Hda-mediated inactivation of the DnaA protein and dnaA gene autoregulation act in concert to ensure homeostatic maintenance of the Escherichia coli chromosome

Genes and Development

Volumn 20, Issue 15, 2006, Pages 2121-2134

  Riber, Leise ^a   Olsson, Jan A ^b   Jensen, Rasmus B ^a   Skovgaard, Ole ^a   Dasgupta, Santanu ^b   Marinus, Martin G ^c   Løbner Olesen, Anders ^a  

^a ROSKILDE UNIVERSITY   (Denmark)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Chromosome replication; dnaA gene expression; E. Coli; Hda protein; RIDA

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DNA; DNA BINDING PROTEIN; REPLICATION INITIATOR PROTEIN DNAA; UNCLASSIFIED DRUG;

ARTICLE; AUTOREGULATION; BACTERIAL CELL; BACTERIAL CHROMOSOME; BACTERIAL GENE; CELL CYCLE; CELL DEATH; DNA REPLICATION; ESCHERICHIA COLI; GENE EXPRESSION; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; CELL DEATH; CHROMOSOMES, BACTERIAL; DNA REPLICATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; REPLICATION ORIGIN; TRANS-ACTIVATORS;

ESCHERICHIA COLI;

EID: 33746604804     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.379506     Document Type: Article

References (54)

1. Blattner, F.R., Plunkett III, G., Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
2. Boye, E. and Løbner-Olesen, A. 1991. Bacterial growth control studied by flow cytometry. Res. Microbiol. 142: 131-135.
3. Boye, E., Løbner-Olesen, A., and Skarstad, K. 2000. Limiting DNA replication to once and only once. EMBO Rep. 1: 479-483.
4. Braun, R.E., O'Day, K., and Wright, A. 1985. Autoregulation of the DNA replication gene dnaA in E. coli. Cell 40: 159-169.
5. Camara, J.E., Skarstad, K., and Crooke, E. 2003. Controlled initiation of chromosomal replication in Escherichia coli requires functional Hda protein. J. Bacteriol. 185: 3244-3248.
6. Camara, J.E., Breier, A.M., Brendler, T., Austin, S., Cozzarelli, N.R., and Crooke, E. 2005. Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep. 6: 736-741.
7. Campbell, J.L. and Kleckner, N. 1990. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62: 967-979.
8. Chang, A.C.Y. and Cohen, S.N. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134: 1141-1156.
9. Clark, D.J. and Maaløe, O. 1967. DNA replication and the division cycle in Escherichia coli. J. Mol. Biol. 23: 99-112.
10. Cooper, S. and Helmstetter, C.E. 1968. Chromosome replication and the division cycle of Escherichia coli B/r. J. Mol. Biol. 31: 519-540.
11. Das, N., Valjavec-Gratian, M., Basuray, A.N., Fekete, R.A., Papp, P.P., Paulsson, J., and Chattoraj, D.K. 2005. Multiple homeostatic mechanisms in the control of P1 plasmid replication. Proc. Natl. Acad. Sci. 102: 2856-2861.
12. Donachie, W.D. 1968. Relationship between cell size and time of initiation of DNA replication. Nature 219: 1077-1079.
13. Garner, J., Durrer, P., Kitchen, J., Brunner, J., and Crooke, E. 1998. Membrane-mediated release of nucleotide from an initiator of chromosomal replication, Escherichia coli DnaA, occurs with insertion of a distinct region of the chromosome into the lipid bilayer. J. Biol. Chem. 273: 5167-5173.
14. Gon, S., Camara, J.E., Klungsøyr, H.K., Crooke, E., Skarstad, K., and Beckwith, J. 2006. A novel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in E. coli. EMBO J. 25: 1137-1147.
15. 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 γδ. Cold Spring Harb. Symp. Quant. Biol. 45: 135-140.
16. Hansen, E.B., Hansen, F.G., and von Meyenburg, K. 1982. The nucleotide sequence of the dnaA gene and the first part of the dnaN gene of Escherichia coli K12. Nucleic Acids Res. 10: 7373-7385.
17. 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.
18. Katayama, T. 1994. The mutant DnaAcos protein which overinitiates replication of the Escherichia coli chromosome is inert to negative regulation for initiation. J. Biol. Chem. 269: 22075-22079.
19. 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.
20. Kato, J. and Katayama, T. 2001. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20: 4253-4262.
21. 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.
22. Lanzer, M. and Bujard, H. 1988. Promoters largely determine the efficiency of repressor action. Proc. Natl. Acad. Sci. 85: 8973-8977.
23. Lee, D.G. and Bell, S.P. 2000. ATPase switches controlling DNA replication initiation. Curr. Opin. Cell Biol. 12: 280-285.
24. Løbner-Olesen, A. and von Freiesleben, U. 1996. Chromosomal replication incompatibility in Dam methyltransferase deficient Escherichia coli cells. EMBO J. 15: 5999-6008.
25. Løbner-Olesen, A., Skarstad, K., Hansen, F.G., von Meyenburg, K., and Boye, E. 1989. The DnaA protein determines the initiation mass of Escherichia coli K- 12. Cell 57: 881-889.
26. 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.
27. Løbner-Olesen, A., Marinus, M.G., and Hansen, F.G. 2003. Role of SeqA and Dam in Escherichia coli gene expression: A global/microarray analysis. Proc. Natl. Acad. Sci. 100: 4672-4677.
28. 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.
29. McGarry, K.C., Ryan, V.T., Grimwade, J.E., and Leonard, A.C. 2004. Two discriminatory binding sites in the Escherichia coli replication origin are required for DNA strand opening by initiator DnaA-ATP. Proc. Natl. Acad. Sci. 101: 2811-2816.
30. Messer, W. and Weigel, C. 1996. Initiation of chromosome replication. In Escherichia coli and Salmonella: Cellular and molecular biology (eds. F.C. Neidhardt et al.), pp. 1578-1601. American Society for Microbiology, Washington D.C.
31. _.1997. DnaA initiator - Also a transcription factor. Mol. Microbiol. 24: 1-6.
32. Miller, J.H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Morigen, 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.
34. Morigen, Løbner-Olesen, A., and Skarstad, K. 2003. Titration of the Escherichia coli DnaA protein to excess datA sites causes destabilization of replication forks, delayed replication initiation and delayed cell division. Mol. Microbiol. 50: 349-362.
35. Nishida, S., Fujimitsu, K., Sekimizu, K., Ohmura, T., Ueda, T., and Katayama, T. 2002. A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: Evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J. Biol. Chem. 277: 14986-14995.
36. Olsson, J., Dasgupta, S., Berg, O.G., and Nordstrom, K. 2002. Eclipse period without sequestration in Escherichia coli. Mol. Microbiol. 44: 1429-1440.
37. Olsson, J.A., Nordstrom, K., Hjort, K., and Dasgupta, S. 2003. Eclipse-synchrony relationship in Escherichia coli strains with mutations affecting sequestration, initiation of replication and superhelicity of the bacterial chromosome. J. Mol. Biol. 334: 919-931.
38. Ortenberg, R., Gon, S., Porat, A., and Beckwith, J. 2004. Interactions of glutaredoxins, ribonucleotide reductase, and components of the DNA replication system of Escherichia coli. Proc. Natl. Acad. Sci. 101: 7439-7444.
39. Ote, T., Hashimoto, M., Ikeuchi, Y., Su'etsugu, M., Suzuki, T., Katayama, T., and Kato, J. 2006. Involvement of the Escherichia coli folate-binding protein YgfZ in RNA modification and regulation of chromosomal replication initiation. Mol. Microbiol. 59: 265-275.
40. Petersen, C. and Møller, L.B. 2000. Invariance of the nucleoside triphosphate pools of Escherichia coli with growth rate. J. Biol. Chem. 275: 3931-3935.
41. Riber, L. and Løbner-Olesen, A. 2005. Coordinated replication and sequestration of oriC and dnaA are required for maintaining controlled once-per-cell-cycle initiation in Escherichia coli. J. Bacteriol. 187: 5605-5613.
42. Sekimizu, K. and Kornberg, A. 1988. Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J. Biol. Chem. 263: 7131-7135.
43. Sekimizu, K., Bramhill, D., and Kornberg, A. 1987. ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50: 259-265.
44. Simmons, L.A., Breier, A.M., Cozzarelli, N.R., and Kaguni, J.M. 2004. Hyperinitiation of DNA replication in Escherichia coli leads to replication fork collapse and inviability. Mol. Microbiol. 51: 349-358.
45. Singer, M., Baker, T.A., Schnitzler, G., Deischel, S.M., Goel, M., Dove, W., Jaacks, K.J., Grossman, A.D., Erickson, J.W., and Gross, C.A. 1989. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol. Rev. 53: 1-24.
46. Skarstad, K., Boye, E., and Steen, H.B. 1986. Timing of initiation of chromosome replication in individual E. coli cells. EMBO J. 5: 1711-1717.
47. 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.
48. Speck, C., Weigel, C., and Messer, W. 1999. ATP- and ADP-dnaA protein, a molecular switch in gene regulation. EMBO J. 18: 6169-6176.
49. Su'etsugu, M., Takata, M., Kubota, T., Matsuda, Y., and Katayama, T. 2004. Molecular mechanism of DNA replication-coupled inactivation of the initiator protein in Escherichia coli: Interaction of DnaA with the sliding clamp-loaded DNA and the sliding clamp-Hda complex. Genes Cells 9: 509-522.
50. Su'etsugu, M., Shimuta, T.R., Ishida, T., Kawakami, H., and Katayama, T. 2005. Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J. Biol. Chem. 280: 6528-6536.
51. 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.
52. von Freiesleben, U., Krekling, M.A., Hansen, F.G., and Løbner-Olesen, A. 2000. The eclipse period of Escherichia coli. EMBO J. 19: 6240-6248.
53. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G., and Court, D.L. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. 97: 5978-5983.
54. Yung, B.Y., Crooke, E., and Kornberg, A. 1990. Fate of the DnaA initiator protein in replication at the origin of the Escherichia coli chromosome in vitro. J. Biol. Chem. 265: 1282-1285.