Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis

Nature

Volumn 457, Issue 7227, 2009, Pages 336-339

  Hamdan, Samir M ^a   Loparo, Joseph J ^a   Takahashi, Masateru ^a   Richardson, Charles C ^a   Van Oijen, Antoine M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; OKAZAKI FRAGMENT;

DNA; ENZYME ACTIVITY; PROTEIN;

ARTICLE; BACTERIOPHAGE T7; DNA REPLICATION; DNA STRAND; DNA STRUCTURE; DNA SYNTHESIS INHIBITION; DNA TEMPLATE; MOLECULAR DYNAMICS; PRIORITY JOURNAL;

BACTERIOPHAGE LAMBDA; BACTERIOPHAGE T7; DNA REPLICATION; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; MICROSCOPY, FLUORESCENCE; MULTIENZYME COMPLEXES; TIME FACTORS;

PROKARYOTA;

EID: 58249114971     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature07512     Document Type: Article

References (27)

1. Benkovic, S. J., Valentine, A. M. & Salinas, F. Replisome-mediated DNA replication. Annu. Rev. Biochem. 70, 181-208 (2001).
2. Johnson, A. & O'Donnell, M. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74, 283-315 (2005).
3. Alberts, B. M. et al. Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb. Symp. Quant. Biol. 47, 655-668 (1983).
4. Chastain, P. D., Makhov, A. M., Nossal, N. G. & Griffith, J. D. Analysis of the Okazaki fragment distributions along single long DNAs replicated by the bacteriophage T4 proteins. Mol. Cell 6, 803-814 (2000).
5. Park, K., Debyser, Z., Tabor, S., Richardson, C. C. & Griffith, J. D. Formation of a DNA loop at the replication fork generated by bacteriophage T7 replication proteins. J. Biol. Chem. 273, 5260-5270 (1998).
6. Carver, T. E., Sexton, D. J. & Benkovic, S. J. Dissociation of bacteriophage T4 DNA polymerase and its processivity clamp after completion of Okazaki fragment synthesis. Biochemistry 36, 14409-14417 (1997).
7. López de Saro, F. J., Georgescu, R. E. & O'Donnell, M. A peptide switch regulates DNA polymerase processivity. Proc. Natl Acad. Sci. USA 100, 14689-14694 (2003).
8. Hacker, K. J. & Alberts, B. M. The rapid dissociation of the T4 DNA-polymerase holoenzyme when stopped by a DNA hairpin helix: a model for polymerase release following the termination of each Okazaki fragment. J. Biol. Chem. 269, 24221-24228 (1994).
9. Li, X. & Marians, K. J. Two distinct triggers for cycling of the lagging strand polymerase at the replication fork. J. Biol. Chem. 275, 34757-34765 (2000).
10. Yang, J., Nelson, S. W. & Benkovic, S. J. The control mechanism for lagging strand polymerase recycling during bacteriophage T4 DNA replication. Mol. Cell 21, 153-164 (2006).
11. Nossal, N. G., Makhov, A. M., Chastain, P. D., Jones, C. E. & Griffith, J. D. Architecture of the bacteriophage T4 replication complex revealed with nanoscale biopointers. J. Biol. Chem. 282, 1098-1108 (2007).
12. Wu, C. A., Zechner, E. L., Reems, J. A., McHenry, C. S. & Marians, K. J. Coordinated leading-strand and lagging-strand synthesis at the Escherichia coli DNA-replication fork: primase action regulates the cycle of Okazaki fragment synthesis. J. Biol. Chem. 267, 4074-4083 (1992).
13. Lee, J., Chastain, P. D., Griffith, J. D. & Richardson, C. C. Lagging strand synthesis in coordinated DNA synthesis by bacteriophage T7 replication proteins. J. Mol. Biol. 316, 19-34 (2002).
14. Tougu, K. & Marians, K. J. The interaction between helicase and primase sets the replication fork clock. J. Biol. Chem. 271, 21398-21405 (1996).
15. Richardson, C. C. Bacteriophage T7: minimal requirements for the replication of a duplex DNA molecule. Cell 33, 315-317 (1983).
16. Lee, J. B. et al. DNA primase acts as a molecular brake in DNA replication. Nature 439, 621-624 (2006).
17. Tanner, N. A. et al. Single-molecule studies of fork dynamics in Escherichia coli DNA replication. Nature Struct. Mol. Biol. 15, 170-176 (2008).
18. Hamdan, S. M. et al. Dynamic DNA helicase-DNA polymerase interactions assure processive replication fork movement. Mol. Cell 27, 539-549 (2007).
19. van Oijen, A. M. et al. Single-molecule kinetics of lambda exonuclease reveal base dependence and dynamic disorder. Science 301, 1235-1238 (2003).
20. Lee, J., Chastain, P. D., Kusakabe, T., Griffith, J. D. & Richardson, C. C. Coordinated leading and lagging strand DNA synthesis on a minicircular template. Mol. Cell 1, 1001-1010 (1998).
21. Frick, D. N. & Richardson, C. C. DNA primases. Annu. Rev. Biochem. 70, 39-80 (2001).
22. Qimron, U., Lee, S. J., Hamdan, S. M. & Richardson, C. C. Primer initiation and extension by T7 DNA primase. EMBO J. 25, 2199-2208 (2006).
23. Kusakabe, T. & Richardson, C. C. Gene 4 DNA primase of bacteriophage T7 mediates the annealing and extension of ribo-oligonucleotides at primase recognition sites. J. Biol. Chem. 272, 12446-12453 (1997).
24. Frick, D. N., Kumar, S. & Richardson, C. C. Interaction of ribonucleoside triphosphates with the gene 4 primase of bacteriophage T7. J. Biol. Chem. 274, 35899-35907 (1999).
25. Notarnicola, S. M., Mulcahy, H. L., Lee, J. & Richardson, C. C. The acidic carboxyl terminus of the bacteriophage T7 gene 4 helicase/primase interacts with T7 DNA polymerase. J. Biol. Chem. 272, 18425-18433 (1997).
26. Tabor, S., Huber, H. E. & Richardson, C. C. Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 262, 16212-16223 (1987).
27. Hyland, E. M., Rezende, L. F. & Richardson, C. C. The DNA binding domain of the gene 2.5 single-stranded DNA-binding protein of bacteriophage T7. J. Biol. Chem. 278, 7247-7256 (2003).