DnaB helicase activity is modulated by DNA geometry and force

Biophysical Journal

Volumn 99, Issue 7, 2010, Pages 2170-2179

  Ribeck, Noah ^a   Kaplan, Daniel L ^b   Bruck, Irina ^b   Saleh, Omar A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI;

EID: 77958475756     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.07.039     Document Type: Article

References (45)

1. LeBowitz, J. H., and R. McMacken. 1986. The Escherichia coli DnaB replication protein is a DNA helicase. J. Biol. Chem. 261:4738-4748.
2. Chandler, M., R. E. Bird, and L. Caro. 1975. The replication time of the Escherichia coli K12 chromosome as a function of cell doubling time. J. Mol. Biol. 94:127-132.
3. Kim, S. S., H. G. Dallmann, K. J. Marians. 1996. Coupling of a replicative polymerase and helicase: a T-DnaB interaction mediates rapid replication fork movement. Cell. 84:643-650.
4. Galletto, R., M. J. Jezewska, and W. Bujalowski. 2004. Unzipping mechanism of the double-stranded DNA unwinding by a hexameric helicase: quantitative analysis of the rate of the dsDNA unwinding, processivity and kinetic step-size of the Escherichia coli DnaB helicase using rapid quench-flow method. J. Mol. Biol. 343:83-99.
5. Indiani, C., L. D. Langston, M. O'Donnell. 2009. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc. Natl. Acad. Sci. USA. 106:6031-6038.
6. Enemark, E. J., and L. Joshua-Tor. 2006. Mechanism of DNA translocation in a replicative hexameric helicase. Nature. 442:270-275.
7. Liao, J. C., Y. J. Jeong, G. Oster. 2005. Mechanochemistry of T7 DNA helicase. J. Mol. Biol. 350:452-475.
8. Thomsen, N. D., and J. M. Berger. 2009. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell. 139:523-534.
9. Singleton, M. R., M. R. Sawaya, D. B. Wigley. 2000. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell. 101:589-600.
10. Lohman, T. M., and K. P. Bjornson. 1996. Mechanisms of helicasecatalyzed DNA unwinding. Annu. Rev. Biochem. 65:169-214.
11. Delagoutte, E., and P. H. von Hippel. 2002. Helicase mechanisms and the coupling of helicases within macromolecular machines. Part I: Structures and properties of isolated helicases. Q. Rev. Biophys. 35:431-478.
12. Betterton, M. D., and F. Jülicher. 2003. A motor that makes its own track: helicase unwinding of DNA. Phys. Rev. Lett. 91:258103.
13. Betterton, M. D., and F. Jülicher. 2005. Opening of nucleic-acid double strands by helicases: active versus passive opening. Phys. Rev. E. 71:011904.
14. Johnson, D. S., L. Bai, M. D. Wang. 2007. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell. 129:1299-1309.
15. Lionnet, T., M. M. Spiering, V. Croquette. 2007. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc. Natl. Acad. Sci. USA. 104:19790-19795.
16. Cheng, W., S. Dumont, C. Bustamante. 2007. NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc. Natl. Acad. Sci. USA. 104:13954-13959.
17. Soultanas, P., M. S. Dillingham, D. B. Wigley. 2000. Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism. EMBO J. 19:3799-3810.
18. Amaratunga, M., and T. M. Lohman. 1993. Escherichia coli Rep helicase unwinds DNA by an active mechanism. Biochemistry. 32: 6815-6820.
19. Dessinges, M. N., T. Lionnet, V. Croquette. 2004. Single-molecule assay reveals strand switching and enhanced processivity of UvrD. Proc. Natl. Acad. Sci. USA. 101:6439-6444.
20. Fischer, C. J., N. K. Maluf, and T. M. Lohman. 2004. Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA. J. Mol. Biol. 344:1287-1309.
21. Yuzhakov, A., J. Turner, and M. O'Donnell. 1996. Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell. 86:877-886.
22. Kobori, J. A., and A. Kornberg. 1982. The Escherichia coli DnaC gene product. II. Purification, physical properties, and role in replication. J. Biol. Chem. 257:13763-13769.
23. Kaplan, D. L., and M. O'Donnell. 2002. DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell. 10:647-657.
24. Ribeck, N., and O. A. Saleh. 2008. Multiplexed single-molecule measurements with magnetic tweezers. Rev. Sci. Instrum. 79:094301.
25. Gosse, C., and V. Croquette. 2002. Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys. J. 82:3314-3329.
26. Berg-Sorensen, K., and H. Flyvbjerg. 2004. Power spectrum analysis for optical tweezers. Rev. Sci. Instrum. 75:594-612.
27. Klaue, D., and R. Seidel. 2009. Torsional stiffness of single superparamagnetic microspheres in an external magnetic field. Phys. Rev. Lett. 102:028302.
28. Efron, B., and R. Tibshirani. 1991. Statistical data analysis in the computer age. Science. 253:390-395.
29. Dumont, S., W. Cheng, C. Bustamante. 2006. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature. 439:105-108.
30. Bujalowski, W., and M. J. Jezewska. 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.
31. Bujalowski, W., and M. J. Jezewska. 2000. Kinetic mechanism of the single-stranded DNA recognition by Escherichia coli replicative helicase DnaB protein. Application of the matrix projection operator technique to analyze stopped-flow kinetics. J. Mol. Biol. 295:831-852.
32. Rouzina, I., and V. A. Bloomfield. 2001. Force-induced melting of the DNA double helix. 1. Thermodynamic analysis. Biophys. J. 80:882-893.
33. Cocco, S., J. Yan, J. F. Marko. 2004. Overstretching and force-driven strand separation of double-helix DNA. Phys. Rev. E. 70:011910.
34. Smith, S. B., Y. J. Cui, and C. Bustamante. 1996. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science. 271:795-799.
35. Cluzel, P., A. Lebrun, F. Caron. 1996. DNA: an extensible molecule. Science. 271:792-794.
36. van Mameren, J., P. Gross, E. J. Peterman. 2009. Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc. Natl. Acad. Sci. USA. 106:18231-18236.
37. Bailey, S., W. K. Eliason, and T. A. Steitz. 2007. Structure ofhexameric DnaB helicase and its complex with a domain of DnaG primase. Science. 318:459-463.
38. Bustamante, C., Y. R. Chemla, D. Izhaky. 2004. Mechanical processes in biochemistry. Annu. Rev. Biochem. 73:705-748.
39. Wang, M. D., M. J. Schnitzer, S. M. Block. 1998. Force and velocity measured for single molecules of RNA polymerase. Science. 282:902-907.
40. Galletto, R., M. J. Jezewska, and W. Bujalowski. 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.
41. Rothenberg, E., M. A. Trakselis, T. Ha. 2007. MCM forked substrate specificity involves dynamic interaction with the 5'-tail. J. Biol. Chem. 282:34229-34234.
42. Sawaya, M. R., S. Y. Guo, T. Ellenberger. 1999. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell. 99:167-177.
43. Stano, N. M., Y. J. Jeong, S. S. Patel. 2005. DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase. Nature. 435:370-373.
44. Egelman, E. H., X. Yu, S. S. Patel. 1995. Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl. Acad. Sci. USA. 92:3869-3873.
45. Lo, Y. H., K. L. Tsai, C. D. Hsiao. 2009. The crystal structure of a replicative hexameric helicase DnaC and its complex with single-stranded DNA. Nucleic Acids Res. 37:804-814.