E. coli NusG inhibits backtracking and accelerates pause-free transcription by promoting forward translocation of RNA polymerase

Journal of Molecular Biology

Volumn 399, Issue 1, 2010, Pages 17-30

  Herbert, Kristina M ^a   Zhou, Jing ^a   Mooney, Rachel A ^b   Porta, Arthur La ^c   Landick, Robert ^b   Block, Steven M ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c Bldg 142   (United States)

Author keywords

NusG; Optical tweezers; RNA polymerase; Single molecule biophysics; Transcription

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; ESCHERICHIA COLI PROTEIN; NUCLEOSIDE TRIPHOSPHATE; RNA POLYMERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NUSG; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA TEMPLATE; ESCHERICHIA COLI; GENE FUNCTION; GENE REPRESSION; GENETIC TRANSCRIPTION; MOLECULAR STABILITY; PRIORITY JOURNAL; RNA SYNTHESIS; RNA TRANSLATION; RNA TRANSPORT; TEMPERATURE SENSITIVITY;

ESCHERICHIA COLI;

EID: 77953082083     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.03.051     Document Type: Article

References (50)

1. Downing W.L., Sullivan S.L., Gottesman M.E., Dennis P.P. Sequence and transcriptional pattern of the essential Escherichia coli secE-nusG operon. J. Bacteriol. 1990, 172:1621-1627.
2. Mooney R.A., Schweimer K., Rosch P., Gottesman M., Landick R. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J. Mol. Biol. 2009, 391:341-358.
3. Sullivan S.L., Gottesman M.E. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell 1992, 68:989-994.
4. Li J., Mason S.W., Greenblatt J. Elongation factor NusG interacts with termination factor rho to regulate termination and antitermination of transcription. Genes Dev. 1993, 7:161-172.
5. Nehrke K.W., Platt T. A quaternary transcription termination complex. Reciprocal stabilization by Rho factor and NusG protein. J. Mol. Biol. 1994, 243:830-839.
6. Torres M., Balada J.M., Zellars M., Squires C., Squires C.L. In vivo effect of NusB and NusG on rRNA transcription antitermination. J. Bacteriol. 2004, 186:1304-1310.
7. Zellars M., Squires C.L. Antiterminator-dependent modulation of transcription elongation rates by NusB and NusG. Mol. Microbiol. 1999, 32:1296-1304.
8. Li J., Horwitz R., McCracken S., Greenblatt J. NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage lambda. J. Biol. Chem. 1992, 267:6012-6019.
9. Artsimovitch I., Landick R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl Acad. Sci. USA 2000, 97:7090-7095.
10. Burns C.M., Richardson L.V., Richardson J.P. Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli. J. Mol. Biol. 1998, 278:307-316.
11. Burova E., Hung S.C., Sagitov V., Stitt B.L., Gottesman M.E. Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro. J. Bacteriol. 1995, 177:1388-1392.
12. Yakhnin A.V., Yakhnin H., Babitzke P. Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader. Proc. Natl Acad. Sci. USA 2008, 105:16131-16136.
13. Dalal R.V., Larson M.H., Neuman K.C., Gelles J., Landick R., Block S.M. Pulling on the nascent RNA during transcription does not alter kinetics of elongation or ubiquitous pausing. Mol. Cell 2006, 23:231-239.
14. Herbert K.M., La Porta A., Wong B.J., Mooney R.A., Neuman K.C., Landick R., Block S.M. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 2006, 125:1083-1094.
15. Neuman K.C., Block S.M. Optical trapping. Rev. Sci. Instrum. 2004, 75:2787-2809.
16. Landick R. The regulatory roles and mechanism of transcriptional pausing. Biochem. Soc. Trans. 2006, 34:1062-1066.
17. Toulokhonov I., Landick R. The flap domain is required for pause RNA hairpin inhibition of catalysis by RNA polymerase and can modulate intrinsic termination. Mol. Cell 2003, 12:1125-1136.
18. Komissarova N., Kashlev M. Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3' end of the RNA intact and extruded. Proc. Natl Acad. Sci. USA 1997, 94:1755-1760.
19. Palangat M., Landick R. Roles of RNA:DNA hybrid stability, RNA structure, and active site conformation in pausing by human RNA polymerase II. J. Mol. Biol. 2001, 311:265-282.
20. Nudler E., Mustaev A., Lukhtanov E., Goldfarb A. The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 1997, 89:33-41.
21. Artsimovitch I., Landick R. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 2002, 109:193-203.
22. Palangat M., Hittinger C.T., Landick R. Downstream DNA selectively affects a paused conformation of human RNA polymerase II. J. Mol. Biol. 2004, 341:429-442.
23. Roberts J.W., Yarnell W., Bartlett E., Guo J., Marr M., Ko D.C., et al. Antitermination by bacteriophage lambda Q protein. Cold Spring Harbor Symp. Quant. Biol. 1998, 63:319-325.
24. Shaevitz J.W., Abbondanzieri E.A., Landick R., Block S.M. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 2003, 426:684-687.
25. Erie D.A., Yager T.D., von Hippel P.H. The single-nucleotide addition cycle in transcription: a biophysical and biochemical perspective. Annu. Rev. Biophys. Biomol. Struct. 1992, 21:379-415.
26. Erie D.A., Hajiseyedjavadi O., Young M.C., von Hippel P.H. Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription. Science 1993, 262:867-873.
27. Jeon C., Agarwal K. Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS. Proc. Natl Acad. Sci. USA 1996, 93:13677-13682.
28. Thomas M.J., Platas A.A., Hawley D.K. Transcriptional fidelity and proofreading by RNA polymerase II. Cell 1998, 93:627-637.
29. Schafer D.A., Gelles J., Sheetz M.P., Landick R. Transcription by single molecules of RNA polymerase observed by light microscopy. Nature 1991, 352:444-448.
30. Yin H., Wang M.D., Svoboda K., Landick R., Block S.M., Gelles J. Transcription against an applied force. Science 1995, 270:1653-1657.
31. Wang M.D., Schnitzer M.J., Yin H., Landick R., Gelles J., Block S.M. Force and velocity measured for single molecules of RNA polymerase. Science 1998, 282:902-907.
32. Pasman Z., von Hippel P.H. Regulation of rho-dependent transcription termination by NusG is specific to the Escherichia coli elongation complex. Biochemistry 2000, 39:5573-5585.
33. Bar-Nahum G., Epshtein V., Ruckenstein A.E., Rafikov R., Mustaev A., Nudler E. A ratchet mechanism of transcription elongation and its control. Cell 2005, 120:183-193.
34. Svetlov V., Belogurov G.A., Shabrova E., Vassylyev D.G., Artsimovitch I. Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res. 2007, 35:5694-5705.
35. Abbondanzieri E.A., Shaevitz J.W., Block S.M. Picocalorimetry of transcription RNA polymerase. Biophys. J. 2005, 89:L61-L63.
36. Neuman K.C., Abbondanzieri E.A., Landick R., Gelles J., Block S.M. Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking. Cell 2003, 115:437-447.
37. Bai L., Fulbright R.M., Wang M.D. Mechanochemical kinetics of transcription elongation. Phys. Rev. Lett. 2007, 98:068103.
38. Abbondanzieri E.A., Greenleaf W.J., Shaevitz J.W., Landick R., Block S.M. Direct observation of base-pair stepping by RNA polymerase. Nature 2005, 438:460-465.
39. Guo Q., Sousa R. Translocation by T7 RNA polymerase: a sensitively poised Brownian ratchet. J. Mol. Biol. 2006, 358:241-254.
40. Toulokhonov I., Artsimovitch I., Landick R. Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science 2001, 292:730-733.
41. Donahue B.A., Yin S., Taylor J.S., Reines D., Hanawalt P.C. Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template. Proc. Natl Acad. Sci. USA 1994, 91:8502-8506.
42. Stepanova E., Wang M., Severinov K., Borukhov S. Early transcriptional arrest at Escherichia coli rplN and ompX promoters. J. Biol. Chem. 2009, 284:35702-35713.
43. Kireeva M.L., Kashlev M. Mechanism of sequence-specific pausing of bacterial RNA polymerase. Proc. Natl Acad. Sci. USA 2009, 106:8900-8905.
44. Landick R. Transcriptional pausing without backtracking. Proc. Natl Acad. Sci. USA 2009, 106:8797-8798.
45. Toulokhonov I., Zhang J., Palangat M., Landick R. A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol. Cell 2007, 27:406-419.
46. Voliotis M., Cohen N., Molina-Paris C., Liverpool T.B. Fluctuations, pauses, and backtracking in DNA transcription. Biophys. J. 2008, 94:334-348.
47. Belogurov G.A., Vassylyeva M.N., Svetlov V., Klyuyev S., Grishin N.V., Vassylyev D.G., Artsimovitch I. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol. Cell 2007, 26:117-129.
48. Liao D., Lurz R., Dobrinski B., Dennis P.P. A NusG-like protein from Thermotoga maritima binds to DNA and RNA. J. Bacteriol. 1996, 178:4089-4098.
49. Sevostyanova A., Svetlov V., Vassylyev D.G., Artsimovitch I. The elongation factor RfaH and the initiation factor sigma bind to the same site on the transcription elongation complex. Proc. Natl Acad. Sci. USA 2008, 105:865-870.
50. Tolic-Norrelykke S.F., Engh A.M., Landick R., Gelles J. Diversity in the rates of transcript elongation by single RNA polymerase molecules. J. Biol. Chem. 2004, 279:3292-3299.