coli RNA polymerase. J. Biol. Chem. 272: 24137-24140.
48. Severinova, E., Severinov, K., Fenyo, D., Marr, M., Brody, E.N., Roberts, J.W., Chait, B.T., and Darst, S.A. 1996. Domain organization of the Escherichia coli RNA polymerase σ 70 subunit. J. Mol. Biol. 263: 637-647.
49. Sharp, M.M., Chan, C.L., Lu, C.Z., Marr, M.T., Nechaev, S., Merritt, E.W., Severinov, K., Roberts, J.W., and Gross, C.A. 1999. The interface of σ with core RNA polymerase is extensive, conserved, and functionally specialized. Genes & Dev. 13: 3015-3026.
50. Shimamoto, N., Kamigochi, T., and Utiyama, H. 1986. Release of the σ subunit of Escherichia coli DNA-dependent RNA polymerase depends mainly on time elapsed after the start of initiation, not on length of product RNA. J. Biol. Chem. 261: 11859-11865.
51. Siegele, D.A., Hu, J.C., Walter, W.A., and Gross, C.A. 1989. Altered promoter recognition by mutant forms of the σ 70 subunit of Escherichia coli RNA polymerase. J. Mol. Biol. 206: 591-603.
52. Straus, D.B., Walter, W.A., and Gross, C.A. 1987. The heat shock response of E. coli is regulated by changes in the concentration of σ 32. Nature 329: 348-351.
53. Susa, M., Sen, R., and Shimamoto, N. 2002. Generality of the branched pathway in transcription initiation by Escherichia coli RNA polymerase. J. Biol. Chem. 277: 15407-15412.
54. Taylor, W.E., Straus, D.B., Grossman, A.D., Burton, Z.F., Gross, C. A., and Burgess, R.R. 1984. Transcription from a heat-inducible promoter causes heat shock regulation of the cr subunit of E. coli RNA polymerase. Cell 38: 371-381.
55. + channel inactivation domain. Biophys. J. 69: 2415-2418.
56. Vassylyev, D.G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M.N., Borukhov, S., and Yokoyama, S. 2002. Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature 417: 712-719.
57. Wassarman, K.M. and Storz, G. 2000. 6S RNA regulates E. coli RNA polymerase activity. Cell 101: 613-623.
58. Wu, F.Y., Yarbrough, L.R., and Wu, C.W. 1976. Conformational transition of Escherichia coli RNA polymerase induced by the interaction of σ subunit with core enzyme. Biochemistry 15: 3254-3258.
59. Zhou, Y.N. and Gross, C.A. 1992. How a mutation in the gene encoding σ 70 suppresses the defective heat shock response caused by a mutation in the gene encoding σ 32. J. Bacteriol. 174: 7128-7137.
60. Zhou, Y.N., Kusukawa, N., Erickson, J.W., Gross, C.A., and Yura, T. 1988. Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor σ 32. J. Bacteriol. 170: 3640-3649.
61. Zhou, Y.N., Walter, W.A., and Gross, C.A. 1992. A mutant σ 32 with a small deletion in conserved region 3 of σ has reduced affinity for core RNA polymerase. J. Bacteriol. 174: 5005-5012.