Home LiteratureArticle Details
PMID: 20381500 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

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

Journal of molecular biology ·Vol. 399 ·No. 1 ·2010-05-28 ·Pages 17-30

Herbert KM, Zhou J, Mooney RA, Porta AL, Landick R, Block SM

Abstract

NusG is an essential transcription factor in Escherichia coli that is capable of increasing the overall rate of transcription. Transcript elongation by RNA polymerase (RNAP) is frequently interrupted by pauses of varying durations, and NusG is known to decrease the occupancy of at least some paused states. However, it has not been established whether NusG enhances transcription chiefly by (1) increasing the rate of elongation between pauses, (2) reducing the lifetimes of pauses, or (3) reducing the rate of entry into paused states. Here, we studied transcription by single molecules of RNAP under various conditions of ribonucleoside triphosphate concentration, applied load, and temperature, using an optical trapping assay capable of distinguishing pauses as brief as 1 s. We found that NusG increases the rate of elongation, that is, the pause-free velocity along the template. Because pauses are off-pathway states that compete with elongation, we observed a concomitant decrease in the rate of entry into short-lifetime, paused states. The effects on short pauses and elongation were comparatively modest, however. More dramatic was the effect of NusG on suppressing entry into long-lifetime ("stabilized") pauses. Because a significant fraction of the time required for the transcription of a typical gene may be occupied by long pauses, NusG is capable of exerting a significant modulatory effect on the rates of RNA synthesis. The observed properties of NusG were consistent with a unified model where the function of this accessory factor is to promote transcriptionally downstream motion of the enzyme along the DNA template, which has the effect of forward-biasing RNAP from the pre-translocated state toward the post-translocated state.

MeSH Terms
DNA-Directed RNA Polymerases/metabolism Escherichia coli/enzymology,genetics,metabolism Escherichia coli Proteins/genetics,metabolism Peptide Elongation Factors/genetics,metabolism RNA, Bacterial/metabolism Transcription Factors/genetics,metabolism Transcription, Genetic Translocation, Genetic
Chemicals
Escherichia coli Proteins NusG protein, E coli Peptide Elongation Factors RNA, Bacterial Transcription Factors DNA-Directed RNA Polymerases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Herbert Kristina M
Biophysics Program, Stanford University, Stanford, CA 94305, USA.
Zhou Jing
Mooney Rachel A
Porta Arthur La
Landick Robert
Block Steven M
References (50)
50 references, click to expand
  1. Transcriptional pausing without backtracking.
    Proc Natl Acad Sci U S A. 2009 Jun 2;106(22):8797-8 PMID: 19470457
  2. The single-nucleotide addition cycle in transcription: a biophysical and biochemical perspective.
    Annu Rev Biophys Biomol Struct. 1992;21:379-415 PMID: 1381976
  3. The regulatory roles and mechanism of transcriptional pausing.
    Biochem Soc Trans. 2006 Dec;34(Pt 6):1062-6 PMID: 17073751
  4. Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro.
    J Bacteriol. 1995 Mar;177(5):1388-92 PMID: 7868616
  5. Allosteric control of the RNA polymerase by the elongation factor RfaH.
    Nucleic Acids Res. 2007;35(17):5694-705 PMID: 17711918
  6. Transcriptional fidelity and proofreading by RNA polymerase II.
    Cell. 1998 May 15;93(4):627-37 PMID: 9604937
  7. Picocalorimetry of transcription by RNA polymerase.
    Biophys J. 2005 Dec;89(6):L61-3 PMID: 16239336
  8. Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3' end of the RNA intact and extruded.
    Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1755-60 PMID: 9050851
  9. Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking.
    Cell. 2003 Nov 14;115(4):437-47 PMID: 14622598
  10. NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage lambda.
    J Biol Chem. 1992 Mar 25;267(9):6012-9 PMID: 1532577
  11. Mechanochemical kinetics of transcription elongation.
    Phys Rev Lett. 2007 Feb 9;98(6):068103 PMID: 17358986
  12. Early transcriptional arrest at Escherichia coli rplN and ompX promoters.
    J Biol Chem. 2009 Dec 18;284(51):35702-13 PMID: 19854830
  13. A quaternary transcription termination complex. Reciprocal stabilization by Rho factor and NusG protein.
    J Mol Biol. 1994 Nov 11;243(5):830-9 PMID: 7525972
  14. Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins.
    Science. 2001 Apr 27;292(5517):730-3 PMID: 11326100
  15. A ratchet mechanism of transcription elongation and its control.
    Cell. 2005 Jan 28;120(2):183-93 PMID: 15680325
  16. Requirement for E. coli NusG protein in factor-dependent transcription termination.
    Cell. 1992 Mar 6;68(5):989-94 PMID: 1547498
  17. Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli.
    J Mol Biol. 1998 May 1;278(2):307-16 PMID: 9571053
  18. Sequence-resolved detection of pausing by single RNA polymerase molecules.
    Cell. 2006 Jun 16;125(6):1083-94 PMID: 16777599
  19. A NusG-like protein from Thermotoga maritima binds to DNA and RNA.
    J Bacteriol. 1996 Jul;178(14):4089-98 PMID: 8763936
  20. Antiterminator-dependent modulation of transcription elongation rates by NusB and NusG.
    Mol Microbiol. 1999 Jun;32(6):1296-304 PMID: 10383769
  21. The elongation factor RfaH and the initiation factor sigma bind to the same site on the transcription elongation complex.
    Proc Natl Acad Sci U S A. 2008 Jan 22;105(3):865-70 PMID: 18195372
  22. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals.
    Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7090-5 PMID: 10860976
  23. The flap domain is required for pause RNA hairpin inhibition of catalysis by RNA polymerase and can modulate intrinsic termination.
    Mol Cell. 2003 Nov;12(5):1125-36 PMID: 14636572
  24. Transcription against an applied force.
    Science. 1995 Dec 8;270(5242):1653-7 PMID: 7502073
  25. Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8502-6 PMID: 8078911
  26. Force and velocity measured for single molecules of RNA polymerase.
    Science. 1998 Oct 30;282(5390):902-7 PMID: 9794753
  27. Regulation of rho-dependent transcription termination by NusG is specific to the Escherichia coli elongation complex.
    Biochemistry. 2000 May 9;39(18):5573-85 PMID: 10820031
  28. Diversity in the rates of transcript elongation by single RNA polymerase molecules.
    J Biol Chem. 2004 Jan 30;279(5):3292-9 PMID: 14604986
  29. Translocation by T7 RNA polymerase: a sensitively poised Brownian ratchet.
    J Mol Biol. 2006 Apr 21;358(1):241-54 PMID: 16516229
  30. The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase.
    Cell. 1997 Apr 4;89(1):33-41 PMID: 9094712
  31. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators.
    J Mol Biol. 2009 Aug 14;391(2):341-58 PMID: 19500594
  32. Pulling on the nascent RNA during transcription does not alter kinetics of elongation or ubiquitous pausing.
    Mol Cell. 2006 Jul 21;23(2):231-9 PMID: 16857589
  33. Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader.
    Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16131-6 PMID: 18852477
  34. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand.
    Cell. 2002 Apr 19;109(2):193-203 PMID: 12007406
  35. Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription.
    Science. 1993 Nov 5;262(5135):867-73 PMID: 8235608
  36. Optical trapping.
    Rev Sci Instrum. 2004 Sep;75(9):2787-809 PMID: 16878180
  37. Antitermination by bacteriophage lambda Q protein.
    Cold Spring Harb Symp Quant Biol. 1998;63:319-25 PMID: 10384296
  38. Fluctuations, pauses, and backtracking in DNA transcription.
    Biophys J. 2008 Jan 15;94(2):334-48 PMID: 17720732
  39. Roles of RNA:DNA hybrid stability, RNA structure, and active site conformation in pausing by human RNA polymerase II.
    J Mol Biol. 2001 Aug 10;311(2):265-82 PMID: 11478860
  40. Direct observation of base-pair stepping by RNA polymerase.
    Nature. 2005 Nov 24;438(7067):460-5 PMID: 16284617
  41. Transcription by single molecules of RNA polymerase observed by light microscopy.
    Nature. 1991 Aug 1;352(6334):444-8 PMID: 1861724
  42. Elongation factor NusG interacts with termination factor rho to regulate termination and antitermination of transcription.
    Genes Dev. 1993 Jan;7(1):161-72 PMID: 8422985
  43. Structural basis for converting a general transcription factor into an operon-specific virulence regulator.
    Mol Cell. 2007 Apr 13;26(1):117-29 PMID: 17434131
  44. A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing.
    Mol Cell. 2007 Aug 3;27(3):406-19 PMID: 17679091
  45. Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13677-82 PMID: 8942993
  46. In vivo effect of NusB and NusG on rRNA transcription antitermination.
    J Bacteriol. 2004 Mar;186(5):1304-10 PMID: 14973028
  47. Sequence and transcriptional pattern of the essential Escherichia coli secE-nusG operon.
    J Bacteriol. 1990 Mar;172(3):1621-7 PMID: 2137819
  48. Downstream DNA selectively affects a paused conformation of human RNA polymerase II.
    J Mol Biol. 2004 Aug 6;341(2):429-42 PMID: 15276834
  49. Mechanism of sequence-specific pausing of bacterial RNA polymerase.
    Proc Natl Acad Sci U S A. 2009 Jun 2;106(22):8900-5 PMID: 19416863
  50. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution.
    Nature. 2003 Dec 11;426(6967):684-7 PMID: 14634670
Article Info
Journal
Journal of molecular biology
Abbr.
J Mol Biol
ISSN
1089-8638
Published
2010-05-28
Epub
2010-00-08
Pages
17-30
Language
English
Region
England
NLM ID
2985088R
PMCID
PMC2875378
Subset
IM
Grants
NIGMS NIH HHS · R01 GM057035 · United States
NIGMS NIH HHS · R01 GM057035-13 · United States
NIGMS NIH HHS · R37 GM057035 · United States
NIGMS NIH HHS · R37 GM057035-14 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com