The DnaA Protein Is Not the Limiting Factor for Initiation of Replication in
Cell cycle regulation of the bacterium Escherichia coli has been studied for many years, and its understanding is complicated by the fact that overlapping replication cycles occur during growth in rich media. Under such conditions cells initiate several copies of the chromosome. The active form of the CDC6-like DnaA protein is required for initiation of synchronous and well-timed replication cycles and is in a sense the motor of the cell cycle machine. It has long been debated whether it is the accumulation of enough ATP-DnaA that triggers initiation and determines the replication frequency. In this work we have constructed a strain where the “accumulation of ATP-DnaA triggers initiation” model could be tested. Our results indicate that this model requires some modification. We suggest that cell cycle regulation in E. coli has similarities to that of eukaryotes in that origins are “licensed” to initiate by a cell cycle motor and that the precise timing depends on other signaling.
Vyšlo v časopise:
The DnaA Protein Is Not the Limiting Factor for Initiation of Replication in. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005276
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005276
Souhrn
Cell cycle regulation of the bacterium Escherichia coli has been studied for many years, and its understanding is complicated by the fact that overlapping replication cycles occur during growth in rich media. Under such conditions cells initiate several copies of the chromosome. The active form of the CDC6-like DnaA protein is required for initiation of synchronous and well-timed replication cycles and is in a sense the motor of the cell cycle machine. It has long been debated whether it is the accumulation of enough ATP-DnaA that triggers initiation and determines the replication frequency. In this work we have constructed a strain where the “accumulation of ATP-DnaA triggers initiation” model could be tested. Our results indicate that this model requires some modification. We suggest that cell cycle regulation in E. coli has similarities to that of eukaryotes in that origins are “licensed” to initiate by a cell cycle motor and that the precise timing depends on other signaling.
Zdroje
1. Bramhill D, 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. 2830993
2. Ozaki S, Katayama T (2009) DnaA structure, function, and dynamics in the initiation at the chromosomal origin. Plasmid 62: 71–82. doi: 10.1016/j.plasmid.2009.06.003 19527752
3. Sekimizu K, Bramhill D, Kornberg A (1987) ATP activates DnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50: 259–265. 3036372
4. Fuller RS, Funnell BE, Kornberg A (1984) The DnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38: 889–900. 6091903
5. McGarry KC, Ryan VT, Grimwade JE, Leonard AC (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 U S A 101: 2811–2816. 14978287
6. Speck C, Messer W (2001) Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J 20: 1469–1476. 11250912
7. Ozaki S, Kawakami H, Nakamura K, Fujikawa N, Kagawa W, et al. (2008) A Common Mechanism for the ATP-DnaA-dependent Formation of Open Complexes at the Replication Origin. J Biol Chem 283: 8351–8362. doi: 10.1074/jbc.M708684200 18216012
8. Cassler MR, Grimwade JE, Leonard AC (1995) Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J 14: 5833–5841. 8846776
9. Hansen FG, Christensen BB, Atlung T (1991) The initiator titration model: computer simulation of chromosome and minichromosome control. Res Microbiol 142: 161–167. 1925015
10. Baker TA, Kornberg A (1988) Transcriptional activation of initiation of replication from the E. coli chromosomal origin: An RNA-DNA hybrid near oriC. Cell 55: 113–123. 2458841
11. Lark KG (1972) Evidence for the direct involvement of RNA in the initiation of DNA replication in Escherichia coli 15T-. J Mol Biol 64: 47–60. 4552485
12. Messer W (1972) Initiation of deoxyribonucleic acid replication in Escherichia coli B-r: chronology of events and transcriptional control of initiation. J Bacteriol 112: 7–12. 4562418
13. Skarstad K, Baker TA, 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. 1694129
14. Ishida T, Akimitsu N, Kashioka T, Hatano M, Kubota T, et al. (2004) DiaA, a Novel DnaA-binding Protein, Ensures the Timely Initiation of Escherichia coli Chromosome Replication. J Biol Chem 279: 45546–45555. 15326179
15. Keyamura K, Fujikawa N, Ishida T, Ozaki S, Su'etsugu M, et al. (2007) The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP DnaA-specific initiation complexes. Genes Dev 21: 2083–2099. 17699754
16. Keyamura K, Abe Y, Higashi M, Ueda T, Katayama T (2009) DiaA dynamics are coupled with changes in initial origin complexes leading to helicase loading. J Biol Chem 284: 25038–25050 doi: 10.1074/jbc.M109.002717 19632993
17. Atlung T, Clausen ES, Hansen FG (1985) Autoregulation of the dnaA gene of Escherichia coli K12. Mol Gen Genet 200: 442–450. 2995766
18. Braun RE, O'Day K, Wright A (1985) Autoregulation of the DNA replication gene dnaA in E. coli K-12. Cell 40: 159–169. 2981626
19. Kücherer C, Lother H, Kolling R, Schauzu MA, Messer W (1986) Regulation of transcription of the chromosomal dnaA gene of Escherichia coli. Mol Gen Genet 205: 115–121. 3025553
20. Speck C, Weigel C, Messer W (1999) ATP- and ADP-DnaA protein, a molecular switch in gene regulation. EMBO J 18: 6169–6176. 10545126
21. Messer W, Weigel C (1997) DnaA initiator-also a transcription factor. Mol Microbiol 24: 1–6. 9140960
22. Asai T, Chen CP, Nagata T, Takanami M, Imai M (1992) Transcription in vivo within the replication origin of the Escherichia coli chromosome: a mechanism for activating initiation of replication. Mol Gen Genet 231: 169–178. 1736090
23. Flåtten I, Morigen, Skarstad K (2009) DnaA protein interacts with RNA polymerase and partially protects it from the effect of rifampicin. Mol Microbiol 71: 1018–1030. doi: 10.1111/j.1365-2958.2008.06585.x 19170875
24. Kitagawa R, Mitsuki H, Okazaki T, Ogawa T (1996) A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol Microbiol 19: 1137–1147. 8830270
25. Hansen FG, Christensen BB, Atlung T (2007) Sequence Characteristics Required for Cooperative Binding and Efficient in Vivo Titration of the Replication Initiator Protein DnaA in E. coli. J Mol Biol 367: 942–952. 17316685
26. Kitagawa R, Ozaki T, Moriya S, 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. 9765205
27. Kasho K, Katayama T (2013) DnaA binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation. Proc Natl Acad Sci U S A 110: 936–941. doi: 10.1073/pnas.1212070110 23277577
28. Kato J, Katayama T (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20: 4253–4262. 11483528
29. Fujimitsu K, Su'etsugu M, Yamaguchi Y, Mazda K, Fu N, et al. (2008) Modes of Overinitiation, dnaA Gene Expression, and Inhibition of Cell Division in a Novel Cold-Sensitive hda Mutant of Escherichia coli. J Bacteriol 190: 5368–5381. doi: 10.1128/JB.00044-08 18502852
30. Nishida S, Fujimitsu K, Sekimizu K, Ohmura T, Ueda T, et al. (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. 11839737
31. Morigen, Molina F, Skarstad K (2005) Deletion of the datA Site Does Not Affect Once-per-Cell-Cycle Timing but Induces Rifampin-Resistant Replication. J Bacteriol 187: 3913–3920. 15939703
32. Leonard AC, Grimwade JE (2010) Regulation of DnaA Assembly and Activity: Taking Directions from the Genome. Annu Rev Microbiol 65:19–35
33. Atlung T, Løbner-Olesen A, Hansen FG (1987) Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli. Mol Gen Genet 206: 51–59. 3033441
34. Atlung T, Hansen FG (1993) Three distinct chromosome replication states are induced by increasing concentrations of DnaA protein in Escherichia coli. J Bacteriol 175: 6537–6545. 8407830
35. Løbner-Olesen A, Skarstad K, Hansen FG, von Meyenburg K, Boye E (1989) The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57: 881–889. 2541928
36. Pierucci O, Helmstetter CE, Rickert M, Weinberger M, Leonard AC (1987) Overexpression of the dnaA gene in Escherichia coli B/r: chromosome and minichromosome replication in the presence of rifampin. J Bacteriol 169: 1871–1877. 3032899
37. Pierucci O, Rickert M, Helmstetter CE (1989) DnaA protein overproduction abolishes cell cycle specificity of DNA replication from oriC in Escherichia coli. J Bacteriol 171: 3760–3766. 2544554
38. Skarstad K, Løbner-Olesen A, Atlung T, von Meyenburg K, Boye E (1989) Initiation of DNA replication in Escherichia coli after overproduction of the DnaA protein. Mol Gen Genet 218: 50–56. 2550764
39. Xu YC, Bremer H (1988) Chromosome replication in Escherichia coli induced by oversupply of DnaA. Mol Gen Genet 211: 138–142. 2830461
40. Churchward G, Holmans P, Bremer H (1983) Increased expression of the dnaA gene has no effect on DNA replication in a dnaA+ strain of Escherichia coli. Mol Gen Genet 192: 506–508. 6361492
41. Torheim NK, Boye E, Løbner-Olesen A, Stokke T, Skarstad K (2000) The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37: 629–638. 10931356
42. Charbon G, Riber L, Cohen M, Skovgaard O, Fujimitsu K, et al. (2011) Suppressors of DnaAATP imposed overinitiation in Escherichia coli. Mol Microbiol 79: 914–928. doi: 10.1111/j.1365-2958.2010.07493.x 21299647
43. Koppes L (1987) OriC plasmids do not affect the timing of chromosome replication in Escherichia coli. Mol Gen Genet 209: 188–192. 3312956
44. Stokke C, Flåtten I, Skarstad K (2012) An Easy-To-Use Simulation Program Demonstrates Variations in Bacterial Cell Cycle Parameters Depending on Medium and Temperature. PLoS ONE 7: e30981. doi: 10.1371/journal.pone.0030981 22348034
45. Boye E, Løbner-Olesen A (1991) Bacterial growth control studied by flow cytometry. Res Microbiol 142: 131–135. 1925010
46. Skarstad K, Boye E, Steen HB (1986) Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J 5: 1711–1717. 3527695
47. Simmons LA, Breier AM, Cozzarelli NR, Kaguni JM (2004) Hyperinitiation of DNA replication in Escherichia coli leads to replication fork collapse and inviability. Mol Microbiol 51: 349–358. 14756777
48. Sekimizu K, Bramhill D, Kornberg A (1988) Sequential early stages in the in vitro initiation of replication at the origin of the Escherichia coli chromosome. J Biol Chem 263: 7124–7130. 2835363
49. Sakakibara Y, Tsukano H, Sako T. (981) Organization and transcription of the dnaA and dnaN genes of Escherichia coli. Gene 13: 47–55. 6453739
50. Ma Q, Wood TK (2011) Protein acetylation in prokaryotes increases stress resistance. Biochem Biophys Res Commun 410: 846–851. doi: 10.1016/j.bbrc.2011.06.076 21703240
51. Morigen, Odsbu I, Skarstad K (2009) Growth rate dependent numbers of SeqA structures organize the multiple replication forks in rapidly growing Escherichia coli. Genes Cells 14: 643–657. doi: 10.1111/j.1365-2443.2009.01298.x 19371375
52. Hansen FG, Atlung T, Braun RE, Wright A, Hughes P, et al. (1991) Initiator (DnaA) protein concentration as a function of growth rate in Escherichia coli and Salmonella typhimurium. J Bacteriol 173: 5194–5199. 1860829
53. Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. In: Cold Spring Harb Perspect Biol. 2013 Apr 1;5(4):a012922. doi: 10.1101/cshperspect.a012922 23471435
54. Hill NS KRCDLPA (2012) Cell size and the initiation of DNA replication in bacteria. PLoS Genet 8: e1002549. doi: 10.1371/journal.pgen.1002549 22396664
55. Hill NS BPSYLP (2013) A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism. PLoS Genet 9: e1003663. doi: 10.1371/journal.pgen.1003663 23935518
56. Donachie WD, Blakely GW (2003) Coupling the initiation of chromosome replication to cell size in Escherichia coli. Curr Opin Microbiol 6: 146–150. 12732304
57. Kurokawa K, Nishida S, Emoto A, Sekimizu K, Katayama T (1999) Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J 18: 6642–6652. 10581238
58. Katayama T, Fujimitsu K, Ogawa T (2001) Multiple pathways regulating DnaA function in Escherichia coli: distinct roles for DnaA titration by the datA locus and the regulatory inactivation of DnaA. Biochimie 83: 13–17. 11254969
59. Clark DJ, Maaloe O (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 23: 99–112.
60. Haldimann A, Wanner BL (2001) Conditional-Replication, Integration, Excision, and Retrieval Plasmid-Host Systems for Gene Structure-Function Studies of Bacteria. J Bacteriol 183: 6384–6393. 11591683
61. Morigen, Løbner-Olesen A, 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. 14507385
62. Wold S, Skarstad K, Steen HB, Stokke T, Boye E (1994) The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. EMBO J 13: 2097–2102. 8187762
63. Fossum S, Soreide S, Skarstad K (2003) Lack of SeqA focus formation, specific DNA binding and proper protein multimerization in the Escherichia coli sequestration mutant seqA2. Mol Microbiol 47: 619–632. 12535065
64. McClure R, Balasubramanian D, Sun Y, Bobrovskyy M, Sumby P, Genco CA, Vanderpool CK, Tjaden B (2013) Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res 41: e140. doi: 10.1093/nar/gkt444 23716638
65. Katayama T, Kubota T, Kurokawa K, Crooke E, 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. 9674428
66. Waldminghaus T, Skarstad K (2010) ChIP on Chip: surprising results are often artifacts. BMC Genomics 11: 414. doi: 10.1186/1471-2164-11-414 20602746
67. Guyer MS, Reed RR, Steitz JA, Low KB (1981) Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp Quant Biol 45 Pt 1:135–40. 6271456
68. Jensen KF (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. 8501045
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