Translocation of Escherichia coli RNA polymerase against a protein roadblock in vivo highlights a passive sliding mechanism for transcript elongation

Molecular Microbiology

Volumn 51, Issue 5, 2004, Pages 1471-1481

  Mosrin Huaman, Christine ^a   Turnbough Jr , Charles L ^b   Rahmouni, A Rachid ^a  

^a CENTRE DE BIOPHYSIQUE MOLÉCULAIRE   (France)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOSIDE TRIPHOSPHATE; NUCLEOTIDE; PROTEIN; RNA; RNA POLYMERASE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA TEMPLATE; ESCHERICHIA COLI; GENE CONTROL; IN VIVO STUDY; INTRACELLULAR SPACE; KINETICS; LAC REPRESSOR GENE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REPRESSOR GENE; TRANSCRIPTION ELONGATION;

BACTERIAL PROTEINS; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MACROMOLECULAR SUBSTANCES; NUCLEOTIDES; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 1542616348     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2003.03926.x     Document Type: Article

References (52)

1. Alper, M.D., and Ames, B.N. (1978) Transport of antibiotics and metabolite analogs by systems under cyclic AMP control: positive selection of Salmonella typhimurium cya and crp mutants. J Bacteriol 133: 149-157.
2. Artsimovitch, I., and Landick, R. (2000) Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc Natl Acad Sci USA 97: 7090-7095.
3. Beletskii, A., Grigoriev, A., Joyce, S., and Bhagwat, A.S. (2000) Mutations induced by bacteriophage T7 RNA polymerase and their effects on the composition of the T7 genome. J Mol Biol 300: 1057-1065.
4. Bonekamp, F., Clemmesen, K., Karlstrom, O., and Jensen, K.F. (1984) Mechanism of UTP-modulated attenuation at the pyrE gene of Escherichia coli: an example of operon polarity control through the coupling of translation to transcription. EMBO J 3: 2857-2861.
5. Brosius, J. (1984) Plasmid vectors for the selection of promoters. Gene 27: 151-160.
6. Burns, C.M., Richardson, L.V., and 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.
7. Burova, E., Hung, S.C., Sagitov, V., Stitt, B.L., and Gottesman, M.E. (1995) Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro. J Bacteriol 177: 1388-1392.
8. Cheng, Y., Dylla, S.M., and Turnbough, C.L., Jr (2001) A long T. A tract in the upp initially transcribed region is required for regulation of upp expression by UTP-dependent reiterative transcription in Escherichia coli. J Bacteriol 183:221-228.
9. Das, A. (1992) How the phage lambda N gene product suppresses transcription termination: communication of RNA polymerase with regulatory proteins mediated by signals in nascent RNA. J Bacteriol 17: 6711-6716.
10. Davenport, R.J., Wuite, G.J.L, Landick, R., and Bustamante, C. (2000) Single-molecule study of transcriptional pausing and arrest by E. coli RNA polymerase. Science 287: 2497-2500.
11. Donahue, J.P., and Turnbough, C.L., Jr (1994) Nucleotide-specific transcriptional pausing in the pyrBI leader region of Escherichia coli K-12. J Biol Chem 269: 18185-18191.
12. Dworkin, J., and Losick, R. (2002) Does RNA polymerase help drive chromosome segregation in bacteria? Proc Natl Acad Sci USA 99: 14089-14094.
13. Epshtein, V., Mustaev, A., Markovtsov, V., Bereshchenko, O., Nikiforov, V., and Goldfarb, A. (2002) Swing-gate model of nucleotide entry into the RNA polymerase active center. Mol Cell 10: 623-634.
14. Figueroa-Bossi, N., Guérin, M., Rahmouni, R., Leng, M., and Bossi, L. (1998) The supercoiling sensitivity of a bacterial tRNA promoter parallels its responsiveness to stringent control. EMBO J 17: 2359-2367.
15. Forde, N.R., Izhaky, D., Woodcock, G.R., Wuite, G.J., and Bustamante, C. (2002) Using mechanical force to probe the mechanism of pausing and arrest during continuous elongation by Escherichia coli RNA polymerase. Proc Natl Acad Sci USA 99: 11682-11687.
16. Gaal, T., Bartlett, M.S., Ross, W., Turnbough, C.L., Jr, and Gourse, R.L. (1997) Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278: 2092-2097.
17. Gelles, J., and Landick, R. (1998) RNA polymerase as a molecular motor. Cell 93: 13-16.
18. Guajardo, R., and Sousa, R. (1997) A model for the mechanism of polymerase translocation. J Mol Biol 265: 8-19.
19. Guajardo, R., and Sousa, R. (1999) Characterization of the effects of Escherichia coli replication terminator protein (Tus) on transcription reveals dynamic nature of the Tus block to transcription complex progression. Nucleic Acids Res 27: 2814-2824.
20. Guajardo, R., Lopez, P., Dreyfus, M., and Sousa, R. (1998) NTP concentration effects on initial transcription by T7 RNAP indicate that translocation occurs through passive sliding and reveal that divergent promoters have distinct NTP concentration requirements for productive initiation. J Mol Biol 281: 777-792.
21. Guérin, M., Leng, M., and Rahmouni, A.R. (1996) High resolution mapping of E. coli transcription elongation complex in situ reveals protein interactions with the non-transcribed strand. EMBO J 15: 5397-5407.
22. Gusarov, I., and Nudler, E. (1999) The mechanism of intrinsic transcription termination. Mol Cell 3: 495-504.
23. von Hippel, P.H. (1998) An integrated model of the transcription complex in elongation, termination, and editing. Science 281: 660-665.
24. von Hippel, P.M., and Pasman, Z. (2003) Reaction pathways in transcript elongation. Biophys Chem 101-102: 401-423.
25. Holmes, S.F., and Erie, D.A. (2003) Downstream DNA sequence effects on transcription elongation: NTP binding induces translocation via a ratchet motion. J Biol Chem 278: 35597-35608.
26. King, R.A., Sen, R., and Weisberg, R.A. (2003) Using a lac repressor roadblock to analyze the E. coli transcription elongation complex. Methods Enzymol (in press).
27. Kingston, R.E., Nierman, W.C., and Chamberlin, M.J. (1981) A direct effect of guanosine tetraphosphate on pausing of Escherichia coli RNA polymerase during RNA chain elongation. J Biol Chem 256: 2787-2797.
28. Komissarova, N., and Kashlev, M. (1997a) Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3′ end of the RNA intact and extruded. Proc Natl Acad Sci USA 94: 1755-1760.
29. Komissarova, N., and Kashlev, M. (1997b) RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J Biol Chem 272: 15329-15338.
30. Korzheva, N., Mustaev, A., Kozlov, M., Malhotra, A., Nikiforov, V., Goldfarb, A., and Darst, S.A. (2000) A structural model of transcription elongation. Science 289: 619-625.
31. Landick, R. (1997) RNA polymerase slides home: pause and termination site recognition. Cell 88: 741-744.
32. Levin, J.R., and Chamberlin, M.J. (1987) Mapping and characterization of transcriptional pause sites in the early genetic region of bacteriophage T7. J Mol Biol 196: 61-84.
33. Liu, C., Heath, L.S., and Turnbough, C.L., Jr (1994) Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation. Genes Dev 8: 2904-2912.
34. Nudler, E. (1999) Transcription elongation: structural basis and mechanisms. J Mol Biol 288: 1-12.
35. Nudler, E., Mustaev, A., Lukhtanov, E., and Goldfarb, A. (1997) The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89: 33-41.
36. Pokholok, D.K., Redlak, M., Turnbough, C.L., Jr, Dylla, S., and Holmes, W.M. (1999) Multiple mechanisms are used for growth rate and stringent control of leuV transcriptional initiation in Escherichia coli. J Bacteriol 181: 5771-5782.
37. Poulsen, P., Bonekamp, F., and Jensen, K.F. (1984) Structure of the Escherichia coli pyrE operon and control of pyrE expression by a UTP modulated intercistronic attenuation. EMBO J 3: 1783-1790.
38. Qi, F., and Turnbough, C.L., Jr (1995) Regulation of codBA operon expression in Escherichia coli by UTP-dependent reiterative transcription and UTP-sensitive transcriptional start site switching. J Mol Biol 254: 552-565.
39. Reeder, T.C., and Hawley, D.K. (1996) Promoter proximal sequences modulate RNA polymerase II elongation by a novel mechanism. Cell 87: 767-777.
40. Rees, W.A., Weitzel, S.E., Das, A., and von Hippel, P.H. (1997) Regulation of the elongation-termination decision at intrinsic terminators by antitermination protein N of phage lambda. J Mol Biol 273: 797-813.
41. Richardson, J.P., and Greenblatt, J. (1996) Control of RNA chain elongation and termination. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 822-848.
42. Roland, K.L., Powell, F.E., and Turnbough, C.L., Jr (1985) Role of translation and attenuation in the control of pyrBI operon expression in Escherichia coli K-12. J Bacteriol 163: 991-999.
43. Sadler, W.C., and Switzer, R.L. (1977) Regulation of Salmonella phosphoribosyl pyrophosphate synthetase activity in vivo. J Biol Chem 252: 8504-8511.
44. Samkurashvili, I., and Luse, D.S. (1998) Structural changes in the RNA polymerase II transcription complex during transition from initiation to elongation. Mol Cell Biol 18: 5343-5354.
45. Schneider, D.A., Gaal, T., and Gourse, R.L. (2002) NTP-sensing by rRNA promoters in Escherichia coli is direct. Proc Natl Acad Sci USA 99: 8602-8607.
46. Sidorenkov, I., Komissarova, N., and Kashlev, M. (1998) Crucial role of the RNA:DNA hybrid in the processivity of transcription. Mol Cell 2: 55-64.
47. Toulmé, F., Guérin, M., Robichon, N., Leng, M., and Rahmouni, A.R. (1999) In vivo evidence for back and forth oscillations of the transcription elongation complex. EMBO J 18: 5052-5060.
48. Toulmé, F., Mosrin-Huaman, C., Sparkowski, J., Das, A., Leng, M., and Rahmouni. A.R. (2000) GreA and GreB proteins revive backtracked RNA polymerase in vivo by promoting transcript trimming. EMBO J 19: 6853-6859.
49. Turnbough, C.L., Jr, Hicks, K.L., and Donahue, J.P. (1983) Attenuation control of pyrBI operon expression in Escherichia coli K-12. Proc Natl Acad Sci USA 80: 368-372.
50. Uptain, S.M., Kane, C.M., and Chamberlin, M.J. (1997) Basic mechanisms of transcript elongation and its regulation. Annu Rev Biochem 66: 117-172.
51. Wilson, H.R., Archer, C.D., Liu, J.K., and Turnbough, C.L., Jr (1992) Translational control of pyrC expression mediated by nucleotide-sensitive selection of transcriptional start sites in Escherichia coli. J Bacteriol 174: 514-524.
52. Zhang, G., Campbell, E.A., Minakhin, L., Richter, C., Severinov, K., and Darst, S.A. (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell 98: 811-824.