1887

Chapter 28 : Chromosome Dimer Resolution

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Chromosome Dimer Resolution, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817640/9781555812324_Chap28-1.gif /docserver/preview/fulltext/10.1128/9781555817640/9781555812324_Chap28-2.gif

Abstract:

This chapter presents the processes that can lead to the dimerization of replicons and discusses the mechanisms that ensure their resolution. It also discusses how chromosome dimer resolution is integrated into other aspects of DNA processing during the bacterial cell cycle. The chromosomes and linear plasmids of are linear with hairpin ends. Bidirectional replication is initiated internally and, when complete, generates a circular dimer of the original linear replicon. In this circular dimer, the hairpin sites of the parental DNA are converted into palindromic “telomere” sites, which are used for chromosome dimer resolution. Xer site-specific recombination, which is responsible for chromosome dimer resolution, ensured their stable inheritance within . In and in bacteriophage N15 of , resolution of chromosome dimers is due to the action of a single enzyme, ResT or TelN, respectively. During tyrosine recombinase-mediated site-specific recombination, two tyrosine recombinase molecules bind cooperatively to ~30-bp specific core recombination sites in the DNA. The XerC and XerD site-specific recombinases function in chromosome dimer resolution by adding a single crossover at , a specific 28-bp core site located in the region of termination of replication of the chromosome. In vivo and in vitro studies show that in the absence of FtsK, Holliday junctions (HJs) are created and resolved back to the original substrate in cycles of XerC-mediated strand exchanges. The realization that Xer recombination uses different strategies to ensure resolution selectivity during plasmid and chromosome dimer resolution demonstrates the sophistication that has developed during bacterial evolution.

Citation: Barre F, Sherratt D. 2005. Chromosome Dimer Resolution, p 513-524. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch28

Key Concept Ranking

Chromosomal DNA
0.42797884
Agarose Gel Electrophoresis
0.4100707
0.42797884
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Chromosome dimer formation. The DNA backbone and the base pairing between two DNA strands in a duplex DNA molecule are schematically represented by “ladders.” Parental strands are represented as thin lines, and replicated daughter strands are represented as thick lines to help in the visualization of strand exchanges. The leading strand is shown as a continuous line, whereas the lagging strand is shown first as a dashed line representing the Okazaki fragments, which later become continuous strands. Arrows depict directions of replication. (A) 's replication strategy for linear replicons with covalently closed hairpin ends. The so-called “telomeres” are shown in light gray. Initiation of bidirectional replication occurs internally within the chromosome. Completion of replication produces a dimeric chromosome with two palindromic inverted repeats of the “telomere” sites. (B) Bidirectional replication of circular replicons. Replication will produce two catenated sister chromosomes in the absence of crossing over. An odd number of crossovers between the sister chromosomes generates a dimeric replicon. The region opposite the origin of replication, where chromosome dimer resolution occurs, is shown in light gray. (C) Rolling circle replication of circular replicons. Replication is initiated at a nick and is unidirectional. After one round of replication, the replication fork can continue to displace one of the sister chromosomes, leading to the formation of a multimeric linear concatemer of sister chromosomes that can be processed back into circular monomers or circular multimers by recombination.

Citation: Barre F, Sherratt D. 2005. Chromosome Dimer Resolution, p 513-524. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch28
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Chromosome dimer resolution. (A) Dimer resolution of and bacteriophage N15. DNA is shown as in Fig. 1 . Two ResT (or two TelN) enzymes bind to each of the two “telomere” sequences present as an inverted repeat in the dimeric replicon. Although no structural data are available, they are depicted as interacting with each other by an extension protruding from one molecule, which fits into a socket of the other molecule. (B) The mechanism of dimer resolution by tyrosine sitespecific recombinases. DNA is shown as in Fig. 1 . The C-terminal domain and the N-terminal domain of the recombinase monomers are represented by a large ellipse and small ellipses shaded with a gradient. These two domains form a C-shaped clamp that encircles half of the recombination site. The extreme C-terminal extension from each monomer is depicted by a small shaded circle. In Cre, this C-terminal extension fits into a socket in the C-terminal domain of a neighbor recombinase. DNA strand exchanges are performed successively by one pair of diagonally opposite recombinases in the complex and then the other. A complete cleavage-rejoining reaction by one of the recombinases proceeds in four steps identical to the ones performed by type IB topoisomerases: the initial protein-DNA complex is converted into a stable covalent enzyme-DNA adduct involving a 3′ phosphotyrosine linkage at the active site, before completion of the reaction by rejoining of the DNA. The phosphodiester linkage of the DNA substrate backbone which is attacked in this reaction lies 3 bp (, and ) or 4 bp () away from the center of the recombination site toward the bound recombinase. (C) Xer recombination at and . The and recombination sites are indicated by a thicker line on one of their DNA strands. The core recombination site is shown in gray. XerC binds to the half-site proximal to the accessory sequences. Three negative supercoils are entrapped by the accessory proteins and sequences. Synapsis of the core recombination sites is in antiparallel, with the C-terminal domain of all four recombinases facing the accessory sequences and proteins complex. The nucleoprotein complex structure is not planar but slightly bent, with the four arms of the DNA strands coming from the side of the C-terminal domains of the recombinases when they enter the nucleoprotein complex.

Citation: Barre F, Sherratt D. 2005. Chromosome Dimer Resolution, p 513-524. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch28
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

FtsK and the control of chromosome dimer resolution. (A) Scheme of the FtsK protein, showing the different domains that have been identified and the roles that they have been assigned. The N-terminal domain is shown by a shaded box, and the four transmembrane regions it contains are represented as black lines. A thicker line indicates the long transmembrane helix found at the end of the N-terminal domain. The extreme N terminus points toward the cytoplasm as well as the C-terminal domain of the protein. A dark box at the junction between the N-terminal domain and the linker region of the protein indicates the 50 amino acid residues potentially implicated in multimerization of the FtsK protein. The ATP binding site is shown as a darker box inside the C-terminal domain. (B) FtsK-dependent and independent pathways of Xer recombination at . In the absence of FtsK, the Xer synaptic complex adopts a conformation suitable for XerC-mediated strand exchanges, depicted by a kink at the XerD binding site. FtsK can use the energy of ATP to switch the Xer synaptic complex to a conformation suitable for XerD-strand exchanges, depicted by a kink at the XerC binding site. The intensity of the arrows reflects the probability of recombinational events. XerC and XerD cleavage sites are shown by white and black triangles, respectively. (C) The DNA translocase activity of FtsK can influence the topological outcome of the Xer recombination. Xer recombination between two directly repeated sites (black triangles) on a linear duplex creates one linear and one circular duplex with single sites. The circular product traps negative supercoils (–) preferentially. This is linked to the DNA translocation activity of FtsK, which creates positive supercoils in front of the advancing protein and negative supercoils in its wake. We propose that FtsK translocates along the DNA toward the synaptic complex to contact the recombinases and activate crossover formation by introducing positive writhe and twist onto the complex. Thus, positive supercoils are created between FtsK and the Xer complex, and negative supercoils are created on the other side of FtsK. On the substrate shown, FtsK should load most frequently between the repeated sites. To explain the preferential global negative supercoiling of the circular substrate, we propose two models: (i) the FtsK protein encircles only one duplex DNA; the Xer synaptic complex and/or an additional contact of DNA with the outside of FtsK prevent(s) negative supercoils from diffusing at the ends of the substrate, but allow(s) positive supercoils to diffuse away; (ii) the FtsK protein encircles two duplexes, thus preventing the negative supercoils from diffusing away; the Xer synaptic complex does not prevent the positive supercoils from diffusing away. (D) FtsK plays a safeguard role in DNA segregation when cellular events such as chromosome dimer formation have delayed separation and migration of the two sister chromosomes into the two daughter cells. The two replicated terminus regions remain associated asymmetrically in one of the daughter cells. We propose that FtsK forms an oriented pore through which the two duplex strands of a chromosome can pass. Its directional translocation activity would pump DNA when necessary, while its interaction with Xer- (triangles) can lead to chromosome dimer resolution. FtsK is represented by ovoids, the linker is represented by a zigzag, and the N-terminal part of the protein is represented by rectangles.

Citation: Barre F, Sherratt D. 2005. Chromosome Dimer Resolution, p 513-524. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch28
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817640.chap28
1. Abremski, K.,, and R. Hoess. 1985. Phage P1 Cre- loxP site-specific recombination. Effects of DNA supercoiling on catenation and knotting of recombinant products. J. Mol. Biol. 184: 211 220.
2. Abremski, K.,, R. Hoess,, and N. Sternberg. 1983. Studies on the properties of P1 site-specific recombination: evidence for topologically unlinked products following recombination. Cell 32: 1301 1311.
3. Alen, C.,, D. J. Sherratt,, and S. D. Colloms. 1997. Direct interaction of aminopeptidase A with recombination site DNA in Xer site-specific recombination. EMBO J. 16: 5188 5197.
4. Arciszewska, L. K.,, R. A. Baker,, B. Hallet,, and D. J. Sherratt. 2000. Coordinated control of XerC and XerD catalytic activities during Holliday junction resolution. J. Mol. Biol. 299: 391 403.
5. Arciszewska, L. K.,, I. Grainge,, and D. J. Sherratt. 1997. Action of site-specific recombinases XerC and XerD on tethered Holliday junctions. EMBO J. 16: 3731 3743.
6. Arciszewska, L. K.,, and D. J. Sherratt. 1995. Xer site-specific recombination in vitro. EMBO J. 14: 2112 2120.
7. Aussel, L.,, F. X. Barre,, M. Aroyo,, A. Stasiak,, A. Z. Stasiak,, and D. Sherratt. 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.
8. Austin, S.,, M. Ziese,, and N. Sternberg. 1981. A novel role for site-specific recombination in maintenance of bacterial replicons. Cell 25: 729 736.
9. Barre, F. X.,, M. Aroyo,, S. D. Colloms,, A. Helfrich,, F. Cornet,, and D. J. Sherratt. 2000. FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev. 14: 2976 2988.
10. Barre, F. X.,, B. Soballe,, B. Michel,, M. Aroyo,, M. Robertson,, and D. Sherratt. 2001. Circles: the replication-recombination-chromosome segregation connection. Proc. Natl. Acad. Sci. USA 98: 8189 8195.
11. Bath, J.,, L. J. Wu,, J. Errington,, and J. C. Wang. 2000. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290: 995 997.
12. Begg, K. J.,, S. J. Dewar,, and W. D. Donachie. 1995. A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177: 6211 6222.
13. Blakely, G.,, S. Colloms,, G. May,, M. Burke,, and D. Sherratt. 1991. Escherichia coli XerC recombinase is required for chromosomal segregation at cell division. New Biol. 3: 789 798.
14. Blakely, G.,, G. May,, R. McCulloch,, L. K. Arciszewska,, M. Burke,, S. T. Lovett,, and D. J. Sherratt. 1993. Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75: 351 361.
15. Bregu, M.,, D. J. Sherratt,, and S. D. Colloms. 2002. Accessory factors determine the order of strand exchange in Xer recombination at psi. EMBO J. 21: 3888 3897.
16. Burke, M.,, A. F. Merican,, and D. J. Sherratt. 1994. Mutant Escherichia coli arginine repressor proteins that fail to bind L-arginine, yet retain the ability to bind their normal DNA-binding sites. Mol. Microbiol. 13: 609 618.
17. Capiaux, H.,, F. Cornet,, J. Corre,, M. Guijo,, K. Perals,, J. E. Rebollo,, and J. Louarn. 2001. Polarization of the Escherichia coli chromosome. A view from the terminus. Biochimie 83: 161 170.
18. Capiaux, H.,, C. Lesterlin,, K. Perals,, J. M. Louarn,, and F. Cornet. 2002. A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep. 3: 532 536.
19. Chaconas, G.,, P. E. Stewart,, K. Tilly,, J. L. Bono,, and P. Rosa. 2001. Telomere resolution in the Lyme disease spirochete. EMBO J. 20: 3229 3237.
20. Chen, J. C.,, and J. Beckwith. 2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42: 395 413.
21. Chen, Y.,, U. Narendra,, L. E. Iype,, M. M. Cox,, and P. A. Rice. 2000. Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol. Cell 6: 885 897.
22. Clerget, M. 1991. Site-specific recombination promoted by a short DNA segment of plasmid R1 and by a homologous segment in the terminus region of the Escherichia coli chromosome. New Biol. 3: 780 788.
23. Colloms, S. D.,, C. Alen,, and D. J. Sherratt. 1998. The ArcA/ArcB two-component regulatory system of Escherichia coli is essential for Xer site-specific recombination at psi. Mol. Microbiol. 28: 521 530.
24. Colloms, S. D.,, J. Bath,, and D. J. Sherratt. 1997. Topological selectivity in Xer site-specific recombination. Cell 88: 855 864.
25. Colloms, S. D.,, R. McCulloch,, K. Grant,, L. Neilson,, and D. J. Sherratt. 1996. Xer-mediated site-specific recombination in vitro. EMBO J. 15: 1172 1181.
26. Colloms, S. D.,, P. Sykora,, G. Szatmari,, and D. J. Sherratt. 1990. Recombination at ColE1 cer requires the Escherichia coli xerC gene product, a member of the lambda integrase family of site-specific recombinases. J. Bacteriol. 172: 6973 6980.
27. Cornet, F.,, J. Louarn,, J. Patte,, and J. M. Louarn. 1996. Restriction of the activity of the recombination site dif to a small zone of the Escherichia coli chromosome. Genes Dev. 10: 1152 1161.
28. Cornet, F.,, I. Mortier,, J. Patte,, and J.-M. Louarn. 1994. Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J. Bacteriol. 176: 3188 3195.
29. Corre, J.,, and J.-M. Louarn. 2002. Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli. J. Bacteriol. 184: 3801 3807.
30. Cox, M. M.,, M. F. Goodman,, K. N. Kreuzer,, D. J. Sherratt,, S. J. Sandler,, and K. J. Marians. 2000. The importance of repairing stalled replication forks. Nature 404: 37 41.
31. Deneke, J.,, G. Ziegelin,, R. Lurz,, and E. Lanka. 2000. The protelomerase of temperate Escherichia coli phage N15 has cleaving-joining activity. Proc. Natl. Acad. Sci. USA 97: 7721 7726.
32. Deneke, J.,, G. Ziegelin,, R. Lurz,, and E. Lanka. 2002. Phage N15 telomere resolution. Target requirements for recognition and processing by the protelomerase. J. Biol. Chem. 277: 10410 10419.
33. Dorazi, R.,, and S. J. Dewar. 2000. Membrane topology of the N-terminus of the Escherichia coli FtsK division protein. FEBS Lett. 478: 13 18.
34. Draper, G. C.,, N. McLennan,, K. Begg,, M. Masters,, and W. D. Donachie. 1998. Only the N-terminal domain of FtsK functions in cell division. J. Bacteriol. 180: 4621 4627.
35. Du, S.,, and P. Traktman. 1996. Vaccinia virus DNA replication: two hundred base pairs of telomeric sequence confer optimal replication efficiency on minichromosome templates. Proc. Natl. Acad. Sci. USA 93: 9693 9698.
36. Errington, J.,, J. Bath,, and L. J. Wu. 2001. DNA transport in bacteria. Nat. Rev. Mol. Cell. Biol. 2: 538 545.
36a.. Espeli, O.,, C. Lee,, and K. J. Marians. 2003. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem. 278: 44639 44644.
37. Ferreira, H.,, D. Sherratt,, and L. Arciszewska. 2001. Switching catalytic activity in the XerCD site-specific recombination machine. J. Mol. Biol. 312: 45 57.
38. Garcia, A. D.,, L. Aravind,, E. V. Koonin,, and B. Moss. 2000. Bacterial-type DNA Holliday junction resolvases in eukaryotic viruses. Proc. Natl. Acad. Sci. USA 97: 8926 8931.
39. Garcia, A. D.,, and B. Moss. 2001. Repression of vaccinia virus Holliday junction resolvase inhibits processing of viral DNA into unit-length genomes. J. Virol. 75: 6460 6471.
40. Gopaul, D. N.,, F. Guo,, and G. D. Van Duyne. 1998. Structure of the Holliday junction intermediate in Cre-loxP sitespecific recombination. EMBO J. 17: 4175 4187.
41. Gordon, G. S.,, and A. Wright. 1998. DNA segregation: putting chromosomes in their place. Curr. Biol. 8: R925 R927.
42. Guo, F.,, D. N. Gopaul,, and G. D. van Duyne. 1997. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389: 40 46.
43. Hallet, B.,, L. K. Arciszewska,, and D. J. Sherratt. 1999. Reciprocal control of catalysis by the tyrosine recombinases XerC and XerD: an enzymatic switch in site-specific recombination. Mol. Cell 4: 949 959.
43a.. Ip, S. Y. P.,, M. Bregu,, F.-X. Barre,, and D. J. Sherratt. 2003. Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J. 22: 6399 6407.
44. Kobryn, K.,, and G. Chaconas. 2001. The circle is broken: telomere resolution in linear replicons. Curr. Opin. Microbiol. 4: 558 564.
45. Kobryn, K.,, and G. Chaconas. 2002. ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol. Cell 9: 195 201.
46. Kuempel, P. L.,, J. M. Henson,, L. Dircks,, M. Tecklenburg,, and D. F. Lim. 1991. dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol. 3: 799 811.
47. Kusano, K.,, K. Nakayama,, and H. Nakayama. 1989. Plasmid-mediated lethality and plasmid multimer formation in an Escherichia coli recBC sbcBC mutant. Involvement of RecF recombination pathway genes. J. Mol. Biol. 209: 623 634.
47a.. Lau, I. F.,, S. R. Filipe,, B. Søballe,, O.-A. Økstad,, F.-X. Barre,, and D. J. Sherratt. 2003. Spatial and temporal organisation of replicating Escherichia coli chromosomes. Mol. Microbiol. 49: 731 743.
48. Leslie, N. R.,, and D. J. Sherratt. 1995. Site-specific recombination in the replication terminus region of Escherichia coli: functional replacement of dif. EMBO J. 14: 1561 1570.
49. Liu, G.,, G. C. Draper,, and W. D. Donachie. 1998. FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol. Microbiol. 29: 893 903.
49a.. Massey, T.,, L. Aussel,, F.-X. Barre,, and D. J. Sherratt. 2004. Asymmetric activation of Xer site-specific recombination by FtsK. EMBO Rep. 5: 399 404.
50. Maurizi, M. R.,, and C. C. Li. 2001. AAA proteins: in search of a common molecular basis: International meeting on cellular functions of AAA proteins. EMBO Rep. 2: 980 985.
51. McClintock, B. 1932. A correlation of ring-shaped chromosomes with variegation in Zea mays. Proc. Natl. Acad. Sci. USA 18: 677 681.
52. Michel, B.,, G. D. Recchia,, M. Penel-Colin,, S. D. Ehrlich,, and D. J. Sherratt. 2000. Resolution of Holliday junctions by RuvABC prevents dimer formation in rep mutants and UV irradiated cells. Mol. Microbiol. 37: 181 191.
53. Neuwald, A. F.,, L. Aravind,, J. L. Spouge,, and E. V. Koonin. 1999. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9: 27 43.
54. Niki, H.,, and S. Hiraga. 1998. Polar localization of the replication origin and terminus in Escherichia coli nucleoids during chromosome partitioning. Genes Dev. 12: 1036 1045.
55. Niki, H.,, Y. Yamaichi,, and S. Hiraga. 2000. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14: 212 223.
56. Palaniyar, N.,, E. Gerasimopoulos,, and D. H. Evans. 1999. Shope fibroma virus DNA topoisomerase catalyses Holliday junction resolution and hairpin formation in vitro. J. Mol. Biol. 287: 9 20.
57. Perals, K.,, H. Capiaux,, J. B. Vincourt,, J. M. Louarn,, D. J. Sherratt,, and F. Cornet. 2001. Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol. Microbiol. 39: 904 913.
58. Perals, K.,, F. Cornet,, Y. Merlet,, I. Delon,, and J. M. Louarn. 2000. Functional polarization of the Escherichia coli chromosome terminus: the dif site acts in chromosome dimer resolution only when located between long stretches of opposite polarity. Mol. Microbiol. 36: 33 43.
59. Picardeau, M.,, J. R. Lobry,, and B. J. Hinnebusch. 1999. Physical mapping of an origin of bidirectional replication at the centre of the Borrelia burgdorferi linear chromosome. Mol. Microbiol. 32: 437 445.
60. Recchia, G. D.,, M. Aroyo,, D. Wolf,, G. Blakely,, and D. J. Sherratt. 1999. FtsK-dependent and -independent pathways of Xer site-specific recombination. EMBO J. 18: 5724 5734.
61. Recchia, G. D.,, and D. J. Sherratt. 1999. Conservation of Xer site-specific recombination genes in bacteria. Mol. Microbiol. 34: 1146 1148.
62. Sadowski, P. D. 1995. The Flp recombinase of the 2-microns plasmid of Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 51: 53 91.
63. Sekiguchi, J.,, C. Cheng,, and S. Shuman. 2000. Resolution of a Holliday junction by vaccinia topoisomerase requires a spacer DNA segment 3′ of the CCCTT/ cleavage sites. Nucleic Acids Res. 28: 2658 2663.
64. Sharp, M. D.,, and K. Pogliano. 1999. An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc. Natl. Acad. Sci. USA 96: 14553 14558.
65. Sherratt, D. J.,, I. F. Lau,, and F. X. Barre. 2001. Chromosome segregation. Curr. Opin. Microbiol. 4: 653 659.
66. Silberstein, Z.,, S. Maor,, I. Berger,, and A. Cohen. 1990. Lambda Red-mediated synthesis of plasmid linear multimers in Escherichia coli K12. Mol. Gen. Genet. 223: 496 507.
67. Stark, W. M.,, and M. R. Boocoock,. 1995. Topological selectivity in site-specific recombination, p. 101 129. In D. J. Sherratt (ed.), Mobile Genetic Elements. IRL Press, Oxford, United Kingdom.
68. Steiner, W.,, G. Liu,, W. D. Donachie,, and P. Kuempel. 1999. The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol. Microbiol. 31: 579 583.
69. Steiner, W. W.,, and P. L. Kuempel. 1998. Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J. Bacteriol. 180: 6269 6275.
70. Stirling, C. J.,, S. D. Colloms,, J. F. Collins,, G. Szatmari,, and D. J. Sherratt. 1989. xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase. EMBO J. 8: 1623 1627.
71. Stirling, C. J.,, G. Szatmari,, G. Stewart,, M. C. Smith,, and D. J. Sherratt. 1988. The arginine repressor is essential for plasmid-stabilizing site-specific recombination at the ColE1 cer locus. EMBO J. 7: 4389 4395.
72. Strater, N.,, D. J. Sherratt,, and S. D. Colloms. 1999. X-ray structure of aminopeptidase A from Escherichia coli and a model for the nucleoprotein complex in Xer site-specific recombination. EMBO J. 18: 4513 4522.
73. Subramanya, H. S.,, L. K. Arciszewska,, R. A. Baker,, L. E. Bird,, D. J. Sherratt,, and D. B. Wigley. 1997. Crystal structure of the site-specific recombinase, XerD. EMBO J. 16: 5178 5187.
74. Summers, D. K.,, C. W. Beton,, and H. L. Withers. 1993. Multicopy plasmid instability: the dimer catastrophe hypothesis. Mol. Microbiol. 8: 1031 1038.
75. Summers, D. K.,, and D. J. Sherratt. 1984. Multimerization of high copy number plasmids causes instability: ColE1 encodes a determinant essential for plasmid monomerization and stability. Cell 36: 1097 1103.
76. Thaler, D. S.,, and F. W. Stahl. 1988. DNA double-chain breaks in recombination of phage lambda and of yeast. Annu. Rev. Genet. 22: 169 197.
77. Wang, L.,, and J. Lutkenhaus. 1998. FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol. Microbiol. 29: 731 740.
78. Warren, G. J.,, and A. J. Clark. 1980. Sequence-specific recombination of plasmid ColE1. Proc. Natl. Acad. Sci. USA 77: 6724 6728.
79. Wu, L. J.,, P. J. Lewis,, R. Allmansberger,, P. M. Hauser,, and J. Errington. 1995. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev. 9: 1316 1326.
79a.. Yates, J.,, M. Aroyo,, D. J. Sherratt,, and F.-X. Barre. 2003. Species specificity in the activation of Xer recombination at dif by FtsK. Mol. Microbiol. 49: 241 249.
80. Yu, X. C.,, A. H. Tran,, Q. Sun,, and W. Margolin. 1998. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180: 1296 1304.
81. Yu, X. C.,, E. K. Weihe,, and W. Margolin. 1998. Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J. Bacteriol. 180: 6424 6428.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error