DNA unwinding by ring-shaped T4 helicase gp41 is hindered by tension on the occluded strand

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Ribeck, Noah ^a,b   Saleh, Omar A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Michigan State University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNAB HELICASE; DOUBLE STRANDED DNA; GLYCOPROTEIN GP 41; HELICASE; MOLECULAR MOTOR; SINGLE STRANDED DNA; DNA; DNA HELICASE; DNAB PROTEIN, E COLI; GENE 41 PROTEIN, ENTEROBACTERIA PHAGE T4; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE T4; CONTROLLED STUDY; DNA BINDING; DNA DENATURATION; DNA STRAND; ENZYME ACTIVITY; GENE TRANSLOCATION; PROTEIN DNA INTERACTION; TENSION; CHEMISTRY; CONFORMATION; ENTEROBACTERIA PHAGE T4; ENZYME SPECIFICITY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS;

BACTERIOPHAGE T4; DNA; DNA HELICASES; DNA, SINGLE-STRANDED; DNAB HELICASES; ESCHERICHIA COLI; NUCLEIC ACID CONFORMATION; SUBSTRATE SPECIFICITY; VIRAL PROTEINS;

EID: 84892585537     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079237     Document Type: Article

References (33)

1. Patel SS, Picha KM (2000) Structure and function of hexameric helicases. Annu Rev Biochem 69: 651-697.
2. Hacker KJ, Johnson KA (1997) A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding. Biochemistry 36: 14080-14087.
3. Kaplan DL, Davey MJ, O'Donnell M (2003) Mcm4,6,7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J Biol Chem 278: 49171-49182.
4. Patel SS, Donmez I (2006) Mechanisms of helicases. J Biol Chem 281: 18265-18268.
5. Indiani C, Langston LD, Yurieva O, Goodman MF, O'Donnell M (2009) Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc Natl Acad Sci USA 106: 6031-6038.
6. Ribeck N, Kaplan DL, Bruck I, Saleh OA (2010) DnaB helicase activity is modulated by DNA geometry and force. Biophys J 99: 2170-2179.
7. Ishmael FT, Alley SC, Benkovic SJ (2002) Assembly of the bacteriophage T4 helicase. J Biol Chem 277: 20555-20562.
8. Lionnet T, Spiering MM, Benkovic SJ, Bensimon D, Croquette V (2007) Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc Natl Acad Sci USA 104: 19790-19795.
9. Manosas M, Spiering MM, Zhuang Z, Benkovic SJ, Croquette V (2009) Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nat Chem Biol 5: 904-912.
10. Gosse C, Croquette V (2002) Magnetic tweezers: Micromanipulation and force measurement at the molecular level. Biophys J 82: 3314-3329.
11. Ribeck N, Saleh OA (2008) Multiplexed single-molecule measurements with magnetic tweezers. Rev Sci Instrum 79: 094301.
12. Cheng W, Dumont S, Tinoco I, Bustamante C (2007) NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc Natl Acad Sci USA 104: 13954-13959.
13. Dumont S, Cheng W, Serebrov V, Beran RK, Tinoco I, et al. (2006) RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 439: 105-108.
14. Betterton MD, Julicher F (2003) A motor that makes its own track: Helicase unwinding of DNA. Phys Rev Lett 91: 258103.
15. Betterton MD, Julicher F (2005) Opening of nucleic-acid double strands by helicases: Active versus passive opening. Phys Rev E 71: 011904.
16. Delagoutte E, von Hippel PH (2002) Helicase mechanisms and the coupling of helicases within macromolecular machines Part 1: Structures and properties of isolated helicases. Q Rev Biophys 35: 431-478.
17. Lohman TM, Bjornson KP (1996) Mechanisms of helicase-catalyzed DNA unwinding. Annu Rev Biochem 65: 169-214.
18. Dessinges MN, Lionnet T, Xi XG, Bensimon D, Croquette V (2004) Single-molecule assay reveals strand switching and enhanced processivity of UvrD. Proc Natl Acad Sci USA 101: 6439-6444.
19. Rouzina I, Bloomfield VA (2001) Force-induced melting of the DNA double helix - 1. Thermodynamic analysis. Biophys J 80: 882-893.
20. Johnson DS, Bai L, Smith BY, Patel SS, Wang MD (2007) Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129: 1299-1309.
21. van Mameren J, Gross P, Farge G, Hooijman P, Modesti M, et al. (2009) Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc Natl Acad Sci USA 106: 18231-18236.
22. Guydosh NR, Block SM (2006) Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain. Proc Natl Acad Sci USA 103: 8054-8059.
23. Neuman KC, Abbondanzieri EA, Landick R, Gelles J, Block SM (2003) Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking. Cell 115: 437-447.
24. Itsathitphaisarn O, Wing RA, Eliason WK, Wang J, Steitz TA (2012) The hexameric helicase DnaB adopts a nonplanar conformation during translocation. Cell 151: 267-277.
25. Galletto R, Jezewska MJ, Bujalowski W (2004) Unzipping mechanism of the double-stranded DNA unwinding by a hexameric helicase: The effect of the 3′ arm and the stability of the dsDNA on the unwinding activity of the Escherichia coli DnaB helicase. J Mol Biol 343: 101-114.
26. Jose D, Weitzel SE, Jing D, von Hippel PH (2012) Assembly and subunit stoichiometry of the functional helicase-primase (primosome) complex of bacteriophage T4. Proc Natl Acad Sci USA 109: 13596-13601.
27. Jose D, Weitzel SE, von Hippel PH (2012) Breathing fluctuations in position-specific DNA base pairs are involved in regulating helicase movement into the replication fork. Proc Natl Acad Sci USA 109: 14428-14433.
28. Graham BW, Schauer GD, Leuba SH, Trakselis MA (2011) Steric exclusion and wrapping of the excluded DNA strand occurs along discrete external binding paths during MCM helicase unwinding. Nucleic Acids Res 39: 6585-6595.
29. Rothenberg E, Trakselis MA, Bell SD, Ha T (2007) MCM forked substrate specificity involves dynamic interaction with the 59-tail. J Biol Chem 282: 34229-34234.
30. Bear DG, Hicks PS, Escudero KW, Andrews CL, McSwiggen JA, et al. (1988) Interactions of Escherichia coli transcription termination factor rho with RNA - 2. Election Microscopy and nuclease protection experiments. J Mol Biol 199: 623-635.
31. Yu X, Horiguchi T, Shigesada K, Egelman EH (2000) Three-dimensional reconstruction of transcription termination factor rho: Orientation of the N-terminal domain and visualization of an RNA-binding site. J Mol Biol 299: 1279-1287.
32. Bujalowski W, Jezewska MJ (1995) Interactions of Escherichia coli primary replicative helicase DnaB protein with single-stranded DNA. The nucleic acid does not wrap around the protein hexamer. Biochemistry 34: 8513-8519.
33. Gao DX, McHenry CS (2001) Tau binds and organizes Escherichia coli replication proteins through distinct domains - Domain IV, located within the unique C terminus of tau, binds the replication fork helicase, DnaB. J Biol Chem 276: 4441-4446.