Titration of the Escherichia coli DnaA protein to excess datA sites causes destabilization of replication forks, delayed replication initiation and delayed cell division

Molecular Microbiology

Volumn 50, Issue 1, 2003, Pages 349-362

  Morigen, ^a   Løbner Olesen, Anders ^b   Skarstad, Kirsten ^a  

^a INSTITUTE OF CANCER RESEARCH   (Norway)

^b ROSKILDE UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; ESCHERICHIA COLI PROTEIN;

ARTICLE; BINDING SITE; CELL DIVISION; CHROMOSOME REPLICATION; CONTROLLED STUDY; GENE DOSAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TITRIMETRY; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL DIVISION; DNA HELICASES; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXODEOXYRIBONUCLEASE V; GENE DOSAGE; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN BINDING; REC A RECOMBINASES; REPLICATION ORIGIN; SOS RESPONSE (GENETICS); SUPPRESSION, GENETIC; TRANSCRIPTION FACTORS; TRANSFORMATION, BACTERIAL; ULTRAVIOLET RAYS;

ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0141707074     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03695.x     Document Type: Article

References (68)

1. Atlung, T., and Hansen, F.G. (1993) Three distinct chromosome replication states are induced by increasing concentrations of DnaA protein in Escherichia coli. J Bacteriol 175: 6537-6545.
2. Atlung, T., and Hansen, F.G. (2002) Effect of different concentrations of H-NS protein on chromosome replication and the cell cycle in Escherichia coli. J Bacteriol 184: 1843-1850.
3. Begg, K.J., and Donachie, W.D. (1991) Experiments on chromosome separation and positioning in Escherichia coli. New Biol 3: 475-486.
4. Bernander, R., Dasgupta, S., and Nordstrom, K. (1991) The E. coli cell cycle and the plasmid R1 replication cycle in the absence of the DnaA protein. Cell 64: 1145-1153.
5. Bierne, H., and Michel, B. (1994) When replication forks stop. Mol Microbiol 13: 17-23.
6. Bogan, J.A., and Helmstetter, C.E. (1997) DNA sequestration and transcription in the oriC region of Escherichia coli. Mol Microbiol 26: 889-896.
7. Boye, E., and Løbner-Olesen, A. (1991) Bacterial growth control studied by flow cytometry. Res Microbiol 142: 131-135.
8. Boye, E., Stokke, T., Kleckner, N., and Skarstad, K. (1996) Coordinating DNA replication initiation with cell growth: differential roles for DnaA and SeqA proteins. Proc Natl Acad Sci USA 93: 12206-12211.
9. Boye, E., Løbner-Olesen, A., and Skarstad, K. (2000) Limiting DNA replication to once and only once. EMBO Rep 1: 479-483.
10. Boye, E., Blinkova, A., and Walker, J.R. (2001) Defective initiation in an Escherichia coli dnaA (Cs, Sx) mutant. Biochimie 83: 25-32.
11. Bramhill, D., and Kornberg, A. (1988) Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52: 743-755.
12. Brewer, B.J. (1988) When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53: 679-686.
13. Campbell, J.L., and Kleckner, N. (1990) E. coli oriC and the dnaA gene promoter are sequestered from dam methyl-transferase following the passage of the chromosomal replication fork. Cell 62: 967-979.
14. Cha, R.S., and Kleckner, N. (2002) ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
15. Clark, D.J., and Maaløe, O. (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 23: 99-112.
16. Fram, R.J., Mack, S.L., George, M., and Marinus, M.G. (1989) DNA repair mechanisms affecting cytotoxicity by streptozotocin in E. coli. Mutat Res 218: 125-133.
17. von Freiesleben, U., Rasmussen, K.V., and Schaechter, M. (1994) SeqA limits DnaA activity in replication from oriC in Escherichia coli. Mol Microbiol 14: 763-772.
18. von Freiesleben, U., Krekling, M.A., Hansen, F.G., and Løbner-Olesen, A. (2000a) The eclipse period of Escherichia coli. EMBO J 19: 6240-6248.
19. von Freiesleben, U., Rasmussen, K.V., Atlung, T., and Hansen, F.G. (2000b) Rifampicin-resistant initiation of chromosome replication from oriC in ihf mutants. Mol Microbiol 37: 1087-1093.
20. French, S. (1992) Consequences of replication fork movement through transcription units in vivo. Science 258: 1362-1365.
21. Fuller, R.S., Funnell, B.E., and Kornberg, A. (1984) The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38: 889-900.
22. Gines-Candelaria, E., Blinkova, A., and Walker, J.R. (1995) Mutations in Escherichia coli dnaA which suppress a dnaX(Ts) polymerization mutation and are dominant when located in the chromosomal allele and recessive on plasmids. J Bacteriol 177: 705-715.
23. Grompone, G., Ehrlich, S.D., and Michel, B. (2003) Replication restart in gyrB Escherichia coli mutants. Mol Microbiol 48: 845-854.
24. Guyer, M.S., Reed, R.R., Steitz, J.A., and Low, K.B. (1981) Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp Quant Biol 45 (Part 1): 135-140.
25. Hansen, F.G., Christensen, B.B., and Atlung, T. (1991) The initiator titration model: computer simulation of chromosome and minichromosome control. Res Microbiol 142: 161-167.
26. Hwang, D.S., and Kornberg, A. (1992) Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem 267: 23083-23086.
27. Jensen, K.F. (1993) The Escherichia coli K-12 'wild types' W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175: 3401-3407.
28. Katayama, T., Kubota, T., Kurokawa, K., Crooke, E., and Sekimizu, K. (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94: 61-71.
29. Kato, J., and Katayama, T. (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20: 4253-4262.
30. Kitagawa, R., Mitsuki, H., Okazaki, T., and Ogawa, T. (1996) A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol Microbiol 19: 1137-1147.
31. Kitagawa, R., Ozaki, T., Moriya, S., and Ogawa, T. (1998) Negative control of replication initiation by a novel chromosomal locus exhibiting exceptional affinity for Escherichia coli DnaA protein. Genes Dev 12: 3032-3043.
32. Kogoma, T., Cadwell, G.W., Barnard, K.G., and Asai, T. (1996) The DNA replication priming protein, PriA, is required for homologous recombination and double-strand break repair. J Bacteriol 178: 1258-1264.
33. Kornberg, A., and Baker, T.A. (1992) DNA Replication. New York: Freeman.
34. Kowalczykowski, S.C., Dixon, D.A., Eggleston, A.K., Lauder, S.D., and Rehrauer, W.M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58: 401-465.
35. Kuzminov, A. (1995a) Collapse and repair of replication forks in Escherichia coli. Mol Microbiol 16: 373-384.
36. Kuzminov, A. (1995b) Instability of inhibited replication forks in E. coli. Bioessays 17: 733-741.
37. Løbner-Olesen, A., and von Freiesleben, U. (1996) Chromosomal replication incompatibility in Dam methyltransferase deficient Escherichia coli cells. EMBO J 15: 5999-6008.
38. Løbner-Olesen, A., Hansen, F.G., Rasmussen, K.V., Martin, B., and Kuempel, P.L. (1994) The initiation cascade for chromosome replication in wild-type and Dam methyltransferase deficient Escherichia coli cells. EMBO J 13: 1856-1862.
39. Lu, M., Campbell, J.L., Boye, E., and Kleckner, N. (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77: 413-426.
40. Magee, T.R., Asai, T., Malka, D., and Kogoma, T. (1992) DNA damage-inducible origins of DNA replication in Escherichia coli. EMBO J 11: 4219-4225.
41. Masters, M., Paterson, T., Popplewell, A.G., Owen-Hughes, T., Pringie, J.H., and Begg, K.J. (1989) The effect of DnaA protein levels and the rate of initiation at oriC on transcription originating in the ftsQ and ftsA genes in in vivo experiments. Mol Gen Genet 216: 475-483.
42. Messer, W., and Weigel, C. (1997) DnaA initiator - also a transcription factor. Mol Microbiol 24: 1-6.
43. Michel, B., Ehrlich, S.D., and Uzest, M. (1997) DNA double-strand breaks caused by replication arrest. EMBO J 16: 430-438.
44. Morigen, M., Boye, E., Skarstad, K., and Løbner-Olesen, A. (2001) Regulation of chromosomal replication by DnaA protein availability in Escherichia coli: effects of the datA region. Biochim Biophys Acta 1521: 73-80.
45. Mount, D.W., Low, K.B., and Edmiston, S.J. (1972) Dominant mutations (lex) in Escherichia coli K-12 which affect radiation sensitivity and frequency of ultraviolet light-induced mutations. J Bacteriol 112: 886-893.
46. Ogawa, T., Yamada, Y., Kuroda, T., Kishi, T., and Moriya, S. (2002) The datA locus predominantly contributes to the initiator titration mechanism in the control of replication initiation in Escherichia coli. Mol Microbiol 44: 1367-1375.
47. Rangarajan, S., Woodgate, R., and Goodman, M.F. (2002) Replication restart in UV-irradiated Escherichia coli involving pols II, III, V, PriA, RecA and RecFOR proteins. Mol Microbiol 43: 617-628.
48. Robu, M.E., Inman, R.B., and Cox, M.M. (2001) RecA protein promotes the regression of stalled replication forks in vitro. Proc Natl Acad Sci USA 98: 8211-8218.
49. Rothstein, R., Michel, B., and Gangloff, S. (2000) Replication fork pausing and recombination or 'gimme a break'. Genes Dev 14: 1-10.
50. Sandler, S.J., and Marians, K.J. (2000) Role of PriA in replication fork reactivation in Escherichia coli. J Bacteriol 182: 9-13.
51. Sassanfar, M., and Roberts, J.W. (1990) Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol 212: 79-96.
52. Schaper, S., and Messer, W. (1995) Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J Biol Chem 270: 17622-17626.
53. Seigneur, M., Ehrlich, S.D., and Michel, B. (2000) RuvABC-dependent double-strand breaks in dnaBts mutants require RecA. Mol Microbiol 38: 565-574.
54. Skarstad, K., and Wold, S. (1995) The speed of the Escherichia coli fork in vivo depends on the DnaB:DnaC ratio. Mol Microbiol 17: 825-831.
55. Skarstad, K., Boye, E., and Steen, H.B. (1986) Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J 5: 1711-1717.
56. Skarstad, K., Løbner-Olesen, A., Atlung, T., von Meyenburg, K., and Boye, E. (1989) Initiation of DNA replication in Escherichia coli after overproduction of the DnaA protein. Mol Gen Genet 218: 50-56.
57. Skarstad, K., Baker, T.A., and Kornberg, A. (1990) Strand separation required for initiation of replication at the chromosomal origin of E. coli is facilitated by a distant RNA-DNA hybrid. EMBO J 9: 2341-2348.
58. Skarstad, K., Lueder, G., Lurz, R., Speck, C., and Messer, W. (2000) The Escherichia coli SeqA protein binds specifically and co-operatively to two sites in hemimethylated and fully methylated oriC. Mol Microbiol 36: 1319-1326.
59. Smith, R.W.P., McAteer, S., and Masters, M. (1996) The coupling between ftsZ transcription and initiation of DNA replication is not mediated by the DnaA-boxes upstream of ftsZ or by DnaA. Mol Microbiol 21: 361-372.
60. Speck, C., and Messer, W. (2001) Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J 20: 1469-1476.
61. Speck, C., Weigel, C., and Messer, W. (1999) ATP- and ADP-DnaA protein, a molecular switch in gene regulation. EMBO J 18: 6169-6176.
62. Suter, W., and Jaeger, I. (1982) Comparative evaluation of different pairs of DNA repair-deficient and DNA repair-proficient bacterial tester strains for rapid detection of chemical mutagens and carcinogens. Mutat Res 97: 1-18.
63. Taghbalout, A., Landoulsi, A., Kern, R., Yamazoe, M., Hiraga, S., Holland, B., et al. (2000) Competition between the replication initiator DnaA and the sequestration factor SeqA for binding to the hemimethylated chromosomal origin of E. coli in vitro. Genes Cells 5: 873-884.
64. Torheim, N.K., Boye, E., Løbner-Olesen, A., Stokke, T., and Skarstad, K. (2000) The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37: 629-638.
65. Vadi, H.V. (1983) Differences in transformation of repair-deficient mutants of E. coli. Carcinogenesis 4: 1379-1384.
66. Walker, G.C. (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48: 60-93.
67. Wold, S., Skarstad, K., Steen, H.B., Stokke, T., and Boye, E. (1994) The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. EMBO J 13: 2097-2102.
68. Wold, S., Boye, E., Slater, S., Kleckner, N., and Skarstad, K. (1998) Effects of purified SeqA protein on oriC-dependent DNA replication in vitro. EMBO J 17: 4158-4165.