PriA mediates DNA replication pathway choice at recombination intermediates

Molecular Cell

Volumn 11, Issue 3, 2003, Pages 817-826

  Xu, Liewei ^a   Marians, Kenneth J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE III HOLOENZYME; DNA TOPOISOMERASE (ATP HYDROLYSING); DOUBLE STRANDED DNA; HOLOENZYME; PROTEIN; PROTEIN PRIA; RESTART PRIMOSOMAL PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; DNA RECOMBINATION; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; RECA GENE;

EID: 0037352498     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00061-3     Document Type: Article

References (63)

1. Al-Deib A.A., Mahdi A.A., Lloyd R.G. Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12. J. Bacteriol. 178:1996;6782-6789.
2. Arai K., Low R., Kobori J., Shlomai J., Kornberg A. Mechanism of dnaB protein action. V. Association of dnaB protein, protein n′, and other repriming proteins in the primosome of DNA replication. J. Biol. Chem. 256:1981;5273-5280.
3. Bork J.M., Cox M.M., Inman R.B. The RecOR proteins modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J. 20:2001;7313-7322.
4. Clark A.J., Sandler S.J. Homologous genetic recombination. the pieces begin to fall into place Crit. Rev. Microbiol. 20:1994;125-142.
5. 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. USA. 94:1997;3714-3719.
6. 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. 404:2000;37-41.
7. Gregg A.V., McGlynn P., Jaktaji R.P., Lloyd R.G. Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. Mol. Cell. 9:2002;241-251.
8. Griffin T.J. 4th, Kolodner R.D. Purification and preliminary characterization of the Escherichia coli K-12 recF protein. J. Bacteriol. 172:1990;6291-6299.
9. Griffith J., Shores C.G. RecA protein rapidly crystallizes in the presence of spermidine. a valuable step in its purification and physical characterization Biochemistry. 24:1985;158-162.
10. Haber J.E. DNA recombination. the replication connection Trends Biochem. Sci. 24:1999;271-275.
11. Hiasa H., Marians K.J. Primase couples leading- and lagging-strand DNA synthesis from oriC. J. Biol. Chem. 269:1994;6058-6063.
12. Hiasa H., Marians K.J. Two distinct modes of strand unlinking during theta-type DNA replication. J. Biol. Chem. 271:1996;21529-21535.
13. 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. 177:1995;783-791.
14. Itoh T., Tomizawa J. Initiation of replication of plasmid ColE1 DNA by RNA polymerase, ribonuclease H, and DNA polymerase I. Cold Spring Harb. Symp. Quant. Biol. 43:1979;409-417.
15. Iwabuchi M., Shibata T., Ohtani T., Natori M., Ando T. ATP-dependent unwinding of the double helix and extensive supercoiling by Escherichia coli recA protein in the presence of topoisomerase. J. Biol. Chem. 258:1983;12394-12404.
16. Jones J.M., Nakai H. Duplex opening by primosome protein PriA for replisome assembly on a recombination intermediate. J. Mol. Biol. 289:1999;503-516.
17. Jones J.M., Nakai H. Escherichia coli PriA helicase. fork binding orients the helicase to unwind the lagging strand side of arrested replication forks J. Mol. Biol. 312:2001;935-947.
18. Kaguni J.M., Kornberg A. Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes. Cell. 38:1984;183-190.
19. Kim S., Dallmann H.G., McHenry C.S., Marians K.J. Coupling of a replicative polymerase and helicase. a τ-DnaB interaction mediates rapid replication fork movement Cell. 84:1996;643-650.
20. Klevan L., Wang J.C. Deoxyribonucleic acid gyrase-deoxyribonucleic acid complex containing 140 base pairs of deoxyribonucleic acid and an α2 β2 protein core. Biochemistry. 19:1980;5229-5234.
21. Kogoma T. Recombination by replication. Cell. 85:1996;625-627.
22. Kowalczykowski S.C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25:2000;156-165.
23. Kuzminov A. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16:1995;373-384.
24. Kuzminov A. Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ Microbiol. Mol. Biol. Rev. 63:1999;751-813.
25. Lasken R.S., Kornberg A. The primosomal protein n′ of Escherichia coli is a DNA helicase. J. Biol. Chem. 263:1988;5512-5518.
26. Lee M.S., Marians K.J. Escherichia coli replication factor Y, a component of the primosome, can act as a DNA helicase. Proc. Natl. Acad. Sci. USA. 84:1987;8345-8349.
27. Liu J., Marians K.J. PriA-directed assembly of a primosome on D loop DNA. J. Biol. Chem. 274:1999;25033-25041.
28. 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. USA. 96:1999;3552-3555.
29. Lloyd R.G., Evans N.P., Buckman C. Formation of recombinant lacZ+ DNA in conjugational crosses with a recB mutant of Escherichia coli K-12 depends on recF, recJ, and recO. Mol. Gen. Genet. 209:1987;135-141.
30. 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 K-12. Mol. Gen. Genet. 212:1988;317-324.
31. Low R.L., Arai K., Kornberg A. Conservation of the primosome in successive stages of φX174 DNA replication. Proc. Natl. Acad. Sci. USA. 78:1981;1436-1440.
32. Luisi-DeLuca C., Kolodner R. Purification and characterization of the Escherichia coli RecO protein. Renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein. J. Mol. Biol. 236:1994;124-138.
33. Lusetti S.L., Cox M.M. The bacterial recA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71:2002;71-100.
34. 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. 216:1989;503-510.
35. Marians K.J. Prokaryotic DNA replication. Annu. Rev. Biochem. 61:1992;673-719.
36. Marians K.J. φX174-type primosomal proteins. purification and assay Methods Enzymol. 262:1995;507-521.
37. 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. 270:1997;212-221.
38. Michel B., Ehrlich S.D., Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J. 16:1997;430-438.
39. Mok M., Marians K.J. The Escherichia coli preprimosome and DnaB helicase can form replication forks that move at the same rate. J. Biol. Chem. 262:1987;16644-16654.
40. Ng J.Y., Marians K.J. The ordered assembly of the φX174-type primosome. I. Isolation and identification of intermediate protein-DNA complexes. J. Biol. Chem. 271:1996;15642-15648. a.
41. Ng J.Y., Marians K.J. The ordered assembly of the φX174-type primosome. II. Preservation of primosome composition from assembly through replication. J. Biol. Chem. 271:1996;15649-15655. b.
42. Nurse P., Liu J., Marians K.J. Two modes of PriA binding to DNA. J. Biol. Chem. 274:1999;25026-25032.
43. Peter B.J., Ullsperger C., Hiasa H., Marians K.J., Cozzarelli N.R. The structure of supercoiled intermediates in DNA replication. Cell. 94:1998;819-827.
44. Roman L.J., Kowalczykowski S.C. Characterization of the helicase activity of the Escherichia coli RecBCD enzyme using a novel helicase assay. Biochemistry. 28:1989;2863-2873.
45. Rothstein R., Michel B., Gangloff S. Replication fork pausing and recombination or "gimme a break." Genes Dev. 14:2000;1-10.
46. Sandler S.J. Multiple genetic pathways for restarting DNA replication forks in Escherichia coli K-12. Genetics. 155:2000;487-497.
47. Sandler S.J., Marians K.J. Role of PriA in replication fork reactivation in Escherichia coli. J. Bacteriol. 182:2000;9-13.
48. 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. 143:1996;5-13.
49. Sandler S.J., McCool J.D., Do T.T., Johansen R.U. PriA mutations that affect PriA-PriC function during replication restart. Mol. Microbiol. 41:2001;697-704.
50. Seigneur M., Bidnenko V., Ehrlich S.D., Michel B. RuvAB acts at arrested replication forks. Cell. 95:1998;419-430.
51. 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. 5:1986;3401-3406.
52. Shan Q., Bork J.M., Webb B.L., Inman R.B., Cox M.M. RecA protein filaments. end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins J. Mol. Biol. 265:1997;519-540.
53. Shlomai J., Kornberg A. An Escherichia coli replication protein that recognizes a unique sequence within a hairpin region in φX174 DNA. Proc. Natl. Acad. Sci. USA. 77:1980;799-803.
54. Ullsperger C., Cozzarelli N.R. Contrasting enzymatic activities of topoisomerase IV and DNA gyrase from Escherichia coli. J. Biol. Chem. 271:1996;31549-31555.
55. Umezu K., Kolodner R.D. Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein. J. Biol. Chem. 269:1994;30005-30013.
56. Umezu K., Chi N.W., Kolodner R.D. Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc. Natl. Acad. Sci. USA. 90:1993;3875-3879.
57. Velankar S.S., Soultanas P., Dillingham M.S., Subramanya H.S., Wigley D.B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell. 97:1999;75-84.
58. Webb B.L., Cox M.M., Inman R.B. An interaction between the Escherichia coli RecF and RecR proteins dependent on ATP and double-stranded DNA. J. Biol. Chem. 270:1995;31397-31404.
59. Webb B.L., Cox M.M., Inman R.B. Recombinational DNA repair. the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps Cell. 91:1997;347-356.
60. Xu L., Marians K.J. A dynamic RecA filament permits DNA polymerase-catalyzed extension of the invading strand in recombination intermediates. J. Biol. Chem. 277:2002;14321-14328.
61. Yuzhakov A., Turner J., O'Donnell M. Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell. 86:1996;877-886.
62. Zavitz K.H., Marians K.J. Dissecting the functional role of PriA protein-catalysed primosome assembly in Escherichia coli DNA replication. Mol. Microbiol. 5:1991;2869-2873.
63. Zavitz K.H., Marians K.J. ATPase-deficient mutants of the Escherichia coli DNA replication protein PriA are capable of catalyzing the assembly of active primosomes. J. Biol. Chem. 267:1992;6933-6940.