Home LiteratureArticle Details
PMID: 20423906 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Active and passive mechanisms of helicases.

Nucleic acids research ·Vol. 38 ·No. 16 ·2010-09-00 ·Pages 5518-26

Manosas M, Xi XG, Bensimon D, Croquette V

Abstract

In this work, we discuss the active or passive character of helicases. In the past years, several studies have used the theoretical framework proposed by Betterton and Julicher [Betterton, M.D. and Julicher, F. (2005) Opening of nucleic-acid double strands by helicases: active versus passive opening. Phys. Rev. E, 71, 11904-11911.] to analyse the unwinding data and assess the mechanism of the helicase under study (active versus passive). However, this procedure has given rise to apparently contradictory interpretations: helicases exhibiting similar behaviour have been classified as both active and passive enzymes [Johnson, D.S., Bai, L. Smith, B.Y., Patel, S.S. and Wang, M.D. (2007) Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell, 129, 1299-1309; Lionnet, T., Spiering, M.M., Benkovic, S.J., Bensimon, D. and Croquette, V. (2007) Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism Proc. Natl Acid. Sci., 104, 19790-19795]. In this work, we show that when the helicase under study has not been previously well characterized (namely, if its step size and rate of slippage are unknown) a multi-parameter fit to the afore-mentioned model can indeed lead to contradictory interpretations. We thus propose to differentiate between active and passive helicases on the basis of the comparison between their observed translocation velocity on single-stranded nucleic acid and their unwinding rate of double-stranded nucleic acid (with various GC content and under different tensions). A threshold separating active from passive behaviour is proposed following an analysis of the reported activities of different helicases. We study and contrast the mechanism of two helicases that exemplify these two behaviours: active for the RecQ helicase and passive for the gp41 helicase.

MeSH Terms
Biocatalysis DNA/chemistry,metabolism DNA Helicases/metabolism Models, Biological RecQ Helicases/metabolism Viral Proteins/metabolism
Chemicals
Viral Proteins gene 41 protein, Enterobacteria phage T4 DNA RecQ protein, E coli DNA Helicases RecQ Helicases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Manosas Maria
Laboratoire de Physique Statistique, Ecole Normale Superieure, UPMC Univ Paris 06, Universit Paris Diderot, CNRS, 24 rue Lhomond, 75005 Paris, France.
Xi Xu Guang
Bensimon David
Croquette Vincent
References (34)
34 references, click to expand
  1. A zinc ribbon protein in DNA replication: primer synthesis and macromolecular interactions by the bacteriophage T4 primase.
    Biochemistry. 2001 Dec 18;40(50):15074-85 PMID: 11735390
  2. Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome.
    Nat Chem Biol. 2009 Dec;5(12):904-12 PMID: 19838204
  3. T7 DNA helicase: a molecular motor that processively and unidirectionally translocates along single-stranded DNA.
    J Mol Biol. 2002 Aug 30;321(5):807-19 PMID: 12206763
  4. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19790-5 PMID: 18077411
  5. Molecular mechanisms of the functional coupling of the helicase (gp41) and polymerase (gp43) of bacteriophage T4 within the DNA replication fork.
    Biochemistry. 2001 Apr 10;40(14):4459-77 PMID: 11284703
  6. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase.
    Science. 2007 Jul 27;317(5837):513-6 PMID: 17656723
  7. Magnetic tweezers: micromanipulation and force measurement at the molecular level.
    Biophys J. 2002 Jun;82(6):3314-29 PMID: 12023254
  8. The Escherichia coli RecQ helicase functions as a monomer.
    J Biol Chem. 2003 Sep 12;278(37):34925-33 PMID: 12805371
  9. The DNA-unwinding mechanism of the ring helicase of bacteriophage T7.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7264-9 PMID: 15123793
  10. Impediment of E. coli UvrD by DNA-destabilizing force reveals a strained-inchworm mechanism of DNA unwinding.
    EMBO J. 2008 Dec 17;27(24):3279-87 PMID: 19008855
  11. DNA helicases: new breeds of translocating motors and molecular pumps.
    Cell. 1996 Jul 26;86(2):177-80 PMID: 8706121
  12. The replication time of the Escherichia coli K12 chromosome as a function of cell doubling time.
    J Mol Biol. 1975 May 5;94(1):127-32 PMID: 1095767
  13. Slow nucleic acid unzipping kinetics from sequence-defined barriers.
    Eur Phys J E Soft Matter. 2003 Feb;10(2):153-61 PMID: 15011069
  14. Efficient in vitro replication of double-stranded DNA templates by a purified T4 bacteriophage replication system.
    J Biol Chem. 1980 May 10;255(9):4290-3 PMID: 6989836
  15. Opening of nucleic-acid double strands by helicases: active versus passive opening.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2005 Jan;71(1 Pt 1):011904 PMID: 15697627
  16. A general model for nucleic acid helicases and their "coupling" within macromolecular machines.
    Cell. 2001 Jan 26;104(2):177-90 PMID: 11207360
  17. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity.
    Nature. 2000 Mar 2;404(6773):103-6 PMID: 10716452
  18. Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement.
    Cell. 1996 Feb 23;84(4):643-50 PMID: 8598050
  19. Mechanism of ATP-dependent translocation of E.coli UvrD monomers along single-stranded DNA.
    J Mol Biol. 2004 Dec 10;344(5):1287-309 PMID: 15561144
  20. DINAMelt web server for nucleic acid melting prediction.
    Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W577-81 PMID: 15980540
  21. Replication by a single DNA polymerase of a stretched single-stranded DNA.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12002-7 PMID: 11050232
  22. Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed.
    Biochemistry. 2000 Jan 11;39(1):205-12 PMID: 10625495
  23. Mechanisms of helicase-catalyzed DNA unwinding.
    Annu Rev Biochem. 1996;65:169-214 PMID: 8811178
  24. The elasticity of a single supercoiled DNA molecule.
    Science. 1996 Mar 29;271(5257):1835-7 PMID: 8596951
  25. Reversible unfolding of single RNA molecules by mechanical force.
    Science. 2001 Apr 27;292(5517):733-7 PMID: 11326101
  26. Unwinding the 'Gordian knot' of helicase action.
    Trends Biochem Sci. 2001 Jan;26(1):47-54 PMID: 11165517
  27. Studies of base pair kinetics by NMR measurement of proton exchange.
    Methods Enzymol. 1995;261:383-413 PMID: 8569504
  28. DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase.
    Nature. 2005 May 19;435(7040):370-3 PMID: 15902262
  29. Autoinhibition of Escherichia coli Rep monomer helicase activity by its 2B subdomain.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10076-81 PMID: 16009938
  30. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase.
    Cell. 2007 Jun 29;129(7):1299-309 PMID: 17604719
  31. NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork.
    Proc Natl Acad Sci U S A. 2007 Aug 28;104(35):13954-9 PMID: 17709749
  32. A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA.
    Mol Cell. 2007 May 11;26(3):335-47 PMID: 17499041
  33. Forward and reverse motion of single RecBCD molecules on DNA.
    Biophys J. 2004 Mar;86(3):1640-8 PMID: 14990491
  34. Nucleic acid unwinding by hepatitis C virus and bacteriophage t7 helicases is sensitive to base pair stability.
    J Biol Chem. 2007 Jul 20;282(29):21116-23 PMID: 17504766
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2010-09-00
Epub
2010-00-27
Pages
5518-26
Language
English
Region
England
NLM ID
0411011
PMCID
PMC2938219
Subset
IM
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