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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2004 Jan 29;359(1441):71–77. doi: 10.1098/rstb.2003.1366

Mechanisms of replication fork restart in Escherichia coli.

Kenneth J Marians 1
PMCID: PMC1693301  PMID: 15065658

Abstract

Replication of the genome is crucial for the accurate transmission of genetic information. It has become clear over the last decade that the orderly progression of replication forks in both prokaryotes and eukaryotes is disrupted with high frequency by encounters with various obstacles either on or in the template strands. Survival of the organism then becomes dependent on both removal of the obstruction and resumption of replication. This latter point is particularly important in bacteria, where the number of replication forks per genome is nominally only two. Replication restart in Escherichia coli is accomplished by the action of the restart primosomal proteins, which use both recombination intermediates and stalled replication forks as substrates for loading new replication forks. These reactions have been reconstituted with purified recombination and replication proteins.

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Selected References

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  1. Bouché J. P., Zechel K., Kornberg A. dnaG gene product, a rifampicin-resistant RNA polymerase, initiates the conversion of a single-stranded coliphage DNA to its duplex replicative form. J Biol Chem. 1975 Aug 10;250(15):5995–6001. [PubMed] [Google Scholar]
  2. Clark A. J., Sandler S. J. Homologous genetic recombination: the pieces begin to fall into place. Crit Rev Microbiol. 1994;20(2):125–142. doi: 10.3109/10408419409113552. [DOI] [PubMed] [Google Scholar]
  3. Courcelle J., Carswell-Crumpton C., Hanawalt P. C. recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3714–3719. doi: 10.1073/pnas.94.8.3714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cox M. M., Goodman M. F., Kreuzer K. N., Sherratt D. J., Sandler S. J., Marians K. J. The importance of repairing stalled replication forks. Nature. 2000 Mar 2;404(6773):37–41. doi: 10.1038/35003501. [DOI] [PubMed] [Google Scholar]
  5. Fuller R. S., Funnell B. E., Kornberg A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell. 1984 Oct;38(3):889–900. doi: 10.1016/0092-8674(84)90284-8. [DOI] [PubMed] [Google Scholar]
  6. Horiuchi T., Fujimura Y. Recombinational rescue of the stalled DNA replication fork: a model based on analysis of an Escherichia coli strain with a chromosome region difficult to replicate. J Bacteriol. 1995 Feb;177(3):783–791. doi: 10.1128/jb.177.3.783-791.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kaguni J. M., Kornberg A. Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes. Cell. 1984 Aug;38(1):183–190. doi: 10.1016/0092-8674(84)90539-7. [DOI] [PubMed] [Google Scholar]
  8. Kim S., Dallmann H. G., McHenry C. S., Marians K. J. Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement. Cell. 1996 Feb 23;84(4):643–650. doi: 10.1016/s0092-8674(00)81039-9. [DOI] [PubMed] [Google Scholar]
  9. Kogoma T., Cadwell G. W., Barnard K. G., Asai T. The DNA replication priming protein, PriA, is required for homologous recombination and double-strand break repair. J Bacteriol. 1996 Mar;178(5):1258–1264. doi: 10.1128/jb.178.5.1258-1264.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kogoma T. Recombination by replication. Cell. 1996 May 31;85(5):625–627. doi: 10.1016/s0092-8674(00)81229-5. [DOI] [PubMed] [Google Scholar]
  11. Kowalczykowski S. C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem Sci. 2000 Apr;25(4):156–165. doi: 10.1016/s0968-0004(00)01569-3. [DOI] [PubMed] [Google Scholar]
  12. Kuzminov A. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev. 1999 Dec;63(4):751-813, table of contents. doi: 10.1128/mmbr.63.4.751-813.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lane H. E., Denhardt D. T. The rep mutation. IV. Slower movement of replication forks in Escherichia coli rep strains. J Mol Biol. 1975 Sep 5;97(1):99–112. doi: 10.1016/s0022-2836(75)80025-8. [DOI] [PubMed] [Google Scholar]
  14. LeBowitz J. H., McMacken R. The Escherichia coli dnaB replication protein is a DNA helicase. J Biol Chem. 1986 Apr 5;261(10):4738–4748. [PubMed] [Google Scholar]
  15. Lee E. H., Kornberg A. Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n' protein. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3029–3032. doi: 10.1073/pnas.88.8.3029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Liu J., Xu L., Sandler S. J., Marians K. J. Replication fork assembly at recombination intermediates is required for bacterial growth. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3552–3555. doi: 10.1073/pnas.96.7.3552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lloyd R. G., Evans N. P., Buckman C. Formation of recombinant lacZ+ DNA in conjugational crosses with a recB mutant of Escherichia coli K12 depends on recF, recJ, and recO. Mol Gen Genet. 1987 Aug;209(1):135–141. doi: 10.1007/BF00329848. [DOI] [PubMed] [Google Scholar]
  18. Lloyd R. G., Porton M. C., Buckman C. Effect of recF, recJ, recN, recO and ruv mutations on ultraviolet survival and genetic recombination in a recD strain of Escherichia coli K12. Mol Gen Genet. 1988 May;212(2):317–324. doi: 10.1007/BF00334702. [DOI] [PubMed] [Google Scholar]
  19. Lusetti Shelley L., Cox Michael M. The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem. 2001 Nov 9;71:71–100. doi: 10.1146/annurev.biochem.71.083101.133940. [DOI] [PubMed] [Google Scholar]
  20. Mahdi A. A., Lloyd R. G. Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair. Mol Gen Genet. 1989 Apr;216(2-3):503–510. doi: 10.1007/BF00334397. [DOI] [PubMed] [Google Scholar]
  21. Marians K. J. Enzymology of DNA in replication in prokaryotes. CRC Crit Rev Biochem. 1984;17(2):153–215. doi: 10.3109/10409238409113604. [DOI] [PubMed] [Google Scholar]
  22. Marians K. J. Prokaryotic DNA replication. Annu Rev Biochem. 1992;61:673–719. doi: 10.1146/annurev.bi.61.070192.003325. [DOI] [PubMed] [Google Scholar]
  23. Masai H., Asai T., Kubota Y., Arai K., Kogoma T. Escherichia coli PriA protein is essential for inducible and constitutive stable DNA replication. EMBO J. 1994 Nov 15;13(22):5338–5345. doi: 10.1002/j.1460-2075.1994.tb06868.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McCool J. D., Sandler S. J. Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2::kan mutant. Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8203–8210. doi: 10.1073/pnas.121007698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McGlynn P., Al-Deib A. A., Liu J., Marians K. J., Lloyd R. G. The DNA replication protein PriA and the recombination protein RecG bind D-loops. J Mol Biol. 1997 Jul 11;270(2):212–221. doi: 10.1006/jmbi.1997.1120. [DOI] [PubMed] [Google Scholar]
  26. McHenry C. S. Purification and characterization of DNA polymerase III'. Identification of tau as a subunit of the DNA polymerase III holoenzyme. J Biol Chem. 1982 Mar 10;257(5):2657–2663. [PubMed] [Google Scholar]
  27. Michel B., Ehrlich S. D., Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J. 1997 Jan 15;16(2):430–438. doi: 10.1093/emboj/16.2.430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Minden J. S., Marians K. J. Replication of pBR322 DNA in vitro with purified proteins. Requirement for topoisomerase I in the maintenance of template specificity. J Biol Chem. 1985 Aug 5;260(16):9316–9325. [PubMed] [Google Scholar]
  29. Nurse P., Zavitz K. H., Marians K. J. Inactivation of the Escherichia coli priA DNA replication protein induces the SOS response. J Bacteriol. 1991 Nov;173(21):6686–6693. doi: 10.1128/jb.173.21.6686-6693.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Peter B. J., Ullsperger C., Hiasa H., Marians K. J., Cozzarelli N. R. The structure of supercoiled intermediates in DNA replication. Cell. 1998 Sep 18;94(6):819–827. doi: 10.1016/s0092-8674(00)81740-7. [DOI] [PubMed] [Google Scholar]
  31. Pierce A. J., Stark J. M., Araujo F. D., Moynahan M. E., Berwick M., Jasin M. Double-strand breaks and tumorigenesis. Trends Cell Biol. 2001 Nov;11(11):S52–S59. doi: 10.1016/s0962-8924(01)02149-3. [DOI] [PubMed] [Google Scholar]
  32. Rothstein R., Michel B., Gangloff S. Replication fork pausing and recombination or "gimme a break". Genes Dev. 2000 Jan 1;14(1):1–10. [PubMed] [Google Scholar]
  33. Sandler S. J., Marians K. J. Role of PriA in replication fork reactivation in Escherichia coli. J Bacteriol. 2000 Jan;182(1):9–13. doi: 10.1128/jb.182.1.9-13.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sandler S. J. Multiple genetic pathways for restarting DNA replication forks in Escherichia coli K-12. Genetics. 2000 Jun;155(2):487–497. doi: 10.1093/genetics/155.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sandler S. J., Samra H. S., Clark A. J. Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. Genetics. 1996 May;143(1):5–13. doi: 10.1093/genetics/143.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Seigneur M., Bidnenko V., Ehrlich S. D., Michel B. RuvAB acts at arrested replication forks. Cell. 1998 Oct 30;95(3):419–430. doi: 10.1016/s0092-8674(00)81772-9. [DOI] [PubMed] [Google Scholar]
  37. Seufert W., Messer W. Initiation of Escherichia coli minichromosome replication at oriC and at protein n' recognition sites. Two modes for initiating DNA synthesis in vitro. EMBO J. 1986 Dec 1;5(12):3401–3406. doi: 10.1002/j.1460-2075.1986.tb04656.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shlomai J., Kornberg A. An Escherichia coli replication protein that recognizes a unique sequence within a hairpin region in phi X174 DNA. Proc Natl Acad Sci U S A. 1980 Feb;77(2):799–803. doi: 10.1073/pnas.77.2.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tougu K., Peng H., Marians K. J. Identification of a domain of Escherichia coli primase required for functional interaction with the DnaB helicase at the replication fork. J Biol Chem. 1994 Feb 11;269(6):4675–4682. [PubMed] [Google Scholar]
  40. WATSON J. D., CRICK F. H. Genetical implications of the structure of deoxyribonucleic acid. Nature. 1953 May 30;171(4361):964–967. doi: 10.1038/171964b0. [DOI] [PubMed] [Google Scholar]
  41. Xu Liewei, Marians Kenneth J. PriA mediates DNA replication pathway choice at recombination intermediates. Mol Cell. 2003 Mar;11(3):817–826. doi: 10.1016/s1097-2765(03)00061-3. [DOI] [PubMed] [Google Scholar]
  42. Yuzhakov A., Turner J., O'Donnell M. Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell. 1996 Sep 20;86(6):877–886. doi: 10.1016/s0092-8674(00)80163-4. [DOI] [PubMed] [Google Scholar]
  43. Zavitz K. H., Marians K. J. Dissecting the functional role of PriA protein-catalysed primosome assembly in Escherichia coli DNA replication. Mol Microbiol. 1991 Dec;5(12):2869–2873. doi: 10.1111/j.1365-2958.1991.tb01846.x. [DOI] [PubMed] [Google Scholar]

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