Clamp-loader-helicase interaction in Bacillus. Leucine 381 is critical for pentamerization and helicase binding of the Bacillus τ protein

Biochemistry

Volumn 42, Issue 37, 2003, Pages 10955-10964

  Haroniti, A ^a   Till, R ^a   Smith, M C M ^a   Soultanas, P ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; DNA; FILTRATION; GENES; MUTAGENESIS; OLIGOMERS; PROTEINS;

PENTAMERIZATION;

BACTERIA;

BACTERIAL PROTEIN; HELICASE; LEUCINE; OLIGOMER;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; CIRCULAR DICHROISM; COMPLEX FORMATION; CROSS LINKING; ENZYME BINDING; GEL FILTRATION; HEAT SENSITIVITY; ISOMERISM; MOLECULAR MODEL; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; AMINO ACIDS; BACILLUS; BACILLUS STEAROTHERMOPHILUS; BACTERIAL PROTEINS; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; CLONING, MOLECULAR; CROSS-LINKING REAGENTS; DIMERIZATION; DNA HELICASES; DNA POLYMERASE III; GLUTARAL; LEUCINE; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PLASMIDS; PROTEIN BINDING; PROTEIN CONFORMATION; TAU PROTEINS; TEMPERATURE; TIME FACTORS; ULTRACENTRIFUGATION;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 0141653974     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034955g     Document Type: Article

References (38)

1. Kornberg, A., and Baker, T. A. (1991) DNA replication, 2nd ed., W. H. Freeman, New York.
2. Kelman, Z., and O'Donnell, M. (1995) DNA polymerase III holoenzyme: Structure and function of a chromosomal replicating machine, Annu. Rev. Biochem. 64, 171-200.
3. Stillman, B. (1994) Smart machines at the DNA replication fork, Cell 78, 725-728.
4. Waga, S., and Stillman, B. (1998) The DNA replication fork in eukaryotic cells, Annu. Rev. Biochem. 67, 721-751.
5. Young, M. C., Reddy, M. K., and von Hippel, P. H. (1992) Structure and function of the bacteriophage T4 DNA polymerase holoenzyme, Biochemistry 31, 8675-8690.
6. Blinkowa, A. L., and Walker, J. R. (1990) Programed ribosomal frameshifting generates the Escherichisa coli DNA polymerase III γ subunit from within the τ subunit reading frame, Nucleic Acids Res. 18, 1725-1729.
7. Tsuchihashi, Z. (1991) Translational frameshifting in the Escherichia coli dnaX gene in vitro, Nucleic Acids Res. 19, 2457-2462.
8. Ellison, V., and Stillman, B. (2001) Opening of the clamp: An intimate view of an ATP-driven biological machine, Cell 106, 655-660.
9. Kim, D. R., and McHenry, C. S. (1996) Biotin tagging deletion analysis of domain limits involved in protein-macromolecular interactions. Mapping the τ binding domain of the DNA polymerase III α subunit. J. Biol. Chem. 271, 20690-20698.
10. Kim, S., Dallmann, H. G., McHenry, C. S., and Marians, K. J. (1996) Coupling of a replicative polymerase and helicase: A τ-DnaB interaction mediates rapid replication fork movement, Cell 84, 643-650.
11. Glover, B. P., and McHenry, C. S. (1998) The χπ subunits of DNA polymerase III holoenzyme bind to single-stranded DNA-binding protein (SSB) and facilitate replication of an SSB-coated template, J. Biol. Chem. 273, 23476-23484.
12. McAlear, M. A., Tuffo, K. M., and Holm, C. (1996) The large subunit of replication factor C (Rfc1p/Cdc44p) is required for DNA replication and DNA repair in Saccharomyces cerevisiae, Genetics 142, 65-78.
13. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
14. Gao, D., and McHenry, C. S. (2001) τ binds and organizes Escherichia coli replication proteins through distinct domains. Partial proteolysis of terminally tagged τ to determine candidate domains and assign domain V as the α binding domain, J. Biol. Chem. 276, 4433-4440.
15. Gao, D., and McHenry, C. S. (2001) τ binds and organizes Escherichia coli replication proteins through distinct domains. Domain IV, located within the unique C terminus of τ, binds the replication fork helicase, J. Biol. Chem. 276, 4441-4446.
16. Jeruzalmi, D., O'Donnell, M., and Kuriyan, J. (2001) Crystal structure of the processivity clamp loader γ complex of Escherichia coli DNA polymerase III, Cell 106, 429-441.
17. Jeruzalmi, D., Yurieva, O., Zhao, Y., Young, M., Stewart, J., Hingorani, M., O'Donnell, M., and Kuriyan, J. (2001) Mechanism of processivity clamp opening by the δ subunit wrench of the clamp loader complex of Escherichia coli DNA polymerase III, Cell 106, 417-428.
18. Guenther, B. D., Onrust, R., Sali, A., O'Donnell, M., and Kuriyan, J. (1996) Crystal structure of the δ′ subunit of the clamp-loader complex of Escherichia coli DNA polymerase III, Cell 91, 335-345.
19. Kong, X. P., Onrust, R., O'Donnell, M., and Kuriyan, J. (1992) Three-dimensional structure of the β subunit of Escherichia coli DNA polymerase III holoenzyme: a sliding DNA clamp, Cell 69, 425-437.
20. Onrust, R., Finkelstein, J., Naktinis, V., Turner, J., Fang, L., and O'Donnell, M. (1995) Assembly of a chromosomal replication machine: two polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. I. Organization of the clamp loader, J. Biol. Chem. 270, 13348-13357.
21. Dallmann, H. G., and McHenry, C. S. (1995) DnaX complex of Escherichia coli DNA polymerase III holoenzyme. Physical characterization of the DnaX subunits and complexes, J. Biol. Chem. 270, 29563-29569.
22. 3δδ′, EMBO J. 19, 6536-6545.
23. Gao, D., and McHenry, C. S. (2001) τ binds and organizes Escherichia coli replication proteins through distinct domains. Domain III, shared by γ and τ, binds δδ′, J. Biol. Chem. 276, 4447-4453.
24. Glover, B. P., and McHenry, C. S. (2000) The DnaX-binding subunits δ′ and ψ are bound to γ and not τ in the DNA polymerase III holoenzyme, J. Biol. Chem. 275, 3017-3020.
25. Bird, L. E., Pan, H., Soultanas, P., and Wigley, D. B. (2000) Mapping protein-protein interactions within a stable complex of DNA primase and DnaB helicase from Bacillus stearothermophilus, Biochemistry 39, 171-182.
26. Baker, D. G. (1982) Cloning and amplified expression of the tyrosyl-tRNA synthetase genes of Bacillus stearothermophilus and Escherichia coli, Eur. J. Biochem. 125, 357-360.
27. Martinez-Jimenez, M. I., Mesa, P., and Alonso, J. C. (2002) Bacillus subtilis τ subunit of DNA polymerase III interacts with bacteriophage SPP1 replicative DNA helicase G40P, Nucleic Acids Res. 30, 5056-5064.
28. Bird, L. E., and Wigley, D. B. (1999) The Bacillus stearothermophilus replicative helicase: cloning overexpression and activity, Biochem. Biophys. Acta 1444, 424-428.
29. McPherson, M. J., Quirke, P., and Taylor, G. R. (1992) PCR, a practical approach, pp 207-209, IRL Press, Oxford.
30. Harding, S. E., Rowe, A. J., and Horton, J. C. (1992) Analytical ultracentrifugation in biochemistry and polymer science, Ch. 7, pp 909-126, The Royal Society of Chemistry, Letchworth, UK.
31. Bhavsar, A. P., Zhao, X., and Brown, E. D. (2001) Development and characterisation of a xylose-dependent system for expression of cloned genes in Bacillus subtilis: conditional complementation of a teichoic acid mutant, Appl. Environ. Microbiol. 67, 403-410.
32. Bhavsar, A. P., Beveridge, T. J., and Brown, E. D. (2001) Precise deletion of tagD and controlled depletion of its product glycerol 3-phosphate cytidylyltransferase leads to irregular morphology and lysis of Bacillus subtilis grown at physiological temperature, J. Bacteriol. 183, 6688-6693.
33. Link, A. J., Phillips, D., and Church, G. M. (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization, J. Bacteriol. 179, 6228-6237.
34. Harwood, C. R., and Cutting, S. M. (1990) Molecular Biological Methods for Bacillus, John Wiley and Sons, New York.
35. Dallmann, H. G., Kim, S., Pritchard, A. E., Marians, K. J., and McHenry, C. S. (2000) Characterization of the unique C terminus of the Escherichia coli τ protein: Monomeric C-τ binds α and DnaB and can partially replace τ in reconstituted replication forks, J. Biol. Chem. 275, 15512-15519.
36. Stukenberg, P. T., Turner, J., and O'Donnell, M. (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps, Cell 78, 877-887.
37. Lahue, R. S., Au, K. G., and Modrich, P. (1989) DNA mismatch correction in a defined system, Science 245, 160-164.
38. Haroniti, A., Anderson, C., Doddridge, Z., Gardiner, L., Roberts, C. J., Allen, S., and Soultanas, P. (2003) The clamp-loader-helicase interaction in Bacillus. Atomic force microscopy reveals the structural organisation of the DnaB-tau complex in Bacillus, Structure (submitted for publication).