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

Journal of Molecular Biology

Volumn 343, Issue 1, 2004, Pages 83-99

  Galletto, Roberto ^a   Jezewska, Maria J ^a   Bujalowski, Wlodzimierz ^a  

^a The Sealy Ctr for Struct Biology   (United States)

Author keywords

E. coli DnaB helicase; helicase mechanism; processivity; rapid quench flow; single turnover kinetics

Indexed keywords

DNA B; DOUBLE STRANDED DNA; HELICASE;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; DNA STRAND; DNA SUPERCOILING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONPHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN METABOLISM; RNA REPLICATION; TEMPERATURE DEPENDENCE;

ESCHERICHIA COLI;

EID: 4644261530     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.055     Document Type: Article

References (46)

1. J.H. LeBowitz, and R. McMacken The Escherichia coli dnaB replication protein is a DNA helicase J. Biol. Chem. 261 1986 4738 4748
2. T. Baker, B.E. Funnel, and A. Kornberg Helicase action of dnaB protein during replication from Escherichia coli chromosomal origin in vitro J. Biol. Chem. 262 1987 6877 6885
3. A. Kornberg, and T.A. Baker DNA Replication 1992 Freeman, San Francisco
4. J. Marszalek, and J.M. Kaguni DnaA protein directs the binding of the DnaB protein in initiation of DNA replication J. Biol. Chem. 276 2001 44919 44925
5. S. Kim, G. Dallman, C.S. McHenry, and K.J. Marians Coupling of a replicative polymerase and helicase: a τ-DnaB interactions mediates rapid replication fork movement Cell 84 1996 643 650
6. W. Bujalowski, M.M. Klonowska, and M.J. Jezewska Oligomeric structure of Escherichia coli primary replicative helicase DnaB protein J. Biol. Chem. 269 1994 31350 31358
7. M.J. Jezewska, and W. Bujalowski Global conformational transitions in E. coli primary replicative DnaB Protein induced by ATP, ADP and single-stranded DNA binding J. Biol. Chem. 271 1996 4261 4265
8. E.H. Egelman, X. Yu, R. Wild, M.M. Hingorani, and S.S. Patel 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 1995 3869 3873
9. S. Yang, X. Yu, M.S. VanLoock, M.J. Jezewska, W. Bujalowski, and E.H. Egelman Flexibility of the rings: structural asymmetry in the DnaB hexameric helicase J. Mol. Biol. 321 2002 839 849
10. M.C. San Martin, N.P.J. Stamford, N. Dammerova, N.E. Dixon, and J.M. Carazo A structural model for the Escherichia coli DnaB helicase based on electron microscopy data J. Struct. Biol. 114 1995 167 176
11. M.J. Jezewska, U.-S. Kim, and W. Bujalowski Binding of Escherichia coli primary replicative helicase DnaB protein to single-stranded DNA. Long-range allosteric conformational changes within the protein hexamer Biochemistry 35 1996 2129 2145
12. W. Bujalowski, and M.J. Jezewska 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 1995 8513 8519
13. M.J. Jezewska, and W. Bujalowski A general method of analysis of ligand binding to competing macromolecules using the spectroscopic signal originating from a reference macromolecule. Application to Escherichia coli replicative helicase DnaB protein-nucleic acid interactions Biochemistry 35 1996 2117 2128
14. M.J. Jezewska, S. Rajendran, and W. Bujalowski Strand specificity in the interactions of Escherichia coli primary replicative helicase DnaB protein with replication fork Biochemistry 36 1997 10320 10326
15. M.J. Jezewska, S. Rajendran, and W. Bujalowski Functional and structural heterogeneity of the DNA binding of the E. coli primary replicative helicase DnaB protein J. Biol. Chem. 273 1998 9058 9069
16. M.J. Jezewska, S. Rajendran, D. Bujalowska, and W. Bujalowski Does ssDNA pass through the inner channel of the protein hexamer in the complex with the E. coli DnaB helicase? Fluorescence energy transfer studies J. Biol. Chem. 273 1998 10515 10529
17. F. Dong, E.P. Gogol, and P.H. von Hippel The phage T4-coded DNA replication helicase (gp41) forms a hexamer upon activation by nucleoside triphosphate J. Biol. Chem. 270 1995 7462 7473
18. K.J. Hacker, and K.A. Johnson A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding Biochemistry 36 1997 14080 14087
19. E.H. Egelman, X. Yu, R. Wild, M.M. Hingorani, and S.S. Patel 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 1995 3869 3873
20. W. Bujalowski, and M.J. Jezewska 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 2000 831 852
21. T.M. Lohman, and K.P. Bjornson Mechanisms of helicase-catalyzed DNA unwinding Annu. Rev. Biochem. 65 1996 169 214
22. P.H. von Hippel, and E. Delagoutte Helicase mechanisms and the coupling of helicases within macromolecular machines. Part I: Structures and properties of isolated helicases Quart. Rev. Biophys. 35 2002 431 478
23. P.H. von Hippel, and E. Delagoutte Helicase mechanisms and the coupling of helicases within macromolecular machines. Part II: Integration of helicases into cellular processes Quart. Rev. Biophys. 36 2003 1 69
24. J.A. Ali, and T.M. Lohman Kinetic measurement of the step size of DNA unwinding by Escherichia coli UvrD helicase Science 275 1997 377 3380
25. A.L. Lucius, A. Vindigni, R. Gregorian, J.A. Ali, A.F. Taylor, G.R. Smith, and T.M. Lohman DNA unwinding step-size of the E. coli recBCD helicase determined from single-turnover chemical quenched-flow kinetics J. Mol. Biol. 324 2002 409 428
26. L.J. Roman, A.K. Eggleston, and S.C. Kowalczykowski Processivity of the DNA helicase activity of the Escherichia coli RecBCD enzyme J. Biol. Chem. 267 1992 4207 4214
27. B. Nanduri, A.K. Byrd, R.L. Eoff, A.J. Tackett, and K.D. Raney Pre-steady state DNA unwinding by bacteriophage T4 Dda helicase reveals a monomeric molecular motor Proc. Natl Acad. Sci. USA 99 2002 14722 14727
28. E. Jankowsky, C.H. Gross, S. Shuman, and A.M. Pyle The DexH protein NPH-II is a processive and directional motor for unwinding RNA Nature 403 2002 447 451
29. M.C. Young, S.B. Kuhl, and P.H. von Hippel Kinetic theory of ATP-driven translocases on one-dimensional polymer lattices J. Mol. Biol. 235 1994 1436 1446
30. K.A. Johnson Rapid quench kinetic analysis of polymerases adenosinetriphosphatases, and enzyme intermediates Methods Enzymol. 249 1995 38 61
31. Asp catalyzed by the RNA component of Bacillus subtilis ribonuclease P Biochemistry 33 1994 10294 10304
32. A.L. Lucius, N.K. Maluf, C.J. Fischer, and T.M. Lohman 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
33. M.J. Jezewska, S. Rajendran, and W. Bujalowski Complex of Escherichia coli primary replicative helicase DnaB protein with a replication fork. Recognition and structure Biochemistry 37 1998 3116 3136
34. S. Rajendran, M.J. Jezewska, and W. Bujalowski Multiple-step kinetic mechanism of DNA-independent ATP binding and hydrolysis by Escherichia coli replicative helicase DnaB protein: quantitative analysis using the rapid quench-flow method J. Mol. Biol. 303 2000 773 795
35. W. Bujalowski, and M.J. Jezewska Kinetic mechanism of nucleotide cofactor binding to Escherichia coli replicative helicase DnaB protein. Stopped-flow kinetic studies using fluorescent, ribose-, and base-modified nucleotide analog Biochemistry 39 2000 2106 2122
36. R.S. Berry, S.A. Rice, and J. Ross Physical Chemistry 2000 Wiley & Sons New York 876 958
37. N. Nakayama, N. Arai, Y. Kaziro, and K. Arai Structural and functional studies of the dnaB protein using limited proteolysis J. Biol. Chem. 259 1984 88 96
38. D-E. Kim, M. Narayan, and S.S. Patel DNA T7 helicase: a molecular motor that processively translocates along single-stranded DNA J. Mol. Biol. 321 2002 807 819
39. T.L. Hill, and T. Tsuchiya Theoretical aspects of translocation on DNA: adenosine triphosphatases and treadmilling binding proteins Proc. Natl Acad. Sci. USA 78 1981 4796 48000
40. D. Porschke, and M. Eigen Cooperative non-enzymatic base recognition. III. Kinetics of the helix-coil transition of the oligoribouridilic- oligoriboadenylic acid system and of oligoriboadenylic acid alone at acidic pH J. Mol. Biol. 62 1971 361 381
41. M.E. Craig, D.M. Crothers, and P. Doty Relaxation kinetics of dimer formation by self complementary oligonucleotides J. Mol. Biol. 62 1971 383 401
42. W. Bujalowski, and M.M. Klonowska Negative cooperativity in the binding of nucleotides to Escherichia coli replicative helicase dnaB protein. Interactions with fluorescent nucleotide analogs Biochemistry 32 1993 5888 5900
43. Y-J. Jeong, M. Levin, and S.S. Patel The DNA-unwinding mechanism of the ring helicase of bacteriophage T7 Proc. Natl Acad. Sci. USA 101 2004 7264 7269
44. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edit., vol. 1, p. 6.39, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. W. Bujalowski, and M.M. Klonowska Close proximity of tryptophan residues and ATP-binding site in Escherichia coli primary replicative helicase DnaB protein. Molecular topography of the enzyme J. Biol. Chem. 269 1994 31359 31371
46. R. Galletto, M.J. Jezewska, and W. Bujalowski 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 2004 101 114