T7 replisome directly overcomes DNA damage

Nature Communications

Volumn 6, Issue , 2015, Pages

  Sun, Bo ^a,b,c   Pandey, Manjula ^d   Inman, James T ^a,b   Yang, Yi ^a,b   Kashlev, Mikhail ^e   Patel, Smita S ^d   Wang, Michelle D ^a,b  

^a Cornell University   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c SHANGHAITECH UNIVERSITY   (China)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DOUBLE STRANDED DNA; EXONUCLEASE; GENOMIC DNA; HELICASE; PYRIMIDINE DIMER; SINGLE STRANDED DNA; DNA DIRECTED DNA POLYMERASE; DNA HELICASE; VIRUS DNA;

DNA; LESION; PROTEIN; VIRUS;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA ADDUCT; DNA BINDING; DNA DAMAGE; DNA DENATURATION; DNA REPLICATION; DNA SYNTHESIS; DNA TEMPLATE; ENTEROBACTERIA PHAGE T7; NONHUMAN; REPLISOME; CELL LINE; ESCHERICHIA COLI; GENETICS; METABOLISM;

BACTERIOPHAGE T7; CELL LINE; DNA DAMAGE; DNA HELICASES; DNA REPLICATION; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; PYRIMIDINE DIMERS;

EID: 84950268197     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10260     Document Type: Article

References (50)

1. Cox, M. M. et al. The importance of repairing stalled replication forks. Nature 404, 37-41 (2000).
2. Yeeles, J. T. P., Poli, J., Marians, K. J. & Pasero, P. Rescuing stalled or damaged replication forks. Cold Spring Harb. Perspect. Biol. 5, 1-15 (2013).
3. Kowalczykowski, S. C. Initiation of genetic recombination and recombinationdependent replication. Trends Biochem. Sci. 25, 156-165 (2000).
4. Nelson, S. W. & Benkovic, S. J. Response of the bacteriophage T4 replisome to noncoding lesions and regression of a stalled replication fork. J. Mol. Biol. 401, 743-756 (2010).
5. McInerney, P. & O'Donnell, M. Functional uncoupling of twin polymerases: mechanism of polymerase dissociation from a lagging-strand block. J. Biol. Chem. 279, 21543-21551 (2004).
6. McInerney, P. & O'Donnell, M. Replisome fate upon encountering a leading strand block and clearance from DNA by recombination proteins. J. Biol. Chem. 282, 25903-25916 (2007).
7. Higuchi, K. et al. Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells 8, 437-449 (2003).
8. Zhu, B., Lee, S. J. & Richardson, C. C. Bypass of a nick by the replisome of bacteriophage T7. J. Biol. Chem. 286, 28488-28497 (2011).
9. Manosas, M., Perumal, S. K., Croquette, V. & Benkovic, S. J. Direct observation of stalled fork restart via fork regression in the T4 replication system. Science 338, 1217-1220 (2012).
10. Courcelle, J., Donaldson, J. R., Chow, K. H. & Courcelle, C. T. DNA damageinduced replication fork regression and processing in Escherichia coli. Science 299, 1064-1067 (2003).
11. Yeeles, J. T. P. & Marians, K. J. The Escherichia coli replisome is inherently DNA damage tolerant. Science 334, 235-238 (2011).
12. Sale, J. E., Lehmann, A. R. & Woodgate, R. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol. 13, 141-152 (2012).
13. Kath, J. E. et al. Polymerase exchange on single DNA molecules reveals processivity clamp control of translesion synthesis. Proc. Natl Acad. Sci. USA 111, 7647-7652 (2014).
14. Rudolph, C. J., Upton, A. L. & Lloyd, R. G. Replication fork stalling and cell cycle arrest in UV-irradiated Escherichia coli. Genes Dev. 21, 668-681 (2007).
15. Hamdan, S. M. & Richardson, C. C. Motors, switches, and contacts in the replisome. Annu. Rev. Biochem. 78, 205-243 (2009).
16. Delagoutte, E. & von Hippel, P. H. Helicase mechanisms and the coupling of helicases within macromolecular machines - Part II: integration of helicases into cellular processes. Q. Rev. Biophys. 36, 1-69 (2003).
17. Brown, W. C. & Romano, L. J. Benzo[a]pyrene-DNA adducts inhibit translocation by the gene 4 protein of bacteriophage T7. J. Biol. Chem. 264, 6748-6754 (1989).
18. Johnson, D. S., Bai, L., Smith, B. Y., Patel, S. S. & Wang, M. D. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129, 1299-1309 (2007).
19. Sun, B. et al. ATP-induced helicase slippage reveals highly coordinated subunits. Nature 478, 132-135 (2011).
20. 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).
21. Stano, N. M. et al. DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase. Nature 435, 370-373 (2005).
22. Manosas, M. et al. Mechanism of strand displacement synthesis by DNA replicative polymerases. Nucleic Acids Res. 40, 6174-6186 (2012).
23. McCulloch, S. D. & Kunkel, T. A. Multiple solutions to inefficient lesion bypass by T7 DNA polyrnerase. DNA Repair (Amst). 5, 1373-1383 (2006).
24. Smith, C. A., Baeten, J. & Taylor, J. S. The ability of a variety of polymerases to synthesize past site-specific cis-syn, trans-syn-II, (6-4), and Dewar photoproducts of thymidylyl-(3 '-4 5 ')-thymidine. J. Biol. Chem. 273, 21933-21940 (1998).
25. Pandey, M. & Patel, S. S. Helicase and polymerase move together close to the fork junction and copy DNA in one-nucleotide steps. Cell Rep. 6, 1129-1138 (2014).
26. Kulczyk, A. W. et al. An interaction between DNA polymerase and helicase is essential for the high processivity of the bacteriophage T7 replisome. J. Biol. Chem. 287, 39050-39060 (2012).
27. Hamdan, S. M. et al. Dynamic DNA helicase-DNA polymerase interactions assure processive replication fork movement. Mol. Cell 27, 539-549 (2007).
28. Zhang, H. et al. Helicase-DNA polymerase interaction is critical to initiate leading-strand DNA synthesis. Proc. Natl Acad. Sci. USA 108, 9372-9377 (2011).
29. 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).
30. Doublie, S., Tabor, S., Long, A. M., Richardson, C. C. & Ellenberger, T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 angstrom resolution. Nature 391, 251-258 (1998).
31. Li, Y. et al. Nucleotide insertion opposite a cis-syn thymine dimer by a replicative DNA polymerase from bacteriophage T7. Nat. Struct. Mol. Biol. 11, 784-790 (2004).
32. Romano, L. J., Tamanoi, F. & Richardson, C. C. Initiation of DNA replication at the primary origin of bacteriophage T7 by purified proteins: requirement for T7 RNA polymerase. Proc. Natl Acad. Sci. USA 78, 4107-4111 (1981).
33. Sun, L. P., Wang, M., Kool, E. T. & Taylor, J. S. Pyrene nucleotide as a mechanistic probe: evidence for a transient abasic site-like intermediate in the bypass of dipyrimidine photoproducts by T7 DNA polymerase. Biochemistry 39, 14603-14610 (2000).
34. Taylor, J. S. New structural and mechanistic insight into the A-rule and the instructional and non-instructional behavior of DNA photoproducts and other lesions. Mutat. Res. 510, 55-70 (2002).
35. Nandakumar, D., Pandey, M. & Patel, S. S. Cooperative base pair melting by helicase and polymerase positioned one nucleotide from each other. Elife 4, 1-23 (2015).
36. Lieberman, K. R., Dahl, J. M. & Wang, H. Kinetic mechanism at the branchpoint between the DNA synthesis and editing pathways in individual DNA polymerase complexes. J. Am. Chem. Soc. 136, 7117-7131 (2014).
37. Patel, S. S., Rosenberg, A. H., Studier, F. W. & Johnson, K. A. Large scale purification and biochemical characterization of T7 primase/helicase proteins. Evidence for homodimer and heterodimer formation. J. Biol. Chem. 267, 15013-15021 (1992).
38. Patel, S. S., Wong, I. & Johnson, K. A. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30, 511-525 (1991).
39. Inman, J. T. et al. DNA Y structure: a versatile, multidimensional single molecule assay. Nano Lett. 14, 6475-6480 (2014).
40. Schafer, D. A., Gelles, J., Sheetz, M. P. & Landick, R. Transcription by single molecules of rna-polymerase observed by light-microscopy. Nature 352, 444-448 (1991).
41. Jin, J. et al. Synergistic action of RNA polymerases in overcoming the nucleosomal barrier. Nat. Struct. Mol. Biol. 17, 745-752 (2010).
42. Peterman, E. J., Gittes, F. & Schmidt, C. F. Laser-induced heating in optical traps. Biophys. J. 84, 1308-1316 (2003).
43. Hingorani, M. M. & Patel, S. S. Interactions of bacteriophage T7 DNA primase/ helicase protein with single-stranded and double-stranded DNAs. Biochemistry 32, 12478-12487 (1993).
44. Egelman, E. H., Yu, X., Wild, R., Hingorani, M. M. & Patel, S. S. 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 (1995).
45. Patel, S. S. & Hingorani, M. M. Oligomeric structure of bacteriophage T7 DNA primase/helicase proteins. J. Biol. Chem. 268, 10668-10675 (1993).
46. Wang, M. D., Yin, H., Landick, R., Gelles, J. & Block, S. M. Stretching DNA with optical tweezers. Biophys. J. 72, 1335-1346 (1997).
47. Smith, S. B., Cui, Y. & Bustamante, C. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271, 795-799 (1996).
48. Hall, M. A. et al. High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat. Struct. Mol. Biol. 16, 124-129 (2009).
49. Shundrovsky, A., Smith, C. L., Lis, J. T., Peterson, C. L. & Wang, M. D. Probing SWI/SNF remodeling of the nucleosome by unzipping single DNA molecules. Nat. Struct. Mol. Biol. 13, 549-554 (2006).
50. Pandey, M., Levin, M. K. & Patel, S. S. Experimental and computational analysis of DNA unwinding and polymerization kinetics. Methods. Mol. Biol. 587, 57-83 (2010).