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Replication Origin of E. coli and the Mechanism of Initiation

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Molecular Life Sciences

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Synopsis

The process of DNA replication can be formally divided into the stages of initiation, the elongation of nascent DNA, and termination. In E. coli, DNA replication initiates at a specific location (oriC) on the circular duplex chromosome. This site is where the replication fork machinery is assembled, leading to duplication of the E. coli chromosome. At oriC, specific biochemical events must take place in a step-wise manner in order to establish the enzymatic machinery that will operate at a replication fork. The first step involves the recognition of DNA sequence elements in oriC by the replication initiator (DnaA). Its interaction with these DNA sequences leads to the assembly of a DnaA oligomer that unwinds a region within oriC. DnaA then interacts with DnaB in a complex with DnaC to load the replicative DNA helicase (DnaB) onto the single-stranded DNA in the unwound region. After helicase loading and its activation, involving the binding of primase (DnaG) to DnaB and primer...

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References

  • Atkinson J, Gupta MK, McGlynn P (2011) Interaction of Rep and DnaB on DNA. Nucleic Acids Res 39(4):1351–1359

    Article  CAS  PubMed  Google Scholar 

  • Barcena M et al (2001) The DnaB.DnaC complex: a structure based on dimers assembled around an occluded channel. EMBO J 20(6):1462–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates DB et al (1995) The DnaA box R4 in the minimal oriC is dispensable for initiation of Escherichia coli chromosome replication. Nucleic Acids Res 23(16):3119–3125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell SP, Kaguni JM (2013) Helicase loading at chromosomal origins of replication. Cold Spring Harb Perspect Biol 5(6):pii:a010124

    Google Scholar 

  • Boye E et al (1993) Regulation of DNA replication in Escherichia coli. In: Fanning E, Knippers R, Winnacker EL (eds) DNA replication and the cell cycle, vol 43, Mosbacher Kolloquium. Springer, Berlin, pp 15–26

    Chapter  Google Scholar 

  • 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(5):743–755

    Article  CAS  PubMed  Google Scholar 

  • Brendler T, Austin S (1999) Binding of SeqA protein to DNA requires interaction between two or more complexes bound to separate hemimethylated GATC sequences. EMBO J 18(8):2304–2310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brendler T, Abeles A, Austin S (1995) A protein that binds to the P1 origin core and the oriC 13mer region in a methylation-specific fashion is the product of the host seqA gene. EMBO J 14(16):4083–4089

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carr KM, Kaguni JM (2001) Stoichiometry of DnaA and DnaB protein in initiation at the Escherichia coli chromosomal origin. J Biol Chem 276(48):44919–44925

    Article  CAS  PubMed  Google Scholar 

  • Cassler MR, Grimwade JE, Leonard AC (1995) Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J 14(23):5833–5841

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crooke E et al (1993) Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J Mol Biol 233(1):16–24

    Article  CAS  PubMed  Google Scholar 

  • Davey MJ et al (2002) The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J 21(12):3148–3159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duderstadt KE et al (2010) Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J Biol Chem 285(36):28229–28239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478(7368):209–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erzberger JP, Pirruccello MM, Berger JM (2002) The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J 21(18):4763–4773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erzberger JP, Mott ML, Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13(8):676–683

    Article  CAS  PubMed  Google Scholar 

  • Fang L, Davey MJ, O’Donnell M (1999) Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin. Mol Cell 4(4):541–553

    Article  CAS  PubMed  Google Scholar 

  • 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(26):24627–24633

    Article  CAS  PubMed  Google Scholar 

  • Finkel SE, Johnson RC (1992) The Fis protein: it’s not just for DNA inversion anymore [published erratum appears in Mol Microbiol 1993 Mar;7(2):1023]. Mol Microbiol 6(22):3257–3265

    Google Scholar 

  • Flamm EL, Weisberg RA (1985) Primary structure of the hip gene of Escherichia coli and of its product, the beta subunit of integration host factor. J Mol Biol 183(2):117–128

    Article  CAS  PubMed  Google Scholar 

  • 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(3):889–900

    Article  CAS  PubMed  Google Scholar 

  • Galletto R, Jezewska MJ, Bujalowski W (2003) Interactions of the Escherichia coli DnaB helicase hexamer with the replication factor the DnaC protein. Effect of nucleotide cofactors and the ssDNA on protein-protein interactions and the topology of the complex. J Mol Biol 329(3):441–465

    Article  CAS  PubMed  Google Scholar 

  • Gille H, Messer W (1991) Localized DNA melting and structural pertubations in the origin of replication, oriC, of Escherichia coli in vitro and in vivo. EMBO J 10(6):1579–1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gille H et al (1991) The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli. Nucleic Acids Res 19(15):4167–4172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimwade JE, Ryan VT, Leonard AC (2000) IHF redistributes bound initiator protein, DnaA, on supercoiled oriC of Escherichia coli. Mol Microbiol 35(4):835–844

    Article  CAS  PubMed  Google Scholar 

  • Hiasa H, Marians KJ (1994) Fis cannot support oriC DNA replication in vitro. J Biol Chem 269(40):24999–25003

    CAS  PubMed  Google Scholar 

  • Hupert-Kocurek K et al (2007) Genetic method to analyze essential genes of Escherichia coli. Appl Environ Microbiol 73(21):7075–7082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(32):23083–23086

    CAS  PubMed  Google Scholar 

  • Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356

    Article  CAS  PubMed  Google Scholar 

  • Jacob F, Brenner S, Cuzin F (1963) On the regulation of DNA replication in bacteria. Cold Spring Harb Symp Quant Biol 28:329–348

    Article  CAS  Google Scholar 

  • Kano Y, Imamoto F (1990) Requirement of integration host factor (IHF) for growth of Escherichia coli deficient in HU protein. Gene 89(1):133–137

    Article  CAS  PubMed  Google Scholar 

  • Kaur G et al (2014) Building the bacterial orisome: high-affinity DnaA recognition plays a role in setting the conformation of oriC DNA. Mol Microbiol 91(6):1148–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(29):27420–27430

    Article  CAS  PubMed  Google Scholar 

  • Keyamura K et al (2009) DiaA dynamics are coupled with changes in initial origin complexes leading to helicase loading. J Biol Chem 284(37):25038–25050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S et al (1996) Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement. Cell 84(4):643–650

    Article  CAS  PubMed  Google Scholar 

  • Langer U et al (1996) A comprehensive set of DnaA-box mutations in the replication origin, oriC, of Escherichia coli. Mol Microbiol 21(2):301–311

    Article  CAS  PubMed  Google Scholar 

  • Leonard AC, Grimwade JE (2011) Regulation of DnaA assembly and activity: taking directions from the genome. Annu Rev Microbiol 65:19–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludlam AV et al (2001) Essential amino acids of Escherichia coli DnaC protein in an N-terminal domain interact with DnaB helicase. J Biol Chem 276(29):27345–27353

    Article  CAS  PubMed  Google Scholar 

  • Makowska-Grzyska M, Kaguni JM (2010) Primase directs the release of DnaC from DnaB. Mol Cell 37(1):90–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margulies C, Kaguni JM (1996) Ordered and sequential binding of DnaA protein to oriC, the chromosomal origin of Escherichia coli. J Biol Chem 271(29):17035–17040

    Article  CAS  PubMed  Google Scholar 

  • Margulies C, Kaguni JM (1998) The FIS protein fails to block the binding of DnaA protein to oriC, the Escherichia coli chromosomal origin. Nucleic Acids Res 26(22):5170–5175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marszalek J, Kaguni JM (1994) DnaA protein directs the binding of DnaB protein in initiation of DNA replication in Escherichia coli. J Biol Chem 269(7):4883–4890

    CAS  PubMed  Google Scholar 

  • Matsui M et al (1985) Sites of dnaA protein-binding in the replication origin of the Escherichia coli K-12 chromosome. J Mol Biol 184(3):529–533

    Article  CAS  PubMed  Google Scholar 

  • McGarry KC et al (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(9):2811–2816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messer W et al (1992) The complex for replication initiation of Escherichia coli. Chromosoma 102(1 Suppl):S1–S6

    Article  CAS  PubMed  Google Scholar 

  • Mitkova AV, Khopde SM, Biswas SB (2003) Mechanism and stoichiometry of interaction of DnaG primase with DnaB helicase of Escherichia coli in RNA primer synthesis. J Biol Chem 278(52):52253–52261

    Article  CAS  PubMed  Google Scholar 

  • Mott ML et al (2008) Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 135(4):623–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oka A et al (1980) Replication origin of the Escherichia coli K-12 chromosome: the size and structure of the minimum DNA segment carrying the information for autonomous replication. Mol Gen Genet 178(1):9–20

    Article  CAS  PubMed  Google Scholar 

  • Ozaki S, Katayama T (2012) Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation. Nucleic Acids Res 40(4):1648–1665

    Google Scholar 

  • Ozaki S et al (2008) A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J Biol Chem 283(13):8351–8362

    Article  CAS  PubMed  Google Scholar 

  • Polaczek P (1990) Bending of the origin of replication of E. coli by binding of IHF at a specific site. New Biol 2(3):265–271

    CAS  PubMed  Google Scholar 

  • Rice PA et al (1996) Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87(7):1295–1306

    Article  CAS  PubMed  Google Scholar 

  • Rozgaja TA et al (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(2):475–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan VT et al (2002) IHF and HU stimulate assembly of pre-replication complexes at Escherichia coli oriC by two different mechanisms. Mol Microbiol 46(1):113–124

    Article  CAS  PubMed  Google Scholar 

  • Schaper S, Messer W (1995) Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J Biol Chem 270(29):17622–17626

    Article  CAS  PubMed  Google Scholar 

  • Seitz H, Weigel C, Messer W (2000) The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 37(5):1270–1279

    Article  CAS  PubMed  Google Scholar 

  • 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(2):259–265

    Article  CAS  PubMed  Google Scholar 

  • Slater S et al (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(6):927–936

    Article  CAS  PubMed  Google Scholar 

  • Speck C, Messer W (2001) Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J 20(6):1469–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stepankiw N et al (2009) The right half of the Escherichia coli replication origin is not essential for viability, but facilitates multi-forked replication. Mol Microbiol 74(2):467–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutton MD et al (1998) E. coli DnaA protein: the N-terminal domain and loading of DnaB helicase at the E. coli chromosomal origin. J Biol Chem 273:34255–34262

    Article  CAS  PubMed  Google Scholar 

  • von Meyenburg K, Hansen FG (1980) The origin of replication, oriC, of the Escherichia coli chromosome: genes near oriC and construction of oriC deletion mutations. ICN-UCLA Symp Mol Cell Biol 19:137–159

    Google Scholar 

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Acknowledgments

I thank the members of my lab for their support while I wrote. This work is supported by Grant GM090063 from the National Institutes of Health and by the Michigan Agricultural Experiment Station.

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Michigan State University, 322 Biochemistry Building, 48823, East Lansing, MI, USA

    Jon M. Kaguni

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  1. Jon M. Kaguni
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Correspondence to Jon M. Kaguni .

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Editors and Affiliations

  1. Texas A&M University, College Station, TX, USA

    Robert D. Wells

  2. Penn State College of Medicine, Hershey, PA, USA

    Judith S. Bond

  3. University of California, Berkeley, CA, USA

    Judith Klinman

  4. University of Texas Health Science Center, San Antonio, TX, USA

    Bettie Sue Siler Masters

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Kaguni, J.M. (2018). Replication Origin of E. coli and the Mechanism of Initiation. In: Wells, R.D., Bond, J.S., Klinman, J., Masters, B.S.S. (eds) Molecular Life Sciences. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1531-2_56

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