Preferential D-loop extension by a translesion DNA polymerase underlies error-prone recombination

Nature Structural and Molecular Biology

Volumn 20, Issue 6, 2013, Pages 748-755

  Pomerantz, Richard T ^a,c   Kurth, Isabel ^a,d   Goodman, Myron F ^b   O'Donnell, Mike E ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d RGenix   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; DNA POLYMERASE IV; EXONUCLEASE; RECA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; D LOOP EXTENSION; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; ENZYME ACTIVITY; IN VITRO STUDY; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURE ACTIVITY RELATION;

DNA POLYMERASE II; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; RECOMBINATION, GENETIC;

ESCHERICHIA COLI;

EID: 84878932551     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2573     Document Type: Article

References (51)

1. Cox, M.M. Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu. Rev. Genet. 35, 53-82 (2001). (Pubitemid 34032970)
2. Cox, M.M. et al. The importance of repairing stalled replication forks. Nature 404, 37-41 (2000). (Pubitemid 30143124)
3. Mazon, G., Mimitou, E.P. & Symington, L.S. SnapShot: homologous recombination in DNA double-strand break repair. Cell 142, 646, 646.e1 (2010).
4. Li, X. & Heyer, W.D. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18, 99-113 (2008).
5. Heller, R.C. & Marians, K.J. Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol. Cell Biol. 7, 932-943 (2006). (Pubitemid 44871419)
6. Zahradka, K. et al. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443, 569-573 (2006). (Pubitemid 44527291)
7. Motamedi, M.R., Szigety, S.K. & Rosenberg, S.M. Double-strand-break repair recombination in Escherichia coli: physical evidence for a DNA replication mechanism in vivo. Genes Dev. 13, 2889-2903 (1999).
8. Lydeard, J.R. et al. Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev. 24, 1133-1144 (2010).
9. Kawamoto, T. et al. Dual roles for DNA polymerase ? in homologous DNA recombination and translesion DNA synthesis. Mol. Cell 20, 793-799 (2005). (Pubitemid 41740700)
10. Kane, D.P., Shusterman, M., Rong, Y. & McVey, M. Competition between replicative and translesion polymerases during homologous recombination repair in Drosophila. PLoS Genet. 8, e1002659 (2012).
11. Li, X., Stith, C.M., Burgers, P.M. & Heyer, W.D. PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase delta. Mol. Cell 36, 704-713 (2009).
12. Hashimoto, Y., Puddu, F. & Costanzo, V. RAD51-and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat. Struct. Mol. Biol. 19, 17-24 (2012).
13. Moldovan, G.L. et al. DNA polymerase POLN participates in cross-link repair and homologous recombination. Mol. Cell Biol. 30, 1088-1096 (2010).
14. McIlwraith, M.J. et al. Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol. Cell 20, 783-792 (2005).
15. Kohzaki, M. et al. DNA polymerases ? and ? are required for efficient immunoglobulin V gene diversification in chicken. J. Cell Biol. 189, 1117-1127 (2010).
16. Rosenberg, S.M. Evolving responsively: adaptive mutation. Nat. Rev. Genet. 2, 504-515 (2001). (Pubitemid 33674024)
17. Ponder, R.G., Fonville, N.C. & Rosenberg, S.M. A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol. Cell 19, 791-804 (2005). (Pubitemid 41316673)
18. McKenzie, G.J., Lee, P.L., Lombardo, M.J., Hastings, P.J. & Rosenberg, S.M. SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell 7, 571-579 (2001). (Pubitemid 32706349)
19. Foster, P.L. Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42, 373-397 (2007). (Pubitemid 47537271)
20. Hastings, P.J. et al. Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS ONE 5, e10862 (2010).
21. Shee, C., Gibson, J.L. & Rosenberg, S.M. Two mechanisms produce mutation hotspots at DNA breaks in Escherichia coli. Cell Rep. 2, 714-721 (2012).
22. Harris, R.S., Bull, H.J. & Rosenberg, S.M. A direct role for DNA polymerase III in adaptive reversion of a frameshift mutation in Escherichia coli. Mutat. Res. 375, 19-24 (1997). (Pubitemid 27152198)
23. Schlacher, K., Cox, M.M., Woodgate, R. & Goodman, M.F. RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature 442, 883-887 (2006). (Pubitemid 44285938)
24. Petrosino, J.F., Galhardo, R.S., Morales, L.D. & Rosenberg, S.M. Stress-induced ?-lactam antibiotic resistance mutation and sequences of stationary-phase mutations in the Escherichia coli chromosome. J. Bacteriol. 191, 5881-5889 (2009).
25. Kim, S.R., Matsui, K., Yamada, M., Gruz, P. & Nohmi, T. Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol. Genet. Genomics 266, 207-215 (2001). (Pubitemid 32938414)
26. Tippin, B., Pham, P. & Goodman, M.F. Error-prone replication for better or worse. Trends Microbiol. 12, 288-295 (2004). (Pubitemid 38686377)
27. Akerlund, T., Nordstrom, K. & Bernander, R. Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J. Bacteriol. 177, 6791-6797 (1995).
28. Withers, H.L. & Bernander, R. Characterization of dnaC2 and dnaC28 mutants by flow cytometry. J. Bacteriol. 180, 1624-1631 (1998). (Pubitemid 28173038)
29. Godoy, V.G. et al. UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol. Cell 28, 1058-1070 (2007). (Pubitemid 350297024)
30. Kobayashi, S., Valentine, M.R., Pham, P., O'Donnell, M. & Goodman, M.F. Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment. J. Biol. Chem. 277, 34198-34207 (2002).
31. Galhardo, R.S. et al. DinB upregulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 182, 55-68 (2009).
32. Xu, L. & Marians, K.J. PriA mediates DNA replication pathway choice at recombination intermediates. Mol. Cell 11, 817-826 (2003). (Pubitemid 36388763)
33. Shlomai, J. & Kornberg, A. A prepriming DNA replication enzyme of Escherichia coli. I. Purification of protein n?: a sequence-specific, DNA-dependent ATPase. J. Biol. Chem. 255, 6789-6793 (1980).
34. Frisch, R.L. et al. Separate DNA Pol II-and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J. Bacteriol. 192, 4694-4700 (2010).
35. Foster, P.L., Gudmundsson, G., Trimarchi, J.M., Cai, H. & Goodman, M.F. Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli. Proc. Natl. Acad. Sci. USA 92, 7951-7955 (1995).
36. Bonner, C.A. et al. Purification and characterization of an inducible Escherichia coli DNA polymerase capable of insertion and bypass at abasic lesions in DNA. J. Biol. Chem. 263, 18946-18952 (1988). (Pubitemid 19016355)
37. Cai, H., Yu, H., McEntee, K., Kunkel, T.A. & Goodman, M.F. Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli. J. Biol. Chem. 270, 15327-15335 (1995).
38. Goodman, M.F. et al. DNA Replication and Mutagenesis (American Society for Microbiology, Washington, D.C., 1988).
39. Buckstein, M.H., He, J. & Rubin, H. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J. Bacteriol. 190, 718-726 (2008). (Pubitemid 351360088)
40. Ibarra, B. et al. Proofreading dynamics of a processive DNA polymerase. EMBO J. 28, 2794-2802 (2009).
41. Downey, C.D. & McHenry, C.S. Chaperoning of a replicative polymerase onto a newly assembled DNA-bound sliding clamp by the clamp loader. Mol. Cell 37, 481-491 (2010).
42. Baker, T. & Kornberg, A. DNA Replication, 2nd edn (University Science Books, 1992).
43. Lovett, S.T. Replication arrest-stimulated recombination: dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB. DNA Repair (Amst.) 5, 1421-1427 (2006). (Pubitemid 44739448)
44. Register, J.C. III & Griffith, J. Direct visualization of RecA protein binding to and unwinding duplex DNA following the D-loop cycle. J. Biol. Chem. 263, 11029-11032 (1988).
45. Indiani, C., McInerney, P., Georgescu, R., Goodman, M.F. & O'Donnell, M. A sliding-clamp toolbelt binds high-and low-fidelity DNA polymerases simultaneously. Mol. Cell 19, 805-815 (2005). (Pubitemid 41316674)
46. Georgescu, R.E. et al. Mechanism of polymerase collision release from sliding clamps on the lagging strand. EMBO J. 28, 2981-2991 (2009).
47. Davey, M.J., Fang, L., McInerney, P., Georgescu, R.E. & O'Donnell, M. The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J. 21, 3148-3159 (2002). (Pubitemid 34670398)
48. Indiani, C., Langston, L.D., Yurieva, O., Goodman, M.F. & O'Donnell, M. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc. Natl. Acad. Sci. USA 106, 6031-6038 (2009).
49. Kaplan, D.L. & O'Donnell, M. RuvA is a sliding collar that protects Holliday junctions from unwinding while promoting branch migration. J. Mol. Biol. 355, 473-490 (2006). (Pubitemid 41785751)
50. 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). (Pubitemid 38656565)
51. Pomerantz, R.T. & O'Donnell, M. The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456, 762-766 (2008).