Interactions of the Escherichia coli DnaB-DnaC protein complex with nucleotide cofactors. 1. Allosteric conformational transitions of the complex

Biochemistry

Volumn 48, Issue 29, 2009, Pages 6712-6729

  Roychowdhury, Anasuya ^a   Szymanski, Michal R ^a   Jezewska, Maria J ^a   Bujalowski, Wlodzimierz ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC TRANSITION; BINARY COMPLEXES; COFACTOR; COFACTOR BINDING; COFACTORS; COMPLEX ACTIVITY; CONFORMATIONAL STATE; CONFORMATIONAL TRANSITIONS; COOPERATIVITY; DNAB HELICASE; HELICASE; HEXAMER; NUCLEOTIDE ANALOGUES; NUCLEOTIDE BINDING; PHOSPHATE GROUP; PRODUCT RELEASE; PROTEIN COMPLEXES; PROTEIN COMPONENTS; PROTEIN-DNA INTERACTIONS; REPLICATION FACTORS; SINGLE-STRANDED DNA;

BINDING ENERGY; BINDING SITES; CONFORMATIONS; DNA; ESCHERICHIA COLI; GENES; NUCLEIC ACIDS; STOICHIOMETRY;

NUCLEOTIDES;

BACTERIAL ENZYME; DNAB HELICASE; DNAC HELICASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENZYME BINDING; ESCHERICHIA COLI; HYDROLYSIS; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY;

ALLOSTERIC REGULATION; DNAB HELICASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE; NUCLEOTIDES;

ESCHERICHIA COLI;

EID: 67651222270     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900050x     Document Type: Article

References (60)

1. Kornberg, A., and Baker, T. A. (1992) DNA Replication , Freeman, San Francisco.
2. Kim, S., Dallman, G., McHenry, C. S., and Marians, K. J. (1996) Coupling of a Replicative Polymerase and Helicase: A τ-DnaB Interactions Mediates Rapid Replication Fork Movement. Cell 84, 643-650.
3. Heller, R. C., and Marians, K. J. (2007) Non-Replicative Helicases at the Replication Fork. DNA Repair 6, 945-952.
4. Marszalek, J., and Kaguni, J. M. (2001) DnaA protein directs the binding of the DnaB protein in initiation of DNA replication. J. Biol. Chem. 276, 44919-44925.
5. Roman, L. J., Eggleston, A. K., and Kowalczykowski, S. C. (1992) Processivity of the DNA helicase activity of the Escherichia coli RecBCD enzyme. J. Biol. Chem. 267, 4207-4214.
6. North, S. H., and Nakai, H. (2005) Host Factors That Promote Transpososome Disassembly and the PriA-PriC Pathway For Restart Primosome Assembly. Mol. Microbiol. 56, 1601-1616.
7. Baker, T., Funnel, B. E., and Kornberg, A. (1987) Helicase Action of dnaB Protein during Replication from Escherichia coli Chromosomal Origin in Vitro. J. Biol. Chem. 262, 6877-6885.
8. Wahle, E., Lasken, R. S., and Kornberg, A. (1989) The dnaB-dnaC Replication Protein Complex of Escherichia coli. I. Formation and Properties. J. Biol. Chem. 264, 2463-2468.
9. Wahle, E., Lasken, R. S., and Kornberg, A. (1989) The dnaB-dnaC Replication Protein Complex of Escherichia coli II. Role of the Complex in Mobilizing dnaB Functions. J. Biol. Chem. 264, 2469-2475.
10. LeBowitz, J. H., and McMacken, R. (1986) The Escherichia coli dnaB Replication Protein Is a DNA Helicase. J. Biol. Chem. 261, 4738-4748.
11. Galletto, R., Jezewska, M. J., and Bujalowski, W. (2003) Interactions of the Escherichia coli DnaB Helicase Hexamer with the Replication Factor the DnaC Protein. Effect of Nucleotide Cofactors and the ssDNA on Protein-Protein Interactions and the Topology of the Complex. J. Mol. Biol. 329, 441-465.
12. Bujalowski, W., and Jezewska, M. J. (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.
13. Jezewska, M. J., Kim, U.-S., and Bujalowski, W. (1996) Binding of Escherichia coli Primary Replicative Helicase DnaB Protein to Single-Stranded DNA. Long-Range Allosteric Conformational Changes within the Protein Hexamer. Biochemistry 35, 2129-2145.
14. Jezewska, M. J., and Bujalowski, W. (1996) 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, 2117-2128.
15. Jezewska, M. J., Rajendran, S., and Bujalowski, W. (1997) Strand Specificity in the Interactions of Escherichia coli Primary Replicative Helicase DnaB Protein with Replication Fork. Biochemistry 36, 10320-10326.
16. Jezewska, M. J., Rajendran, S., and Bujalowski, W. (1998) Functional and Structural Heterogeneity of the DNA Binding of the E. coli Primary Replicative Helicase DnaB protein. J. Biol. Chem. 273, 9058-9069.
17. Jezewska, M. J., Rajendran, S., Bujalowska, D., and Bujalowski, W. (1998) 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, 10515-10529.
18. San Martin, C., Radermacher, M., Wolpensinger, B., Miles, C. S., Dixon, N. E., and Caraza, J. M. (2005) Three-Dimensional Reconstructions From Cryoelectron Microscopy Images an Intimate Complex Between Helicase DnaB and Its Loading Partner DnaC. Structure 6, 501-509.
19. Bujalowski, W., Klonowska, M. M., and Jezewska, M. J. (1994) Oligomeric Structure of Escherichia coli Primary Replicative Helicase DnaB Protein. J. Biol. Chem. 269, 31350-31358.
20. Jezewska, M. J., and Bujalowski, W. (1996) Global Conformational Transitions in E. coli Primary Replicative DnaB Protein Induced by ATP, ADP and Single-Stranded DNA Binding. J. Biol. Chem. 271, 4261-4265.
21. Arai, K., and Kornberg, A. (1981) Mechanism of dnaB protein action. Allosteric role of ATP in the alteration of DNA structure by dnaB protein in priming replication. J. Biol. Chem. 256, 5260-5266.
22. Bujalowski, W., and Jezewska, M. J. (2000) 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, 2106-2122.
23. Bujalowski, W., and Klonowska, M. M. (1993) Negative Cooperativity in the Binding of Nucleotides to Escherichia coli Replicative Helicase DnaB Protein. Interactions with Fluorescent Nucleotide Analogs. Biochemistry 32, 5888-5900.
24. Bujalowski, W., and Klonowska, M. M. (1994) 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, 31359-31371.
25. Jezewska, M. J., Kim, U.-S., and Bujalowski, W. (1996) Interactions of Escherichia coli Primary Replicative Helicase DnaB Protein with Nucleotide Cofactors. Biophys. J. 71, 2075-2086.
26. Galletto, R., Rajendran, S., and Bujalowski, W. (2000) Interactions of Nucleotide Cofactors with the Escherichia coli Replication Factor DnaC Protein. Biochemistry 39, 12959-12969.
27. Galletto, R., and Bujalowski, W. (2002) The E. coli Replication Factor DnaC Protein Exists in Two Conformations with Different Nucleotide Binding Capabilities. I. Determination of the Binding Mechanism Using ATP and ADP Fluorescent Analogues. Biochemistry 41, 8907-8920.
28. Galletto, R., and Bujalowski, W. (2002) Kinetics of the E. coli Replication Factor DnaC Protein-Nucleotide Interactions. II. Fluorescence Anisotropy and Transient, Dynamic Quenching Stopped-Flow Studies of the Reaction Intermediates. Biochemistry 41, 8921-8934.
29. Galletto, R., Jezewska, M. J., Maillard, R., and Bujalowski, W. (2005) The Nucleotide-Binding Site of the Escherichia coli DnaC Protein. Cell Biochem. Biophys. 43, 331-353.
30. Galletto, R., Maillard, R., Jezewska, M. J., and Bujalowski, W. (2004) Global Conformation of the Escherichia coli Replication Factor DnaC Protein in Absence and Presence of Nucleotide Cofactors. Biochemistry 43, 10988-11001.
31. Marcinowicz, A., Jezewska, M. J., and Bujalowski, W. (2008) Multiple Global Conformational States of the Hexameric RepA Helicase of Plasmid RSF1010 With Different ssDNA-Binding Capabilities Are Induced By Different Numbers of Bound Nucleotides. Analytical Ultracentrifugation and Dynamic Light Scattering Studies. J. Mol. Biol. 375, 386-408.
32. Rajendran, S., Jezewska, M. J., and Bujalowski, W. (2000) 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, 773-795.
33. Kobori, J. A., and Kornberg, A. (1982) The Escherichia coli dnaC Gene Product. II. Purification, Physical Properties, and Role in Replication. J. Biol. Chem. 257, 13763-13769.
34. Kobori, J. A., and Kornberg, A. (1982) The Escherichia coli dnaC Gene Product, III. Properties of the dnaB-dnaC Protein Complex. J. Biol. Chem. 257, 13770-13775.
35. Galletto, R., Jezewska, M. J., and Bujalowski, W. (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.
36. Galletto, R., Jezewska, M. J., and Bujalowski, W. (2004) Unzipping Mechanism of the Double-Stranded DNA Unwinding by a Hexameric Helicase. The Effect of the 30 Arm and the Stability of the dsDNA on the Unwinding Activity of the Escherichia coli DnaB Helicase. J. Mol. Biol. 343, 101-114.
37. Dong, F., Gogol, E. P., and von Hippel, P. H. (1995) The Phage T4-coded DNA Replication Helicase (gp41) Forms a Hexamer upon Activation by Nucleoside Triphosphate. J. Biol. Chem. 270, 7462-7473.
38. Hacker, K. J., and Johnson, K. A. (1997) A Hexameric Helicase Encircles One DNA Strand and Excludes the Other during DNA Unwinding. Biochemistry 36, 14080-14087.
39. Ali, J. A., and Lohman, T. M. (1997) Kinetic Measurement of the Step Size of DNA Unwinding by Escherichia coli UvrD Helicase. Science 275, 377-3380.
40. Lucius, A. L., Vindigni, A., Gregorian, R., Ali, J. A., Taylor, A. F., Smith, G. R., and Lohman, T. M. (2002) DNA Unwinding Step-Size of the E. coli RecBCD Helicase Determined from Single-Turnover Chemical Quenched-Flow Kinetics. J. Mol. Biol. 324, 409-428.
41. Nanduri, B., Byrd, A. K., Eoff, R. L., Tackett, A. J., and Raney, K. D. (2002) Pre-steady state DNA unwinding by bacteriophage T4 Dda helicase reveals a monomeric molecular motor. Proc. Natl. Acad. Sci. U.S.A. 99, 14722-14727.
42. Jankowsky, E., Gross, C. H., Shuman, S., and Pyle, A. M. (2002) The DexH protein NPH-II is a processive and directional motor for unwinding RNA. Nature 403, 447-451.
43. Young, M. C., Kuhl, S. B., and von Hippel, P. H. (1994) Kinetic Theory of ATP-driven Translocases on One-dimensional Polymer Lattices. J. Mol. Biol. 235, 1436-1446.
44. Lohman, T. M., and Bjornson, K. P. (1996) Mechanisms of Helicase-Catalyzed DNA Unwinding. Annu. Rev. Biochem. 65, 169-214.
45. Huang, S.-G., Weisshart, K., and Fanning, E. (1998) Characterization of the Nucleotide Binding Properties of SV40 T Antigen Using Fluorescent 30(20)-O-(2,4,6-Trinitrophenyl)adenine Nucleotide Analogs. Biochemistry 37, 15336-15344.
46. Bujalowski, W., and Klonowska, M. M. (1994) Structural Characteristics of the Nucleotide Binding Site of E. coli Primary Replicative Helicase DnaB Protein. Studies with Ribose and Base-Modified Fluorescent Nucleotide Analogs. Biochemistry 33, 4682-4694.
47. Bujalowski, W., and Jezewska, M. J. (2000) Spectrophotometry & Spectrofluorimetry. A Practical Approach (Gore, M. G., Ed.) pp 141-165, Oxford University Press, New York.
48. Bujalowski, W. (2006) Thermodynamic and Kinetic Methods of Analyses of Protein-Nucleic Acid Interactions. From Simpler to More Complex Systems. Chem. Rev. 106, 556-606.
49. Lohman, T. M., and Bujalowski, W. (1991) Thermodynamic Methods for the Model-Independent Determination of Equilibrium Binding Isotherms for Protein-DNA Interactions, Using Spectroscopic Approaches to Monitor the Binding. Methods Enzymol. 208, 258-290.
50. Jezewska, M. J., Lucius, A. L., and Bujalowski, W. (2005) Binding of Six Nucleotide Cofactors to the Hexameric Helicase RepA Protein of Plasmid RSF1010. I. Direct Evidence of Cooperative Interactions Between the Nucleotide-Binding Sites of a Hexameric Helicase. Biochemistry 44, 3865-3876.
51. Jezewska, M. J., Lucius, A. L., and Bujalowski, W. (2005) Binding of Six Nucleotide Cofactors to the Hexameric Helicase RepA Protein of Plasmid RSF1010. II. Base Specificity, Nucleotide Structure, Magnesium, and Salt Effect on the Cooperative Binding of the Cofactors. Biochemistry 44, 3877-3890.
52. Lucius, A. L., Jezewska, M. J., and Bujalowski, W. (2006) The Escherichia coli PriA Helicase Has Two Nucleotide-Binding Sites Differing in Their Affinities for Nucleotide Cofactors. I. Intrinsic Affinities, Cooperativities, and Base Specificity of Nucleotide Cofactor Binding. Biochemistry 45, 7202-7216.
53. Jezewska, M. J., Bujalowski, P. J., and Bujalowski, W. (2007) Interactions of the DNA Polymerase X of African Swine Fever Virus With Double-Stranded DNA. Functional Structure of the Complex. J. Mol. Biol. 373, 75-95.
54. Davey, M. J., Fang, L., McInerney, P., Georgescu, R. E., and O'Donnell, M. (2002) The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J. 21, 3148-3159.
55. Galletto, R., Jezewska, M. J., and Bujalowski, W. (2005) Kinetics of Allosteric Conformational Transition of a Macromolecule Prior to Ligand Binding. Analysis of Stopped-Flow Kinetic Experiments. Cell Biochem. Biophys. 42, 121-144.
56. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the Nature of Allosteric Transition: A Plausible Model. J. Mol. Biol. 12, 918-923.
57. Kaplan, D. L., and O'Donnell, M. (2002) DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell 10, 647-657.
58. West, S. C. (1996) DNA helicases: New breeds of translocating motors and molecular pumps. Cell 86, 177-180.
59. Allen, G. C.Jr., and Kornberg, A. (1991) Fine Balance in the Regulation of DnaB Helicase by DnaC Protein in Replication in Escherichia coli. J. Biol. Chem. 266, 22096-22101.
60. Allen, G. C.Jr., Dixon, N. E., and Kornberg, A. (1993) Strand Switching of a Replicative DNA Helicase Promoted by the E. coli Primosome. Cell 74, 713-722.