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Initiation of DNA Replication at the Chromosomal Origin of E. coli, oriC

  • Tsutomu KatayamaEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1042)

Abstract

The Escherichia coli chromosomal origin consists of a duplex-unwinding region and a region bearing a DNA-bending protein, IHF-binding site, and clusters of binding sites for the initiator protein DnaA. ATP-DnaA molecules form highly organized oligomers in a process stimulated by DiaA, a DnaA-binding protein. The resultant ATP-DnaA complexes promote local unwinding of oriC with the aid of IHF, for which specific interaction of DnaA with the single-stranded DNA is crucial. DnaA complexes also interact with DnaB helicases bound to DnaC loaders, promoting loading of DnaB onto the unwound DNA strands for bidirectional replication. Initiation of replication is strictly regulated during the cell cycle by multiple regulatory systems for oriC and DnaA. The activity of oriC is regulated by its methylation state, whereas that of DnaA depends on the form of the bound nucleotide. ATP-DnaA can be yielded from initiation-inactive ADP-DnaA in a timely manner depending on specific chromosomal DNA elements termed DARS (DnaA-reactivating sequences). After initiation, DnaA-bound ATP is hydrolyzed by two systems, yielding ADP-DnaA. In this review, these and other mechanisms of initiation and its regulation in E. coli are described.

Keywords

oriC DnaA IHF DiaA Hda DARS datA Methylation AAA+ In vitro reconstitution 

Notes

Acknowledgments

This work was supported by JSPS KAKENHI Grant Numbers 26291004, 16H00775, 17H03656, and 26650127. I apologize that many papers cannot be cited because of the limitation of space.

References

  1. Abe Y, Jo T, Matsuda Y, Matsunaga C, Katayama T, Ueda T (2007) Structure and function of DnaA N-terminal domains: specific sites and mechanisms in inter-DnaA interaction and in DnaB helicase loading on oriC. J Biol Chem 282:17816–17827PubMedCrossRefGoogle Scholar
  2. Aranovich A, Gdalevsky GY, Cohen-Luria R, Fishov I, Parola AH (2006) Membrane-catalyzed nucleotide exchange on DnaA: effect of surface molecular crowding. J Biol Chem 281:12526–12534PubMedCrossRefGoogle Scholar
  3. 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 206:51–59PubMedCrossRefGoogle Scholar
  4. Bates DB, Boye E, Asai T, Kogoma T (1987) The absence of effect of gid or mioC transcription on the initiation of chromosomal replication in Escherichia coli. Proc Natl Acad Sci USA 94:12497–12502CrossRefGoogle Scholar
  5. Baxter JC, Sutton MD (2012) Evidence for roles of the Escherichia coli Hda protein beyond regulatory inactivation of DnaA. Mol Microbiol 85:648–668PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bogan JA, Helmstetter CE (1997) DNA sequestration and transcription in the oriC region of Escherichia coli. Mol Microbiol 26:889–896PubMedCrossRefGoogle Scholar
  7. Cagliero C, Grand RS, Jones MB, Jin DJ, O’Sullivan JM (2013) Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription. Nucleic Acids Res 41:6058–6071PubMedPubMedCentralCrossRefGoogle Scholar
  8. Camara JE, Breier AM, Brendler T, Austin S, Cozzarelli NR, Crooke E (2005) Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6:736–741PubMedPubMedCentralCrossRefGoogle Scholar
  9. Charbon G, Bjørn L, Mendoza-Chamizo B, Frimodt-Møller J, Løbner-Olesen A (2014) Oxidative DNA damage is instrumental in hyperreplication stress-induced inviability of Escherichia coli. Nucleic Acids Res 42(21):13228–13241PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chodavarapu S, Felczak MM, Rouvière-Yaniv J, Kaguni JM (2008) Escherichia coli DnaA interacts with HU in initiation at the E. coli replication origin. Mol Microbiol 67:781–792PubMedCrossRefGoogle Scholar
  11. Chung YS1, Brendler T, Austin S, Guarné A (2009) Structural insights into the cooperative binding of SeqA to a tandem GATC repeat. Nucleic Acids Res 37:3143–3152PubMedPubMedCentralCrossRefGoogle Scholar
  12. Collier J, Shapiro L (2009) Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191:5706–5716PubMedPubMedCentralCrossRefGoogle Scholar
  13. Costa A, Hood IV, Berger JM (2013) Mechanisms for initiating cellular DNA replication. Annu Rev Biochem 82:25–54PubMedPubMedCentralCrossRefGoogle Scholar
  14. Crooke E, Castuma CE, Kornberg A (1992) The chromosome origin of Escherichia coli stabilizes DnaA protein during rejuvenation by phospholipids. J Biol Chem 267:16779–16782PubMedGoogle Scholar
  15. Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478:209–213PubMedPubMedCentralCrossRefGoogle Scholar
  16. Erzberger JP, Pirruccello MM, Berger JM (2002) The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J 21:4763–4773PubMedPubMedCentralCrossRefGoogle Scholar
  17. Erzberger JP, Mott ML, Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13:676–683PubMedCrossRefGoogle Scholar
  18. Felczak MM, Kaguni JM (2004) The box VII motif of Escherichia coli DnaA protein is required for DnaA oligomerization at the E. coli replication origin. J Biol Chem 279:51156–51162PubMedCrossRefGoogle Scholar
  19. Felczak MM, Simmons LA, Kaguni JM (2005) An essential tryptophan of Escherichia coli DnaA protein functions in oligomerization at the E. coli replication origin. J Biol Chem 280:24627–24633PubMedCrossRefGoogle Scholar
  20. Fernandez-Fernandez C, Gonzalez D, Collier J (2011) Regulation of the activity of the dual-function DnaA protein in Caulobacter crescentus. PLoS One 6:e26028PubMedPubMedCentralCrossRefGoogle Scholar
  21. Fingland N, Flåtten I, Downey CD, Fossum-Raunehaug S, Skarstad K, Crooke E (2012) Depletion of acidic phospholipids influences chromosomal replication in Escherichia coli. Microbiology 1:450–466Google Scholar
  22. Flåtten I, Fossum-Raunehaug S, Taipale R, Martinsen S, Skarstad K (2015) The DnaA protein is not the limiting factor for initiation of replication in Escherichia coli. PLoS Genet 11:e1005276PubMedPubMedCentralCrossRefGoogle Scholar
  23. Fossum-Raunehaug S, Helgesen E, Stokke C, Skarstad K (2014) Escherichia coli SeqA structures relocalize abruptly upon termination of origin sequestration during multifork DNA replication. PLoS One 9:e110575PubMedPubMedCentralCrossRefGoogle Scholar
  24. Frimodt-Møller J, Charbon G, Krogfelt KA, Løbner-Olesen A (2016) DNA replication control is linked to genomic positioning of control regions in Escherichia coli. PLoS Genet 12:e1006286PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fujikawa N, Kurumizaka H, Nureki O, Terada T, Shirouzu M, Katayama T, Yokoyama S (2003) Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res 31:2077–2086PubMedPubMedCentralCrossRefGoogle Scholar
  26. Fujikawa N, Kurumizaka H, Nureki O, Tanaka Y, Yamazoe M, Hiraga S, Yokoyama S (2004) Structural and biochemical analyses of hemimethylated DNA binding by the SeqA protein. Nucleic Acids Res 32:82–92PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fujimitsu K, Su’etsugu M, Yamaguchi Y, Mazda K, Fu N, Kawakami H, Katayama T (2008) Modes of overinitiation, dnaA gene expression, and inhibition of cell division in a novel cold-sensitive hda mutant of Escherichia coli. J Bacteriol 190:5368–5381PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fujimitsu K, Senriuchi T, Katayama T (2009) Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev 23:1221–1233PubMedPubMedCentralCrossRefGoogle Scholar
  29. Garner J, Crooke E (1996) Membrane regulation of the chromosomal replication activity of E. coli DnaA requires a discrete site on the protein. EMBO J 15:3477–3485PubMedPubMedCentralGoogle Scholar
  30. Grimwade JE, Ryan VT, Leonard AC (2000) IHF redistributes bound initiator protein, DnaA, on supercoiled oriC of Escherichia coli. Mol Microbiol 35:835–844PubMedCrossRefGoogle Scholar
  31. Guarné A, Brendler T, Zhao Q, Ghirlando R, Austin S, Yang W (2005) Crystal structure of a SeqA-N filament: implications for DNA replication and chromosome organization. EMBO J 24:1502–1511PubMedPubMedCentralCrossRefGoogle Scholar
  32. Helgesen E, Fossum-Raunehaug S, Sætre F, Schink KO, Skarstad K (2015) Dynamic Escherichia coli SeqA complexes organize the newly replicated DNA at a considerable distance from the replisome. Nucleic Acids Res 43:2730–2743PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hwang DS, Kornberg A (1992) Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem 267:23083–23086PubMedGoogle Scholar
  34. Inoue Y, Tanaka H, Kasho K, Fujimitsu K, Oshima T, Katayama T (2016) Chromosomal location of the DnaA-reactivating sequence DARS2 is important to regulate timely initiation of DNA replication in Escherichia coli. Genes Cells 21:1015–1023PubMedCrossRefGoogle Scholar
  35. Ishida T, Akimitsu N, Kashioka T, Hatano M, Kubota T, Ogata Y, Sekimizu K, Katayama T (2004) DiaA, a novel DnaA-binding protein, ensures the initiation timing of E. coli chromosome replication. J Biol Chem 279:45546–45555PubMedCrossRefGoogle Scholar
  36. Iyer LM, Leipe DD, Koonin EV, Aravind L (2004) Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 146:11–31PubMedCrossRefGoogle Scholar
  37. Jameson KH, Rostami N, Fogg MJ, Turkenburg JP, Grahl A, Murray H, Wilkinson AJ (2014) Structure and interactions of the Bacillus subtilis sporulation inhibitor of DNA replication, SirA, with domain I of DnaA. Mol Microbiol 93:975–991PubMedPubMedCentralCrossRefGoogle Scholar
  38. Kaguni JM (2011) Replication initiation at the Escherichia coli chromosomal origin. Curr Opin Chem Biol 15:606–613PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kang S, Lee H, Han JS, Hwang DS (1999) Interaction of SeqA and Dam methylase on the hemimethylated origin of Escherichia coli chromosomal DNA replication. J Biol Chem 274:11463–11468PubMedCrossRefGoogle Scholar
  40. Kang S, Han JS, Park JH, Skarstad K, Hwang DS (2003) SeqA protein stimulates the relaxing and decatenating activities of Topoisomerase IV. J Biol Chem 278:48779–48785PubMedCrossRefGoogle Scholar
  41. Kano Y, Imamoto F (1990) Requirement of integration host factor (IHF) for growth of Escherichia coli deficient in HU protein. Gene 89:133–137PubMedCrossRefGoogle Scholar
  42. Kasho K, Katayama T (2013) DnaA binding locus datA promotes ATP-DnaA hydrolysis to enable cell cycle-coordinated replication initiation. Proc Natl Acad Sci USA 110:936–941PubMedCrossRefGoogle Scholar
  43. Kasho K, Fujimitsu K, Matoba T, Oshima T, Katayama T (2014) Timely binding of IHF and Fis to DARS2 regulates ATP-DnaA production and replication initiation. Nucleic Acids Res 42:13134–13149PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kasho K, Tanaka H, Sakai R, Katayama T (2017) Cooperative DnaA binding to the negatively supercoiled locus stimulates DnaA-ATP hydrolysis. J Biol Chem 292:1251–1266PubMedCrossRefGoogle Scholar
  45. Katayama T (2008) Roles for the AAA+ motifs of DnaA in the initiation of DNA replication. Biochem Soc Trans 36:78–82PubMedCrossRefGoogle Scholar
  46. 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 94:61–71PubMedCrossRefGoogle Scholar
  47. Katayama T, Ozaki S, Keyamura K, Fujimitsu K (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8:163–170PubMedCrossRefGoogle Scholar
  48. Kato J, Katayama T (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20:4253–4262PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kawakami H, Keyamura K, Katayama T (2005) Formation of an ATP-DnaA-specific initiation complex requires DnaA Arginine 285, a conserved motif in the AAA+ protein family. J Biol Chem 280:27420–27430PubMedCrossRefGoogle Scholar
  50. Kawakami H, Ozaki S, Suzuki S, Nakamura K, Senriuchi T, Su’etsugu M, Fujimitsu K, Katayama T (2006) The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif. Mol Microbiol 62:1310–1324PubMedCrossRefGoogle Scholar
  51. Keyamura K, Katayama T (2011) DnaA protein DNA-binding domain binds to Hda protein to promote inter-AAA+ domain interaction involved in regulatory inactivation of DnaA. J Biol Chem 286:29336–29346PubMedPubMedCentralCrossRefGoogle Scholar
  52. Keyamura K, Fujikawa N, Ishida T, Ozaki S, Su’etsugu M, Fujimitsu K, Kagawa W, Yokoyama S, Kurumizaka H, Katayama T (2007) The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP-DnaA-specific initiation complexes. Genes Dev 21:2083–2099PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 284:25038–25050PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 12:3032–3043PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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 18:6642–6652PubMedPubMedCentralCrossRefGoogle Scholar
  56. Leonard AC, Grimwade JE (2015) The orisome: structure and function. Front Microbiol 6:545PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lu M, Campbell JL, Boye E, Kleckner N (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77:413–426PubMedCrossRefGoogle Scholar
  58. Marszalek J, Zhang W, Hupp TR, Margulies C, Carr KM, Cherry S, Kaguni JM (1996) Domains of DnaA protein involved in interaction with DnaB protein, and in unwinding the Escherichia coli chromosomal origin. J Biol Chem 271:18535–18542PubMedCrossRefGoogle Scholar
  59. 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 USA 101:2811–2816PubMedPubMedCentralCrossRefGoogle Scholar
  60. Miller DT, Grimwade JE, Betteridge T, Rozgaja T, Torgue JJ, Leonard AC (2009) Bacterial origin recognition complexes direct assembly of higher-order DnaA oligomeric structures. Proc Natl Acad Sci USA 106:18479–18484PubMedPubMedCentralCrossRefGoogle Scholar
  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 50:349–362PubMedCrossRefGoogle Scholar
  62. 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 187:3913–3920PubMedPubMedCentralCrossRefGoogle Scholar
  63. Natrajan G, Noirot-Gros MF, Zawilak-Pawlik A, Kapp U, Terradot L (2009) The structure of a DnaA/HobA complex from Helicobacter pylori provides insight into regulation of DNA replication in bacteria. Proc Natl Acad Sci U S A 106:21115–21120PubMedPubMedCentralCrossRefGoogle Scholar
  64. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43PubMedGoogle Scholar
  65. Nievera C, Torgue JJ, Grimwade JE, Leonard AC (2006) SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E coli pre-RC. Mol Cell 24:581–592PubMedPubMedCentralCrossRefGoogle Scholar
  66. Niki H, Yamaichi Y, Hiraga S (2000) Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14:212–223PubMedPubMedCentralGoogle Scholar
  67. Nishida S, Fujimitsu K, Sekimizu K, Ohmura T, Ueda T, 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 277:14986–14995PubMedCrossRefGoogle Scholar
  68. Noguchi Y, Katayama T (2016) The Escherichia coli cryptic prophage protein YfdR binds to DnaA and initiation of chromosomal replication is inhibited by overexpression of the gene cluster yfdQ-yfdR-yfdS-yfdT. Front Microbiol 7:239PubMedPubMedCentralCrossRefGoogle Scholar
  69. Noguchi Y, Sakiyama Y, Kawakami H, Katayama T (2015) The Arg fingers of key DnaA protomers are oriented inward within the replication origin oriC and stimulate DnaA subcomplexes in the initiation complex. J Biol Chem 290:20295–20312PubMedPubMedCentralCrossRefGoogle Scholar
  70. Noirot-Gros MF, Velten M, Yoshimura M, McGovern S, Morimoto T, Ehrlich SD, Ogasawara N, Polard P, Noirot P (2006) Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci USA 103:2368–2373PubMedPubMedCentralCrossRefGoogle Scholar
  71. Nozaki S, Ogawa T (2008) Determination of the minimum domain II size of Escherichia coli DnaA protein essential for cell viability. Microbiology 154:3379–3384PubMedCrossRefGoogle Scholar
  72. Nozaki S, Niki H, Ogawa T (2009a) Replication initiator DnaA of Escherichia coli changes its assembly form on the replication origin during the cell cycle. J Bacteriol 191:4807–4814PubMedPubMedCentralCrossRefGoogle Scholar
  73. Nozaki S, Yamada Y, Ogawa T (2009b) Initiator titration complex formed at datA with the aid of IHF regulates replication timing in Escherichia coli. Genes Cells 14:329–341PubMedCrossRefGoogle Scholar
  74. O’Donnell M, Langston L, Stillman B (2013) Principles and concepts of DNA replication in bacteria, archaea, and eukarya. Cold Spring Harb Perspect Biol 5:a010108PubMedPubMedCentralGoogle Scholar
  75. Obita T, Iwura T, Su’etsugu M, Yoshida Y, Tanaka Y, Katayama T, Ueda T, Imoto T (2002) Determination of the secondary structure in solution of the Escherichia coli DnaA DNA-binding domain. Biochem Biophys Res Commun 299:42–48PubMedCrossRefGoogle Scholar
  76. Odsbu I, Klungsoyr HK, Fossum S, Skarstad K (2005) Specific N-terminal interactions of the Escherichia coli SeqA protein are required to form multimers that restrain negative supercoils and form foci. Genes Cells 10:1039–1049PubMedCrossRefGoogle Scholar
  77. Ogawa T, Okazaki T (1994) Cell cycle-dependent transcription from the gid and mioC promoters of Escherichia coli. J Bacteriol 176:1609–1615PubMedPubMedCentralCrossRefGoogle Scholar
  78. Ogawa T, Yamada Y, Kuroda T, Kishi T, Moriya S (2002) The datA locus predominantly contributes to the initiator titration mechanism in the control of replication initiation in Escherichia coli. Mol Microbiol 44:1367–1375PubMedCrossRefGoogle Scholar
  79. Okumura H, Yoshimura M, Ueki M, Oshima T, Ogasawara N, Ishikawa S (2012) Regulation of chromosomal replication initiation by oriC proximal DnaA-box clusters in Bacillus subtilis. Nucleic Acids Res 40:220–234PubMedCrossRefGoogle Scholar
  80. Ozaki S, Katayama T (2009) DnaA structure, function, and dynamics in the initiation at the chromosomal origin. Plasmid 62:71–82PubMedCrossRefGoogle Scholar
  81. Ozaki S, Katayama T (2012) Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation. Nucleic Acids Res 40:1648–1665PubMedCrossRefGoogle Scholar
  82. Ozaki S, Kawakami H, Nakamura K, Fujikawa N, Kagawa W, Park SY, Yokoyama S, Kurumizaka H, Katayama T (2008) A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J Biol Chem 283:8351–8362PubMedCrossRefGoogle Scholar
  83. Ozaki S, Noguchi Y, Hayashi Y, Miyazaki E, Katayama T (2012a) Differentiation of the DnaA-oriC subcomplex for DNA unwinding in a replication initiation complex. J Biol Chem 287:37458–37471PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ozaki S, Noguchi Y, Nishimura M, Katayama T (2012b) Stable nucleotide binding to DnaA requires a specific glutamic acid residue within the AAA+ box II motif. J Struct Biol 179:242–250PubMedCrossRefGoogle Scholar
  85. Riber L, 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 187:5605–5613PubMedPubMedCentralCrossRefGoogle Scholar
  86. Riber L, Frimodt-Møller J, Charbon G, Løbner-Olesen A (2016) Multiple DNA binding proteins contribute to timing of chromosome replication in E. coli. Front Mol Biosci 3:29PubMedPubMedCentralCrossRefGoogle Scholar
  87. Richardson TT, Harran O, Murray H (2016) The bacterial DnaA-trio replication origin element specifies single-stranded DNA initiator binding. Nature 534:412–416PubMedPubMedCentralCrossRefGoogle Scholar
  88. Rozgaja TA, Grimwade JE, Iqbal M, Czerwonka C, Vora M, Leonard AC (2011) Two oppositely oriented arrays of low-affinity recognition sites in oriC guide progressive binding of DnaA during Escherichia coli pre-RC assembly. Mol Microbiol 82:475–488PubMedPubMedCentralCrossRefGoogle Scholar
  89. Samitt CE, Hansen FG, Miller JF, Schaechter M (1989) In vivo studies of DnaA binding to the origin of replication of Escherichia coli. EMBO J 8:989–993PubMedPubMedCentralGoogle Scholar
  90. Saxena R, Rozgaja T, Grimwade J, Crooke E (2011) Remodeling of nucleoprotein complexes is independent of the nucleotide state of a mutant AAA+ protein. J Biol Chem 286:33770–33777PubMedPubMedCentralCrossRefGoogle Scholar
  91. Saxena R, Fingland N, Patil D, Sharma AK, Crooke E (2013) Crosstalk between DnaA protein, the initiator of Escherichia coli chromosomal replication, and acidic phospholipids present in bacterial membranes. Int J Mol Sci 14:8517–8537PubMedPubMedCentralCrossRefGoogle Scholar
  92. Saxena R, Vasudevan S, Patil D, Ashoura N, Grimwade JE, Crooke E (2015) Nucleotide-induced conformational changes in Escherichia coli DnaA protein are required for bacterial ORC to pre-RC conversion at the chromosomal origin. Int J Mol Sci 16:27897–27911PubMedPubMedCentralCrossRefGoogle Scholar
  93. Scholefield G, Errington J, Murray H (2012) Soj/ParA stalls DNA replication by inhibiting helix formation of the initiator protein DnaA. EMBO J 31:1542–1555PubMedPubMedCentralCrossRefGoogle Scholar
  94. Seitz H, Weigel C, Messer W (2000) The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 37:1270–1279PubMedCrossRefGoogle Scholar
  95. Sekimizu K, Kornberg A (1988) Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem 263:7131–7135PubMedGoogle Scholar
  96. Sekimizu K, Yung BY, Kornberg A (1988) The dnaA protein of Escherichia coli. Abundance, improved purification, and membrane binding. J Biol Chem 263:7136–7140PubMedGoogle Scholar
  97. Shimizu M, Noguchi Y, Sakiyama Y, Kawakami H, Katayama T, Takada S (2016) Near-atomic structural model for bacterial DNA replication initiation complex and its functional insights. Proc Natl Acad Sci U S A 113:E8021–E8030PubMedPubMedCentralCrossRefGoogle Scholar
  98. Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5:a012922PubMedPubMedCentralCrossRefGoogle Scholar
  99. Slater S, Wold S, Lu M, Boye E, Skarstad K, Kleckner N (1995) E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82:927–936PubMedCrossRefGoogle Scholar
  100. Smulczyk-Krawczyszyn A, Jakimowicz D, Ruban-Osmialowska B, Zawilak-Pawlik A, Majka J, Chater K, Zakrzewska-Czerwinska J (2006) Cluster of DnaA boxes involved in regulation of Streptomyces chromosome replication: from in silico to in vivo studies. J Bacteriol 188:6184–6194PubMedPubMedCentralCrossRefGoogle Scholar
  101. Soufo CD, Soufo HJ, Noirot-Gros MF, Steindorf A, Noirot P, Graumann PL (2008) Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev Cell 15:935–941PubMedCrossRefGoogle Scholar
  102. Speck C, Weigel C, Messer W (1999) ATP- and ADP-DnaA protein, a molecular switch in gene regulation. EMBO J 18:6169–6176PubMedPubMedCentralCrossRefGoogle Scholar
  103. Stauffer ME, Chazin WJ (2004) Structural mechanisms of DNA replication, repair, and recombination. J Biol Chem 279:30915–30918PubMedCrossRefGoogle Scholar
  104. Su’etsugu M, Emoto A, Fujimitsu K, Keyamura K, Katayama T (2003) Transcriptional control for initiation of chromosomal replication in Escherichia coli: fluctuation of the level of origin transcription ensures timely initiation. Genes Cells 8:731–745PubMedCrossRefGoogle Scholar
  105. Su’etsugu M, Nakamura K, Keyamura K, Kudo Y, Katayama T (2008) Hda monomerization by ADP binding promotes replicase clamp mediated DnaA-ATP hydrolysis. J Biol Chem 283:36118–36131PubMedPubMedCentralCrossRefGoogle Scholar
  106. Su’etsugu M, Shimuta TR, Ishida T, Kawakami H, Katayama T (2005) Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J Biol Chem 280:6528–6536PubMedCrossRefGoogle Scholar
  107. Su’etsugu M, Harada Y, Keyamura K, Matsunaga C, Kasho K, Abe Y, Ueda T, Katayama T (2013) The DnaA N-terminal domain interacts with Hda to facilitate replicase clamp-mediated inactivation of DnaA. Environ Microbiol 15:3183–3195PubMedCrossRefGoogle Scholar
  108. Sutton MD, Carr KM, Vicente M, Kaguni JM (1998) Escherichia coli DnaA protein: the N-terminal domain and loading of DnaB helicase at the E. coli chromosomal origin. J Biol Chem 273:34255–34262PubMedCrossRefGoogle Scholar
  109. Theisen PW, Grimwade JE, Leonard AC, Bogan JA, Helmstetter CE (1993) Correlation of gene transcription with the time of initiation of chromosome replication in Escherichia coli. Mol Microbiol 10:575–584PubMedCrossRefGoogle Scholar
  110. Torheim NK, Skarstad K (1999) Escherichia coli SeqA protein affects DNA topology and inhibits open complex formation at oriC. EMBO J 18:4882–4888PubMedPubMedCentralCrossRefGoogle Scholar
  111. Valens M, Penaud S, Rossignol M, Cornet F, Boccard F (2004) Macrodomain organization of the Escherichia coli chromosome. EMBO J 23:4330–4341PubMedPubMedCentralCrossRefGoogle Scholar
  112. Waldminghaus T, Skarstad K (2009) The Escherichia coli SeqA protein. Plasmid 61:141–150PubMedCrossRefGoogle Scholar
  113. Wawrzycka A, Gross M, Wasaznik A, Konieczny I (2015) Plasmid replication initiator interactions with origin 13-mers and polymerase subunits contribute to strand-specific replisome assembly. Proc Natl Acad Sci USA 112:E4188–E4296PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wegrzyn K, Fuentes-Perez ME, Bury K, Rajewska M, Moreno-Herrero F, Konieczny I (2014) Sequence-specific interactions of Rep proteins with ssDNA in the AT-rich region of the plasmid replication origin. Nucleic Acids Res 42:7807–7818PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wolański M, Donczew R, Zawilak-Pawlik A, Zakrzewska-Czerwińska J (2015) oriC-encoded instructions for the initiation of bacterial chromosome replication. Front Microbiol 5:735PubMedPubMedCentralGoogle Scholar
  116. Yoshida Y, Obita T, Kokusho Y, Ohmura T, Katayama T, Ueda T, Imoto T (2003) Identification of the region in Escherichia coli DnaA protein required for specific recognition of the DnaA box. Cell Mol Life Sci 60:1998–2008PubMedCrossRefGoogle Scholar
  117. Yung BY, Kornberg A (1988) Membrane attachment activates dnaA protein, the initiation protein of chromosome replication in Escherichia coli. Proc Natl Acad Sci U S A 85:7202–7205PubMedPubMedCentralCrossRefGoogle Scholar
  118. Zawilak-Pawlik A, Kois A, Stingl K, Boneca IG, Skrobuk P, Piotr J, Lurz R, Zakrzewska-Czerwińska J, Labigne A (2007) HobA – a novel protein involved in initiation of chromosomal replication in Helicobacter pylori. Mol Microbiol 65:9799–9794CrossRefGoogle Scholar
  119. Zhang Q, Zhou A, Li S, Ni J, Tao J, Lu J, Wan B, Li S, Zhang J, Zhao S, Zhao GP, Shao F, Yao YF (2016) Reversible lysine acetylation is involved in DNA replication initiation by regulating activities of initiator DnaA in Escherichia coli. Sci Rep 6:30837PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Department of Molecular Biology, Graduate School of Pharmaceutical ScienceKyushu UniversityFukuokaJapan

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