Dda helicase tightly couples translocation on single-stranded DNA to unwinding of duplex DNA: Dda is an optimally active helicase

Journal of Molecular Biology

Volumn 420, Issue 3, 2012, Pages 141-154

  Byrd, Alicia K ^a   Matlock, Dennis L ^b   Bagchi, Debjani ^c   Aarattuthodiyil, Suja ^a   Harrison, David ^a   Croquette, Vincent ^c   Raney, Kevin D ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b HARDING UNIVERSITY   (United States)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

DNA; fluorescence; molecular motor; single molecule; stopped flow

Indexed keywords

DDA HELICASE; DOUBLE STRANDED DNA; HELICASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA DENATURATION; ENZYME ACTIVITY; PRIORITY JOURNAL; VELOCITY;

EID: 84861998735     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.04.007     Document Type: Article

References (57)

1. Dillingham M.S. Superfamily I helicases as modular components of DNA-processing machines Biochem. Soc. Trans. 39 2011 413 423
2. Bustamante C., Cheng W., and Mejia Y.X. Revisiting the central dogma one molecule at a time Cell 144 2011 480 497
3. Maher R.L., Branagan A.M., and Morrical S.W. Coordination of DNA replication and recombination activities in the maintenance of genome stability J. Cell. Biochem. 112 2011 2672 2682
4. Lohman T.M. Escherichia coli DNA helicases: mechanisms of DNA unwinding Mol. Microbiol. 6 1992 5 14
5. Manosas M., Xi X.G., Bensimon D., and Croquette V. Active and passive mechanisms of helicases Nucleic Acids Res. 38 2010 5518 5526
6. Gauss P., Park K., Spencer T.E., and Hacker K.J. DNA helicase requirements for DNA replication during bacteriophage T4 infection J. Bacteriol. 176 1994 1667 1672
7. Kodadek T., and Alberts B.M. Stimulation of protein-directed strand exchange by a DNA helicase Nature 326 1987 312 314
8. Jongeneel C.V., Formosa T., and Alberts B.M. Purification and characterization of the bacteriophage T4 dda protein. A DNA helicase that associates with the viral helix-destabilizing protein J. Biol. Chem. 259 1984 12925 12932
9. Raney K.D., and Benkovic S.J. Bacteriophage T4 Dda helicase translocates in a unidirectional fashion on single-stranded DNA J. Biol. Chem. 270 1995 22236 22242
10. Morris P.D., and Raney K.D. DNA helicases displace streptavidin from biotin-labeled oligonucleotides Biochemistry 38 1999 5164 5171
11. Morris P.D., Tackett A.J., Babb K., Nanduri B., Chick C., Scott J., and Raney K.D. Evidence for a functional monomeric form of the bacteriophage T4 Dda helicase. Dda does not form stable oligomeric structures J. Biol. Chem. 276 2001 19691 19698
12. Nanduri B., Byrd A.K., Eoff R.L., Tackett A.J., and Raney K.D. Pre-steady-state DNA unwinding by bacteriophage T4 Dda helicase reveals a monomeric molecular motor Proc. Natl Acad. Sci. USA 99 2002 14722 14727
13. Eoff R.L., and Raney K.D. Kinetic mechanism for DNA unwinding by multiple molecules of Dda helicase aligned on DNA Biochemistry 49 2010 4543 4553
14. Byrd A.K., and Raney K.D. Increasing the length of the single-stranded overhang enhances unwinding of duplex DNA by bacteriophage T4 Dda helicase Biochemistry 44 2005 12990 12997
15. Byrd A.K., and Raney K.D. Protein displacement by an assembly of helicase molecules aligned along single-stranded DNA Nat. Struct. Mol. Biol. 11 2004 531 538
16. Byrd A.K., and Raney K.D. Displacement of a DNA binding protein by Dda helicase Nucleic Acids Res. 34 2006 3020 3029
17. Tackett A.J., Morris P.D., Dennis R., Goodwin T.E., and Raney K.D. Unwinding of unnatural substrates by a DNA helicase Biochemistry 40 2001 543 548
18. Eoff R.L., and Raney K.D. Intermediates revealed in the kinetic mechanism for DNA unwinding by a monomeric helicase Nat. Struct. Mol. Biol. 13 2006 242 249
19. Young M.C., Kuhl S.B., and von Hippel P.H. Kinetic theory of ATP-driven translocases on one-dimensional polymer lattices J. Mol. Biol. 235 1994 1436 1446
20. Dillingham M.S., Wigley D.B., and Webb M.R. Direct measurement of single-stranded DNA translocation by PcrA helicase using the fluorescent base analogue 2-aminopurine Biochemistry 41 2002 643 651
21. Lucius A.L., Maluf N.K., Fischer C.J., and Lohman T.M. General methods for analysis of sequential n-step kinetic mechanisms: application to single turnover kinetics of helicase-catalyzed DNA unwinding Biophys. J. 85 2003 2224 2239
22. Lionnet T., Dawid A., Bigot S., Barre F.X., Saleh O.A., and Heslot F. DNA mechanics as a tool to probe helicase and translocase activity Nucleic Acids Res. 34 2006 4232 4244
23. Sun B., Johnson D.S., Patel G., Smith B.Y., Pandey M., Patel S.S., and Wang M.D. ATP-induced helicase slippage reveals highly coordinated subunits Nature 478 2011 132 135
24. Dessinges M.N., Lionnet T., Xi X.G., Bensimon D., and Croquette V. Single-molecule assay reveals strand switching and enhanced processivity of UvrD Proc. Natl Acad. Sci. USA 101 2004 6439 6444
25. Dillingham M.S., Wigley D.B., and Webb M.R. Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed Biochemistry 39 2000 205 212
26. Tomko E.J., Fischer C.J., Niedziela-Majka A., and Lohman T.M. A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA Mol. Cell 26 2007 335 347
27. Tomko E.J., Ja H., Park J., Maluf N.K., Ha T., and Lohman T.M. 5′-Single-stranded/duplex DNA junctions are loading sites for E. coli UvrD translocases EMBO J. 29 2010 3826 3839
28. Rajagopal V., Gurjar M., Levin M.K., and Patel S.S. The protease domain increases the translocation stepping efficiency of the hepatitis C virus NS3-4A helicase J. Biol. Chem. 285 2010 17821 17832
29. Matlock D.L., Yeruva L., Byrd A.K., Mackintosh S.G., Langston C., and Brown C. Investigation of translocation, DNA unwinding, and protein displacement by NS3h, the helicase domain from the hepatitis C virus helicase Biochemistry 49 2010 2097 2109
30. Bianco P.R., Brewer L.R., Corzett M., Balhorn R., Yeh Y., Kowalczykowski S.C., and Baskin R.J. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules Nature 409 2001 374 378
31. Myong S., Rasnik I., Joo C., Lohman T.M., and Ha T. Repetitive shuttling of a motor protein on DNA Nature 437 2005 1321 1325
32. Johnson D.S., Bai L., Smith B.Y., Patel S.S., and Wang M.D. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase Cell 129 2007 1299 1309
33. Lionnet T., Spiering M.M., Benkovic S.J., Bensimon D., and Croquette V. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism Proc. Natl Acad. Sci. USA 104 2007 19790 19795
34. Spies M., Amitani I., Baskin R.J., and Kowalczykowski S.C. RecBCD enzyme switches lead motor subunits in response to χ recognition Cell 131 2007 694 705
35. Myong S., Cui S., Cornish P.V., Kirchhofer A., Gack M.U., and Jung J.U. Cytosolic viral sensor RIG-I is a 5′-triphosphate-dependent translocase on double-stranded RNA Science 323 2009 1070 1074
36. Park J., Myong S., Niedziela-Majka A., Lee K.S., Yu J., Lohman T.M., and Ha T. PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps Cell 142 2010 544 555
37. Wu C.G., Bradford C., and Lohman T.M. Escherichia coli RecBC helicase has two translocase activities controlled by a single ATPase motor Nat. Struct. Mol. Biol. 17 2010 1210 1217
38. Betterton M.D., and Julicher F. Opening of nucleic-acid double strands by helicases: active versus passive opening Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 71 2005 011904
39. Raney K.D., Carver T.E., and Benkovic S.J. Stoichiometry and DNA unwinding by the bacteriophage T4 41:59 helicase J. Biol. Chem. 271 1996 14074 14081
40. Dong F., Weitzel S.E., and von Hippel P.H. A coupled complex of T4 DNA replication helicase (gp41) and polymerase (gp43) can perform rapid and processive DNA strand-displacement synthesis Proc. Natl Acad. Sci. USA 93 1996 14456 14461
41. Kim D.E., Narayan M., and Patel S.S. T7 DNA helicase: a molecular motor that processively and unidirectionally translocates along single-stranded DNA J. Mol. Biol. 321 2002 807 819
42. Donmez I., Rajagopal V., Jeong Y.J., and Patel S.S. Nucleic acid unwinding by hepatitis C virus and bacteriophage T7 helicases is sensitive to base pair stability J. Biol. Chem. 282 2007 21116 21123
43. Stano N.M., Jeong Y.J., Donmez I., Tummalapalli P., Levin M.K., and Patel S.S. DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase Nature 435 2005 370 373
44. Sirinakis G., Clapier C.R., Gao Y., Viswanathan R., Cairns B.R., and Zhang Y. The RSC chromatin remodelling ATPase translocates DNA with high force and small step size EMBO J. 30 2011 2364 2372
45. Bedinger P., Hochstrasser M., Victor Jongeneel C., and Alberts B.M. Properties of the T4 bacteriophage DNA replication apparatus: the T4 dda DNA helicase is required to pass a bound RNA polymerase molecule Cell 34 1983 115 123
46. Bedrosian C.L., and Bastia D. Escherichia coli replication terminator protein impedes simian virus 40 (SV40) DNA replication fork movement and SV40 large tumor antigen helicase activity in vitro at a prokaryotic terminus sequence Proc. Natl Acad. Sci. USA 88 1991 2618 2622
47. Yancey-Wrona J.E., and Matson S.W. Bound Lac repressor protein differentially inhibits the unwinding reactions catalyzed by DNA helicases Nucleic Acids Res. 20 1992 6713 6721
48. Azvolinsky A.S., Dunaway S., Torres J.Z., Bessler J.B., and Zakian V.A. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes Genes Dev. 20 2006 3104 3116
49. Guy C.P., Atkinson J., Gupta M.K., Mahdi A., Gwynn E.J., and Rudolph C.J. Rep provides a second motor at the replisome to promote duplication of protein-bound DNA Mol. Cell 36 2009 654 666
50. Antony E., Tomko Q., Xiao L., Krejci L., Lohman T.M., and Ellengerger T. Srs2 disassembles Rad51 filaments by a protein-protein interaction triggering ATP turnover and dissociation of Rad51 from DNA Mol. Cell 35 2009 105 115
51. Boule J.B., Vega L.R., and Zakian V.A. The yeast Pif1p helicase removes telomerase from telomeric DNA Nature 438 2005 57 61
52. Liao J.C., Jeong Y.J., Kim D.E., Patel S.S., and Oster G. Mechanochemistry of T7 DNA helicase J. Mol. Biol. 350 2005 452 475
53. Adelman J.L., Jeong Y.J., Liao J.C., Patel G., Kim D.E., Oster G., and Patel S.S. Mechanochemistry of transcription termination factor Rho Mol. Cell 22 2006 611 621
54. Wang Q., Arnold J.J., Uchida A., Raney K.D., and Cameron C.E. Phosphate release contributes to the rate-limiting step for unwinding by an RNA helicase Nucleic Acids Res. 38 2010 1312 1324
55. Manosas M., Spiering M.M., Zhuang Z., Benkovic S.J., and Croquette V. Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome Nat. Chem. Biol. 5 2009 904 912
56. Johnson K.A., Simpson Z.B., and Blom T. Global Kinetic Explorer: a new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387 2009 20 29
57. Gosse C., and Croquette V. Magnetic tweezers: micromanipulation and force measurement at the molecular level Biophys. J. 82 2002 3314 3329