Termination of DNA Replication in Prokaryotes

Abstract

Most bacteria and archaea have circular chromosomes, in which DNA replication begins at a site known as an origin of replication. Double‐stranded DNA unwound at the origin creates two replication forks that are engaged by DNA polymerase complexes (replisomes) that advance each fork and proceed in opposite directions away from the origin, copying the original strands. Termination of DNA replication occurs when the two forks meet and fuse, creating two separate double‐stranded DNA molecules. In the well‐studied bacteria Escherichia coli and Bacillus subtilis, this occurs in the terminus region, which is situated diametrically opposite the origin. Failure to terminate chromosome replication correctly can lead to problems with genome function and stability, including DNA over‐replication. In contrast, some archaea have multi‐origin chromosomes and do not appear to specifically regulate the location of termination.

Key Concepts

  • Termination of DNA replication occurs when two oppositely orientated replication forks meet and fuse, to create two separate and complete double‐stranded DNA molecules.
  • In circular bacterial chromosomes, termination is restricted to a region called the terminus region, located approximately opposite the origin of replication.
  • A replication fork trap is an opposing arrangement of unidirectional replication terminator (Ter) sites in a region of DNA, which allows replication forks to enter the trap from either direction, but not exit it.
  • Failure to terminate bacterial chromosome replication correctly results in chromosome over‐replication and genome instability.
  • Terminator proteins bind to asymmetric DNA Ter sites to arrest a replication fork approaching the non‐permissive side but allow fork passage from permissive side.

Keywords: DNA replication; replication termination; replication fork arrest; DNA terminators; replication terminator protein; termination utilisation substance; catenanes

Figure 1. Arrangement ofDNAreplication terminators in the circular chromosomes of (a)Escherichia coliand (c)Bacillus subtilis. The two replication forks generated at the origin (oriC) move in opposite directions along the DNA and eventually approach one other and fuse within the terminus region diametrically opposed to oriC. The terminus region constitutes a replication fork trap in which the DNA terminators (denoted Ter) are arranged as two opposed groups, with the red terminators oriented to block movement of the clockwise replication fork and the blue terminators oriented to block the anticlockwise fork. Letters and Roman numbers define Ter sites (A indicates the location of TerA in E. coli; I indicates the location of TerI in B. subtilis). The STer region of the B. subtilis chromosome contains additional terminator sites used only during the stringent response. The chromosomal locations for the origin, the dif chromosome dimer resolution site and the genes for the terminator proteins, Tus (terminus utilisation substance) in E. coli and RTP (replication terminator protein) in B. subtilis, are marked. The location of rrn operons, which are highly transcribed particularly under fast growth conditions, are shown by green arrows, with the arrow pointing in the direction in which transcribing RNA polymerase molecules travel. (b) & (d) show consensus sequences for the E. coli Ter core sequence and the B. subtilis terminators. For B. subtilis the overlapping A and B sites are indicated.
Figure 2. Crystal structures of Terminator protein‐DNAcomplexes. (a) Two crystal structures of the Tus–Ter complex of E. coli indicating the blocking and permissive ends of the complex (left, PDB 2i05), and in the ‘locked’ conformation with DNA unwound at the blocking end and the C6 base of Ter DNA bound to its specific binding pocket in Tus (right, PDB 2i06), which contributes significantly to the fork arrest activity of the complex. (b) Crystal structure of an RTP dimer in complex with the high‐affinity half of TerI (the B site) (PDB 2efw). RTP can form a symmetric dimer in solution and recognises the partial DNA sequence symmetry in each half‐site that makes up each functional Ter site in B. subtilis. However, the partial asymmetry of each half‐site causes the RTP monomers to adopt somewhat different conformations in the half‐site complex (‘wing‐up’ conformation, on the left‐hand monomer, and ‘wing‐down’ conformation on the right‐hand monomer as viewed), and this might play a specific role in establishing cooperativity of binding to the second low‐affinity half‐site (the A site), and optimising contact with the oncoming replisome for its arrest. The cooperative binding of two dimers to each Ter site is essential for fork arrest activity. In the full complex, forks would be arrested when approaching from the right in the image shown. The structural basis for cooperative binding and how the whole complex interacts with the replisome are unknown features of interest.
Figure 3. Chromosome replication and cell growth in cells with one or two replication origins in the presence and absence of a replication fork trap. (a) In the presence of a block to one replication fork on its way from oriC to the termination area the chromosome will remain under‐replicated, as the second fork will be blocked by the Ter/Tus complexes in the termination area. (b) Schematic representation of the replichore arrangement of an E. coli chromosome with an ectopic replication origin termed oriZ in the presence of a functional replication fork trap. oriZ indicates the integration of a duplication of the oriC sequence near the lacZYA operon (Wang et al., ). Directionality of replication and fork fusion locations are indicated by green arrows. (c) Replichore parameters in the termination area of E. coli cells with two replication origins in the absence of a functional replication fork trap (Δtus). If forks escaping the termination area proceed with a speed similar to forks coming from oriC, then the fusion point should be in the location indicated by the blue arrows. If forks escaping the termination area are slowed by an increased number of replication–transcription conflicts, then forks should fuse closer to the termination area, as indicated by the grey arrows. The experimental observation is, however, that the fork fusion point is located closer to oriC (green arrows), indicating that forks escaping the termination area potentially encounter fewer problems than forks coming from oriC (Ivanova et al., ). (d) Schematic representation of the replichore arrangement of an E. coli chromosome replicating exclusively from an ectopic replication origin in the presence (d i) and absence (d ii) of a functional replication fork trap. Directionality of replication and approximate fork fusion locations are indicated by green and blue arrows in the presence and absence of a functional fork trap (Δtus), respectively.
Figure 4. Over‐replication in the termination area in the absence ofRecGhelicase (a) Replication profiles of E. coli cells in exponential phase. The number of reads (normalised against the reads for a stationary wild‐type control) is plotted against the chromosomal coordinate. Positions of oriC (green line) and primary Ter sites are shown above the plotted data with red and blue lines representing the left and right replichore as depicted in a. The termination area between the innermost Ter sites is highlighted in light blue. (b) Growth of a ΔrecG Δtus rpo* strain in which the entire oriC region is deleted. (c) Marker frequency analysis of a ΔrecG Δtus rpo* strain that carries a temperature‐sensitive allele of the main replication initiator protein DnaA. The strain was grown at 42 °C to inactivate DnaA(ts) and therefore prevent n from being active. (d) Marker frequency analysis of chromosome replication in a double origin strain in the presence and absence of RecG. Strains were grown at 37 °C. Reproduced with permission from Rudolph et al. 2013. © Nature.
Figure 5. Schematic illustrating how replication fork fusions might trigger over‐replication in the termination area and how this is normally prevented by proteins such as RecG and/or 3′ exonucleases. Note that the formation of a 3′ flap can occur at both forks. However, for simplicity, the schematic shows only one such reaction. See text for further details.
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References

Ahn KS , Malo MS , Smith MT and Wake RG (1993) Autoregulation of the gene encoding the replication terminator protein of Bacillus subtilis . Gene 132: 7–13.

Alexander JL and Orr‐Weaver TL (2016) Replication fork instability and the consequences of fork collisions from rereplication. Genes & Development 30: 2241–2252.

Andersen PA , Griffiths AA , Duggin IG and Wake RG (2000) Functional specificity of the replication fork‐arrest complexes of Bacillus subtilis and Escherichia coli: significant specificity for Tus‐Ter functioning in E. coli . Molecular Microbiology 36: 1327–1335.

Aussel L , Barre FX , Aroyo M , et al. (2002) FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108: 195–205.

Autret S , Levine A , Vannier F , Fujita Y and Seror SJ (1999) The replication checkpoint control in Bacillus subtilis: identification of a novel RTP‐binding sequence essential for the replication fork arrest after induction of the stringent response. Molecular Microbiology 31: 1665–1679.

Barre FX , Soballe B , Michel B , et al. (2001) Circles: the replication‐recombination‐chromosome segregation connection. Proceedings of the National Academy of Sciences of the United States of America 98: 8189–8195.

Bastia D , Zzaman S , Krings G , et al. (2008) Replication termination mechanism as revealed by Tus‐mediated polar arrest of a sliding helicase. Proceedings of the National Academy of Sciences of the United States of America 105: 12831–12836.

Beattie TR and Reyes‐Lamothe R (2015) A Replisome's journey through the bacterial chromosome. Frontiers in Microbiology 6: 562.

Bedrosian CL and Bastia D (1991) Escherichia coli replication terminator protein impedes simian virus 40 (SV40) DNA replication fork movement and SV40 large tumor antigen helicase activity in vitro at a prokaryotic terminus sequence. Proceedings of the National Academy of Sciences of the United States of America 88: 2618–2622.

Berghuis BA , Dulin D , Xu ZQ , et al. (2015) Strand separation establishes a sustained lock at the Tus‐Ter replication fork barrier. Nature Chemical Biology 11: 579–585.

Bianco PR (2015) I came to a fork in the DNA and there was RecG. Progress in Biophysics and Molecular Biology 117: 166–173.

Bidnenko V , Ehrlich SD and Michel B (2002) Replication fork collapse at replication terminator sequences. The EMBO Journal 21: 3898–3907.

Bigot S , Saleh OA , Lesterlin C , et al. (2005) KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. The EMBO Journal 24: 3770–3780.

Biller SJ and Burkholder WF (2009) The Bacillus subtilis SftA (YtpS) and SpoIIIE DNA translocases play distinct roles in growing cells to ensure faithful chromosome partitioning. Molecular Microbiology 74: 790–809.

Blow JJ and Gillespie PJ (2008) Replication licensing and cancer–a fatal entanglement? Nature Reviews. Cancer 8: 799–806.

Boubakri H , de Septenville AL , Viguera E and Michel B (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. The EMBO Journal 29: 145–157.

Bouche JP , Gelugne JP , Louarn J , Louarn JM and Kaiser K (1982) Relationships between the physical and genetic maps of a 470 x 10(3) base‐pair region around the terminus of Escherichia coli K12 DNA replication. Journal of Molecular Biology 154: 21–32.

Brewer BJ (1988) When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53: 679–686.

Bussiere DE , Bastia D and White SW (1995) Crystal structure of the replication terminator protein from B. subtilis at 2.6 A. Cell 80: 651–660.

Cortez D , Quevillon‐Cheruel S , Gribaldo S , et al. (2010) Evidence for a Xer/dif system for chromosome resolution in archaea. PLoS Genetics 6: e1001166.

Coskun‐Ari FF and Hill TM (1997) Sequence‐specific interactions in the Tus‐Ter complex and the effect of base pair substitutions on arrest of DNA replication in Escherichia coli . The Journal of Biological Chemistry 272: 26448–26456.

Cox MM (2001) Historical overview: searching for replication help in all of the rec places. Proceedings of the National Academy of Sciences of the United States of America 98: 8173–8180.

De Septenville AL , Duigou S , Boubakri H and Michel B (2012) Replication fork reversal after replication‐transcription collision. PLoS Genetics 8: e1002622.

Dimude JU , Stockum A , Midgley‐Smith SL , et al. (2015) The consequences of replicating in the wrong orientation: bacterial chromosome duplication without an active replication origin. MBio 6: e01294–e01315.

Dimude JU , Midgley‐Smith SL , Stein M and Rudolph CJ (2016) Replication termination: containing fork fusion‐mediated pathologies in Escherichia coli . Genes (Basel) 7: 40.

Dimude JU , Stein M , Andrzejewska EE , et al. (2018) Origins left, right, and centre: increasing the number of initiation sites in the Escherichia coli chromosome. Genes (Basel) 9.

Duggin IG , Andersen PA , Smith MT , et al. (1999) Site‐directed mutants of RTP of Bacillus subtilis and the mechanism of replication fork arrest. Journal of Molecular Biology 286: 1325–1335.

Duggin IG , Matthews JM , Dixon NE , Wake RG and Mackay JP (2005) A complex mechanism determines polarity of DNA replication fork arrest by the replication terminator complex of Bacillus subtilis . The Journal of Biological Chemistry 280: 13105–13113.

Duggin IG (2006) DNA replication fork arrest by the Bacillus subtilis RTP‐DNA complex involves a mechanism that is independent of the affinity of RTP‐DNA binding. Journal of Molecular Biology 361: 1–6.

Duggin IG , Wake RG , Bell SD and Hill TM (2008) The replication fork trap and termination of chromosome replication. Molecular Microbiology 70: 1323–1333.

Duggin IG and Bell SD (2009) Termination structures in the Escherichia coli chromosome replication fork trap. Journal of Molecular Biology 387: 532–539.

Duggin IG , Dubarry N and Bell SD (2011) Replication termination and chromosome dimer resolution in the archaeon Sulfolobus solfataricus . The EMBO Journal 30: 145–153.

Elshenawy MM , Jergic S , Xu ZQ , et al. (2015) Replisome speed determines the efficiency of the Tus‐Ter replication termination barrier. Nature 525: 394–398.

Espeli O , Levine C , Hassing H and Marians KJ (2003) Temporal regulation of topoisomerase IV activity in E. coli . Molecular Cell 11: 189–201.

Ferullo DJ and Lovett ST (2008) The Stringent Response and Cell Cycle Arrest in Escherichia coli . PLoS Genetics 4 (12): e1000300. DOI: 10.1371/journal.pgen.1000300

Finkel T , Serrano M and Blasco MA (2007) The common biology of cancer and ageing. Nature 448: 767–774.

Gabbai CB and Marians KJ (2010) Recruitment to stalled replication forks of the PriA DNA helicase and replisome‐loading activities is essential for survival. DNA Repair (Amst) 9: 202–209.

Gambus A (2017) Termination of eukaryotic replication forks. Advances in Experimental Medicine and Biology 1042: 163–187.

Gao F and Zhang CT (2008) Ori‐Finder: a web‐based system for finding oriCs in unannotated bacterial genomes. BMC Bioinformatics 9: 79.

Gao F (2015) Bacteria may have multiple replication origins. Frontiers in Microbiology 6: 324.

Gautam A and Bastia D (2001) A replication terminus located at or near a replication checkpoint of Bacillus subtilis functions independently of stringent control. The Journal of Biological Chemistry 276: 8771–8777.

Grainge I , Lesterlin C and Sherratt DJ (2011) Activation of XerCD‐dif recombination by the FtsK DNA translocase. Nucleic Acids Research 39: 5140–5148.

Grainge I (2013) Simple topology: FtsK‐directed recombination at the dif site. Biochemical Society Transactions 41: 595–600.

Griffiths AA , Andersen PA and Wake RG (1998) Replication terminator protein‐based replication fork‐arrest systems in various Bacillus species. Journal of Bacteriology 180: 3360–3367.

Griffiths AA and Wake RG (2000) Utilization of subsidiary chromosomal replication terminators in Bacillus subtilis . Journal of Bacteriology 182: 1448–1451.

Gupta MK , Guy CP , Yeeles JT , et al. (2013) Protein‐DNA complexes are the primary sources of replication fork pausing in Escherichia coli . Proceedings of the National Academy of Sciences of the United States of America 110: 7252–7257.

Guy CP , Atkinson J , Gupta MK , et al. (2009) Rep provides a second motor at the replisome to promote duplication of protein‐bound DNA. Molecular Cell 36: 654–666.

Hawkins M , Malla S , Blythe MJ , Nieduszynski CA and Allers T (2013) Accelerated growth in the absence of DNA replication origins. Nature 503: 544–547.

Helmstetter C , Cooper S , Pierucci O and Revelas E (1968) On the bacterial life sequence. Cold Spring Harbor Symposia on Quantitative Biology 33: 809–822.

Henderson TA , Nilles AF , Valjavec‐Gratian M and Hill TM (2001) Site‐directed mutagenesis and phylogenetic comparisons of the Escherichia coli Tus protein: DNA‐protein interactions alone can not account for Tus activity. Molecular Genetics and Genomics 265: 941–953.

Hiasa H and Marians KJ (1994) Tus prevents overreplication of oriC plasmid DNA. The Journal of Biological Chemistry 269: 26959–26968.

Hidaka M , Kobayashi T , Ishimi Y , et al. (1992) Termination complex in Escherichia coli inhibits SV40 DNA replication in vitro by impeding the action of T antigen helicase. The Journal of Biological Chemistry 267: 5361–5365.

Hidaka M , Akiyama M and Horiuchi T (1988) A consensus sequence of three DNA replication terminus sites on the E. coli chromosome is highly homologous to the terR sites of the R6K plasmid. Cell 55: 467–475.

Hill TM , Tecklenburg ML , Pelletier AJ and Kuempel PL (1989) tus, the trans‐acting gene required for termination of DNA replication in Escherichia coli, encodes a DNA‐binding protein. Proceedings of the National Academy of Sciences of the United States of America 86: 1593–1597.

Hojgaard A , Szerlong H , Tabor C and Kuempel P (1999) Norfloxacin‐induced DNA cleavage occurs at the dif resolvase locus in Escherichia coli and is the result of interaction with topoisomerase IV. Molecular Microbiology 33: 1027–1036.

Hong X , Cadwell GW and Kogoma T (1995) Escherichia coli RecG and RecA proteins in R‐loop formation. The EMBO Journal 14: 2385–2392.

Ivanova D , Taylor T , Smith SL , et al. (2015) Shaping the landscape of the Escherichia coli chromosome: replication‐transcription encounters in cells with an ectopic replication origin. Nucleic Acids Research 43: 7865–7877.

Jameson KH and Wilkinson AJ (2017) Control of initiation of DNA replication in Bacillus subtilis and Escherichia coli . Genes (Basel) 8: E22.

Jin DJ , Cagliero C and Zhou YN (2012) Growth rate regulation in Escherichia coli . FEMS Microbiology Reviews 36: 269–287.

Kaimer C , Gonzalez‐Pastor JE and Graumann PL (2009) SpoIIIE and a novel type of DNA translocase, SftA, couple chromosome segregation with cell division in Bacillus subtilis . Molecular Microbiology 74: 810–825.

Kaimer C , Schenk K and Graumann PL (2011) Two DNA translocases synergistically affect chromosome dimer resolution in Bacillus subtilis . Journal of Bacteriology 193: 1334–1340.

Kamada K , Horiuchi T , Ohsumi K , Shimamoto N and Morikawa K (1996a) Structure of a replication‐terminator protein complexed with DNA. Nature 383: 598–603.

Kamada K , Ohsumi K , Horiuchi T , Shimamoto N and Morikawa K (1996b) Crystallization and preliminary X‐ray analysis of the Escherichia coli replication terminator protein complexed with DNA. Proteins 24: 402–403.

Kim N and Jinks‐Robertson S (2012) Transcription as a source of genome instability. Nature Reviews. Genetics 13: 204–214.

Krabbe M , Zabielski J , Bernander R and Nordstrom K (1997) Inactivation of the replication‐termination system affects the replication mode and causes unstable maintenance of plasmid R1. Molecular Microbiology 24: 723–735.

Kralicek AV , Vesper NA , Ralston GB , Wake RG and King GF (1993) Symmetry and secondary structure of the replication terminator protein of Bacillus subtilis: sedimentation equilibrium and circular dichroic, infrared, and NMR spectroscopic studies. Biochemistry 32: 10216–10223.

Kralicek AV , Wilson PK , Ralston GB , Wake RG and King GF (1997) Reorganization of terminator DNA upon binding replication terminator protein: implications for the functional replication fork arrest complex. Nucleic Acids Research 25: 590–596.

Kreuzer KN and Cozzarelli NR (1979) Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. Journal of Bacteriology 140: 424–435.

Kuempel PL , Henson JM , Dircks L , Tecklenburg M and Lim DF (1991) dif, a recA‐independent recombination site in the terminus region of the chromosome of Escherichia coli . The New Biologist 3: 799–811.

Kurth I and O'Donnell M (2009) Replisome dynamics during chromosome duplication. EcoSal Plus 3.

Langley DB , Smith MT , Lewis PJ and Wake RG (1993) Protein‐nucleoside contacts in the interaction between the replication terminator protein of Bacillus subtilis and the DNA terminator. Molecular Microbiology 10: 771–779.

Larsen NB , Hickson ID and Mankouri HW (2014) Tus‐Ter as a tool to study site‐specific DNA replication perturbation in eukaryotes. Cell Cycle 13: 2994–2998.

Lau IF , Filipe SR , Soballe B , et al. (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Molecular Microbiology 49: 731–743.

Lee EH , Kornberg A , Hidaka M , Kobayashi T and Horiuchi T (1989) Escherichia coli replication termination protein impedes the action of helicases. Proceedings of the National Academy of Sciences of the United States of America 86: 9104–9108.

Lee EH and Kornberg A (1992) Features of replication fork blockage by the Escherichia coli terminus‐binding protein. The Journal of Biological Chemistry 267: 8778–8784.

Lemon KP , Kurtser I and Grossman AD (2001) Effects of replication termination mutants on chromosome partitioning in Bacillus subtilis . Proceedings of the National Academy of Sciences of the United States of America 98: 212–217.

Lesterlin C , Barre FX and Cornet F (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Molecular Microbiology 54: 1151–1160.

Lewis PJ , Ralston GB , Christopherson RI and Wake RG (1990) Identification of the replication terminator protein binding sites in the terminus region of the Bacillus subtilis chromosome and stoichiometry of the binding. Journal of Molecular Biology 214: 73–84.

Lloyd RG and Rudolph CJ (2016) 25 years on and no end in sight: a perspective on the role of RecG protein. Current Genetics 62: 827–840.

Maduike NZ , Tehranchi AK , Wang JD and Kreuzer KN (2014) Replication of the Escherichia coli chromosome in RNase HI‐deficient cells: multiple initiation regions and fork dynamics. Molecular Microbiology 91: 39–56.

Manna AC , Pai KS , Bussiere DE , et al. (1996) Helicase‐contrahelicase interaction and the mechanism of termination of DNA replication. Cell 87: 881–891.

Marians KJ , Hiasa H , Kim DR and McHenry CS (1998) Role of the core DNA polymerase III subunits at the replication fork. Alpha is the only subunit required for processive replication. The Journal of Biological Chemistry 273: 2452–2457.

Markovitz A (2005) A new in vivo termination function for DNA polymerase I of Escherichia coli K12. Molecular Microbiology 55: 1867–1882.

Matzke AJ , Huettel B , van der Winden J and Matzke M (2005) Use of two‐color fluorescence‐tagged transgenes to study interphase chromosomes in living plants. Plant Physiology 139: 1586–1596.

McGlynn P , Lloyd RG and Marians KJ (2001) Formation of Holliday junctions by regression of nascent DNA in intermediates containing stalled replication forks: RecG stimulates regression even when the DNA is negatively supercoiled. Proceedings of the National Academy of Sciences of the United States of America 98: 8235–8240.

McGlynn P and Guy CP (2008) Replication forks blocked by protein‐DNA complexes have limited stability in vitro. Journal of Molecular Biology 381: 249–255.

McGlynn P , Savery NJ and Dillingham MS (2012) The conflict between DNA replication and transcription. Molecular Microbiology 85: 12–20.

McLean MJ , Wolfe KH and Devine KM (1998) Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. Journal of Molecular Evolution 47: 691–696.

Meijer WJ , Smith M , Wake RG , et al. (1996) Identification and characterization of a novel type of replication terminator with bidirectional activity on the Bacillus subtilis theta plasmid pLS20. Molecular Microbiology 19: 1295–1306.

Merrikh H , Zhang Y , Grossman AD and Wang JD (2012) Replication‐transcription conflicts in bacteria. Nature Reviews. Microbiology 10: 449–458.

Mettrick KA and Grainge I (2016) Stability of blocked replication forks in vivo. Nucleic Acids Research 44: 657–668.

Midgley‐Smith SL , Dimude JU , Taylor T , et al. (2018) Chromosomal over‐replication in Escherichia coli recG cells is triggered by replication fork fusion and amplified if replichore symmetry is disturbed. Nucleic Acids Research 46: 7701–7715.

Mulcair MD , Schaeffer PM , Oakley AJ , et al. (2006) A molecular mousetrap determines polarity of termination of DNA replication in E. coli . Cell 125: 1309–1319.

Mulugu S , Potnis A , Shamsuzzaman J , Taylor KA and Bastia D (2001) Mechanism of termination of DNA replication of Escherichia coli involves helicase‐contrahelicase interaction. Proceedings of the National Academy of Sciences of the United States of America 98: 9569–9574.

Naqvi A , Tinsley E and Khan SA (2003) Purification and characterization of the PcrA helicase of Bacillus anthracis . Journal of Bacteriology 185: 6633–6639.

Natarajan S , Kelley WL and Bastia D (1991) Replication terminator protein of Escherichia coli is a transcriptional repressor of its own synthesis. Proceedings of the National Academy of Sciences of the United States of America 88: 3867–3871.

Neylon C , Kralicek AV , Hill TM and Dixon NE (2005) Replication termination in Escherichia coli: structure and antihelicase activity of the Tus‐Ter complex. Microbiology and Molecular Biology Reviews 69: 501–526.

Nordström K (2006) Plasmid R1–replication and its control. Plasmid 55: 1–26.

Pai KS , Bussiere DE , Wang F , et al. (1996) The structure and function of the replication terminator protein of Bacillus subtilis: identification of the ‘winged helix’ DNA‐binding domain. The EMBO Journal 15: 3164–3173.

Pandey M , Elshenawy MM , Jergic S , et al. (2015) Two mechanisms coordinate replication termination by the Escherichia coli Tus‐Ter complex. Nucleic Acids Research 43: 5924–5935.

Payne BT , van Knippenberg IC , Bell H , et al. (2006) Replication fork blockage by transcription factor‐DNA complexes in Escherichia coli . Nucleic Acids Research 34: 5194–5202.

Peebles CL , Higgins NP , Kreuzer KN , et al. (1979) Structure and activities of Escherichia coli DNA gyrase. Cold Spring Harbor Symposia on Quantitative Biology 43 (Pt 1): 41–52.

Petit MA and Ehrlich D (2002) Essential bacterial helicases that counteract the toxicity of recombination proteins. The EMBO Journal 21: 3137–3147.

Possoz C , Filipe SR , Grainge I and Sherratt DJ (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repressor‐bound DNA in vivo. The EMBO Journal 25: 2596–2604.

Reyes‐Lamothe R , Nicolas E and Sherratt DJ (2012) Chromosome replication and segregation in bacteria. Annual Review of Genetics 46: 121–143.

Roecklein B , Pelletier A and Kuempel P (1991) The tus gene of Escherichia coli: autoregulation, analysis of flanking sequences and identification of a complementary system in Salmonella typhimurium . Research in Microbiology 142: 169–175.

Roecklein BA and Kuempel PL (1992) In vivo characterization of tus gene expression in Escherichia coli . Molecular Microbiology 6: 1655–1661.

Rudolph CJ , Dhillon P , Moore T and Lloyd RG (2007) Avoiding and resolving conflicts between DNA replication and transcription. DNA Repair (Amst) 6: 981–993.

Rudolph CJ , Upton AL and Lloyd RG (2009) Replication fork collisions cause pathological chromosomal amplification in cells lacking RecG DNA translocase. Molecular Microbiology 74: 940–955.

Rudolph CJ , Mahdi AA , Upton AL and Lloyd RG (2010a) RecG protein and single‐strand DNA exonucleases avoid cell lethality associated with PriA helicase activity in Escherichia coli . Genetics 186: 473–492.

Rudolph CJ , Upton AL , Briggs GS and Lloyd RG (2010b) Is RecG a general guardian of the bacterial genome? DNA Repair (Amst) 9: 210–223.

Rudolph CJ , Upton AL , Stockum A , Nieduszynski CA and Lloyd RG (2013) Avoiding chromosome pathology when replication forks collide. Nature 500: 608–611.

Samson RY , Xu Y , Gadelha C , et al. (2013) Specificity and function of archaeal DNA replication initiator proteins. Cell Reports 3: 485–496.

Smith MT and Wake RG (1992) Definition and polarity of action of DNA replication terminators in Bacillus subtilis . Journal of Molecular Biology 227: 648–657.

Smith MT , de Vries CJ , Langley DB , King GF and Wake RG (1996) The Bacillus subtilis DNA replication terminator. Journal of Molecular Biology 260: 54–69.

Srivatsan A , Tehranchi A , MacAlpine DM and Wang JD (2010) Co‐orientation of replication and transcription preserves genome integrity. PLoS Genetics 6: e1000810.

Straight AF , Belmont AS , Robinett CC and Murray AW (1996) GFP tagging of budding yeast chromosomes reveals that protein‐protein interactions can mediate sister chromatid cohesion. Current Biology : CB. 6: 1599–1608.

Tanaka T and Masai H (2006) Stabilization of a stalled replication fork by concerted actions of two helicases. The Journal of Biological Chemistry 281: 3484–3493.

Tomasetti C , Li L and Vogelstein B (2017) Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention. Science 355: 1330–1334.

Trautinger BW , Jaktaji RP , Rusakova E and Lloyd RG (2005) RNA polymerase modulators and DNA repair activities resolve conflicts between DNA replication and transcription. Molecular Cell 19: 247–258.

Upton AL , Grove JI , Mahdi AA , et al. (2014) Cellular location and activity of Escherichia coli RecG proteins shed light on the function of its structurally unresolved C‐terminus. Nucleic Acids Research 42: 5702–5714.

Vivian JP , Porter CJ , Wilce JA and Wilce MC (2007) An asymmetric structure of the Bacillus subtilis replication terminator protein in complex with DNA. Journal of Molecular Biology 370: 481–491.

Wake RG (1996) DNA replication. Tussle with a terminator. Nature 383: 582–583.

Wake R and King G (1997) A tale of two terminators: crystal structures sharpen the debate on DNA replication fork arrest mechanisms. Structure (London, England : 1993) 5: 1–5.

Wang JD , Berkmen MB and Grossman AD (2007) Genome‐wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis . Proceedings of the National Academy of Sciences of the United States of America 104: 5608–5613.

Wang X , Lesterlin C , Reyes‐Lamothe R , Ball G and Sherratt DJ (2011) Replication and segregation of an Escherichia coli chromosome with two replication origins. Proceedings of the National Academy of Sciences of the United States of America 108: E243–E250.

Wendel BM , Courcelle CT and Courcelle J (2014) Completion of DNA replication in Escherichia coli . Proceedings of the National Academy of Sciences of the United States of America 111: 16454–16459.

Wilce JA , Vivian JP , Hastings AF , et al. (2001) Structure of the RTP‐DNA complex and the mechanism of polar replication fork arrest. Nature Structural Biology 8: 206–210.

Willis NA , Chandramouly G , Huang B , et al. (2014) BRCA1 controls homologous recombination at Tus/Ter‐stalled mammalian replication forks. Nature 510: 556–559.

Zaritsky A and Woldringh CL (2015) Chromosome replication, cell growth, division and shape: a personal perspective. Frontiers in Microbiology 6: 756.

Zhang J , Mahdi AA , Briggs GS and Lloyd RG (2010) Promoting and avoiding recombination: contrasting activities of the Escherichia coli RuvABC Holliday junction resolvase and RecG DNA translocase. Genetics 185: 23–37.

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Rudolph, Christian J, Corocher, Tayla‐Ann, Grainge, Ian, and Duggin, Iain G(Jan 2019) Termination of DNA Replication in Prokaryotes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001056.pub3]