Bacterial chromosome segregation

Frontiers in Bioscience

Volumn 17, Issue 3, 2012, Pages 1020-1034

  Possoz, Christophe ^a   Junier, Ivan ^b,c   Espeli, Olivier ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^c Institute of Complex Systems   (France)

Author keywords

Chromosome partition; DNA factory; Entropy; FROS; FtsK; Macrodomains; MatP; MukB; Nucleoid splitting; ParB; Replichores; Review; Sister chromatid cohesion; SMC; Spo0J

Indexed keywords

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES; ESCHERICHIA COLI; VIBRIO CHOLERAE;

BACTERIAL CHROMOSOME; CHROMOSOME SEGREGATION; REVIEW; SISTER CHROMATID EXCHANGE;

CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; SISTER CHROMATID EXCHANGE;

EID: 84859235483     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3971     Document Type: Article

References (109)

1. K. Nasmyth: Segregating sister genomes: the molecular biology of chromosome separation. Science, 297(5581), 559- 65 (2002). (Pubitemid 34815333)
2. F. Jacob and S. Brenner: [On the regulation of DNA synthesis in bacteria: the hypothesis of the replicon.]. C R Hebd Seances Acad Sci, 256, 298-300 (1963).
3. H. Niki, A. Jaffe, R. Imamura, T. Ogura and S. Hiraga: The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J, 10(1), 183-93 (1991). (Pubitemid 21905281)
4. H. J. Nielsen, B. Youngren, F. G. Hansen and S. Austin: Dynamics of Escherichia coli chromosome segregation during multifork replication. J Bacteriol, 189(23), 8660-6 (2007). (Pubitemid 350210036)
5. B. Hu, G. Yang, W. Zhao, Y. Zhang and J. Zhao: MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol, 63(6), 1640-52 (2007). (Pubitemid 46426700)
6. M. A. Fogel and M. K. Waldor: Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol, 55(1), 125-36 (2005). (Pubitemid 40127890)
7. N. Dubarry, F. Pasta and D. Lane: ParABS systems of the four replicons of Burkholderia cenocepacia: new chromosome centromeres confer partition specificity. J Bacteriol, 188(4), 1489-96 (2006). (Pubitemid 43228682)
8. C. D. Webb, A. Teleman, S. Gordon, A. Straight, A. Belmont, D. C. Lin, A. D. Grossman, A. Wright and R. Losick: Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell, 88(5), 667-74 (1997). (Pubitemid 27152409)
9. D. Jakimowicz, P. Zydek, A. Kois, J. Zakrzewska- Czerwinska and K. F. Chater: Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol Microbiol, 65(3), 625-41 (2007). (Pubitemid 47077226)
10. S. Cooper and C. E. Helmstetter: Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol, 31(3), 519-40 (1968).
11. M. Abe and J. Tomizawa: Replication of the escherichia coli K12 chromosome. Proc Natl Acad Sci USA, 58(5), 1911- 8 (1967).
12. L. G. Caro and C. M. Berg: Chromosome replication in some strains of Escherichia coli K12. Cold Spring Harb Symp Quant Biol, 33, 559-73 (1968).
13. G. Piekarski: Zytologisclie Untersuchungen an Bakterien im ultravioletten Licht. Zbl. Bukt., 142(69) (1938).
14. D. J. Mason and D. M. Powelson: Nuclear division as observed in live bacteria by a new technique. J Bacteriol, 71(4), 474-9 (1956).
15. Y. Yamaichi and H. Niki: migS, a cis-acting site that affects bipolar positioning of oriC on the Escherichia coli chromosome. EMBO J, 23(1), 221-33 (2004). (Pubitemid 38165762)
16. D. Bates and N. Kleckner: Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell, 121(6), 899-911 (2005). (Pubitemid 40806421)
17. A. F. Straight, A. S. Belmont, C. C. Robinett and A. W. Murray: GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol, 6(12), 1599-608 (1996). (Pubitemid 27050227)
18. G. S. Gordon, D. Sitnikov, C. D. Webb, A. Teleman, A. Straight, R. Losick, A. W. Murray and A. Wright: Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell, 90(6), 1113-21 (1997). (Pubitemid 27408525)
19. S. Adachi, T. Fukushima and S. Hiraga: Dynamic events of sister chromosomes in the cell cycle of Escherichia coli. Genes Cells, 13(2), 181-97 (2008). (Pubitemid 351188988)
20. Y. Li, K. Sergueev and S. Austin: The segregation of the Escherichia coli origin and terminus of replication. Mol Microbiol, 46(4), 985-96 (2002).
21. Y. Li, B. Youngren, K. Sergueev and S. Austin: Segregation of the Escherichia coli chromosome terminus. Mol Microbiol, 50(3), 825-34 (2003). (Pubitemid 37372246)
22. X. Wang, C. Possoz and D. J. Sherratt: Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev, 19(19), 2367-77 (2005). (Pubitemid 41396913)
23. O. Espeli, R. Mercier and F. Boccard: DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol, 68(6), 1418-27 (2008). (Pubitemid 351725253)
24. S. Elmore, M. Muller, N. Vischer, T. Odijk and C. L. Woldringh: Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli. J Struct Biol, 151(3), 275-87 (2005). (Pubitemid 41338734)
25. P. Srivastava, R. A. Fekete and D. K. Chattoraj: Segregation of the replication terminus of the two Vibrio cholerae chromosomes. J Bacteriol, 188(3), 1060-70 (2006). (Pubitemid 43146422)
26. X. Wang, X. Liu, C. Possoz and D. J. Sherratt: The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev, 20(13), 1727-31 (2006). (Pubitemid 43992881)
27. P. A. Wiggins, K. C. Cheveralls, J. S. Martin, R. Lintner and J. Kondev: Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. Proc Natl Acad Sci USA, 107(11), 4991-5 (2010).
28. R. Mercier, M. A. Petit, S. Schbath, S. Robin, M. El Karoui, F. Boccard and O. Espeli: The MatP/matS sitespecific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell, 135(3), 475-85 (2008).
29. C. Possoz, S. R. Filipe, I. Grainge and D. J. Sherratt: Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. EMBO J, 25(11), 2596-604 (2006). (Pubitemid 44012241)
30. P. H. Viollier, M. Thanbichler, P. T. McGrath, L. West, M. Meewan, H. H. McAdams and L. Shapiro: Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA, 101(25), 9257-62 (2004). (Pubitemid 38812862)
31. H. J. Nielsen, Y. Li, B. Youngren, F. G. Hansen and S. Austin: Progressive segregation of the Escherichia coli chromosome. Mol Microbiol, 61(2), 383-93 (2006). (Pubitemid 44356570)
32. C. W. Shebelut, J. M. Guberman, S. van Teeffelen, A. A. Yakhnina and Z. Gitai: Caulobacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci USA, 107(32), 14194-8 (2010).
33. R. B. Jensen: Analysis of the terminus region of the Caulobacter crescentus chromosome and identification of the dif site. J Bacteriol, 188(16), 6016-9 (2006). (Pubitemid 44384110)
34. M. Valens, S. Penaud, M. Rossignol, F. Cornet and F. Boccard: Macrodomain organization of the Escherichia coli chromosome. EMBO J, 23(21), 4330-41 (2004). (Pubitemid 39546170)
35. Y. Yamaichi, M. A. Fogel and M. K. Waldor: par genes and the pathology of chromosome loss in Vibrio cholerae. Proc Natl Acad Sci USA, 104(2), 630-5 (2007). (Pubitemid 46123076)
36. A. Ryter, P. Schaeffer and H. Ionesco: [Cytologic classification, by their blockage stage, of sporulation mutants of Bacillus subtilis Marburg]. Ann Inst Pasteur (Paris), 110(3), 305-15 (1966).
37. K. Nasmyth and C. H. Haering: Cohesin: its roles and mechanisms. Annu Rev Genet, 43, 525-58 (2009).
38. Y. Sunako, T. Onogi and S. Hiraga: Sister chromosome cohesion of Escherichia coli. Mol Microbiol, 42(5), 1233- 41 (2001). (Pubitemid 34209085)
39. Z. M. Petrushenko, C. H. Lai, R. Rai and V. V. Rybenkov: DNA reshaping by MukB. Right-handed knotting, left-handed supercoiling. J Biol Chem, 281(8), 4606-15 (2006). (Pubitemid 43847719)
40. M. C. Joshi, A. Bourniquel, J. Fisher, B. T. Ho, D. Magnan, N. Kleckner and D. Bates: Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci USA, 108(7), 2765-70 (2011).
41. R. A. Fekete and D. K. Chattoraj: A cis-acting sequence involved in chromosome segregation in Escherichia coli. Mol Microbiol, 55(1), 175-83 (2005). (Pubitemid 40127894)
42. R. Reyes-Lamothe, C. Possoz, O. Danilova and D. J. Sherratt: Independent positioning and action of Escherichia coli replisomes in live cells. Cell, 133(1), 90-102 (2008). (Pubitemid 351442987)
43. C. L. Woldringh and N. Nanninga: Structural and physical aspects of bacterial chromosome segregation. J Struct Biol, 156(2), 273-83 (2006). (Pubitemid 44666441)
44. A. Fiebig, K. Keren and J. A. Theriot: Fine-scale timelapse analysis of the biphasic, dynamic behaviour of the two Vibrio cholerae chromosomes. Mol Microbiol, 60(5), 1164-78 (2006).
45. Z. Gitai, N. A. Dye, A. Reisenauer, M. Wachi and L. Shapiro: MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell, 120(3), 329-41 (2005). (Pubitemid 40222428)
46. J. L. Ptacin, S. F. Lee, E. C. Garner, E. Toro, M. Eckart, L. R. Comolli, W. E. Moerner and L. Shapiro: A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol, 12(8), 791-8 (2010).
47. W. B. Schofield, H. C. Lim and C. Jacobs-Wagner: Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J, 29(18), 3068-81 (2010).
48. A. Rosa and R. Everaers: Structure and dynamics of interphase chromosomes. PLoS Comput Biol, 4(8), e1000153 (2008).
49. P. R. Cook and D. Marenduzzo: Entropic organization of interphase chromosomes. J Cell Biol, 186(6), 825-34 (2009).
50. I. Junier, O. Martin and F. Kepes: Spatial and topological organization of DNA chains induced by gene co-localization. PLoS Comput Biol, 6(2), e1000678 (2010).
51. P. G. De Gennes: Scaling concept in polymer physics. (1998).
52. L. Postow, N. J. Crisona, B. J. Peter, C. D. Hardy and N. R. Cozzarelli: Topological challenges to DNA replication: conformations at the fork. Proc Natl Acad Sci USA, 98(15), 8219-26 (2001). (Pubitemid 32678016)
53. S. Jun: Can entropy save bacteria? In: arXiv. http://arxiv.org/abs/0808. 2646(2008).
54. S. Jun and B. Mulder: Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA, 103(33), 12388-93 (2006). (Pubitemid 44267269)
55. S. Jun and A. Wright: Entropy as the driver of chromosome segregation. Nat Rev Microbiol, 8(8), 600-7 (2010).
56. J. Fan, K. Tuncay and P. J. Ortoleva: Chromosome segregation in Escherichia coli division: a free energydriven string model. Comput Biol Chem, 31(4), 257-64 (2007) 3. (Pubitemid 47089111)
57. T. Odijk: Osmotic compaction of supercoiled DNA into a bacterial nucleoid. Biophys Chem, 73(1-2), 23-9 (1998). (Pubitemid 28325691)
58. G. Ebersbach and K. Gerdes: Plasmid segregation mechanisms. Annu Rev Genet, 39, 453-79 (2005). (Pubitemid 43011123)
59. K. Ireton, N. W. t. Gunther and A. D. Grossman: spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol, 176(17), 5320-9 (1994).
60. M. E. Sharpe and J. Errington: The Bacillus subtilis sojspo0J locus is required for a centromere-like function involved in prespore chromosome partitioning. Mol Microbiol, 21(3), 501-9 (1996). (Pubitemid 26323773)
61. G. R. Bowman, L. R. Comolli, J. Zhu, M. Eckart, M. Koenig, K. H. Downing, W. E. Moerner, T. Earnest and L. Shapiro: A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell, 134(6), 945-55 (2008).
62. M. Thanbichler and L. Shapiro: MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell, 126(1), 147-62 (2006).
63. D. C. Lin and A. D. Grossman: Identification and characterization of a bacterial chromosome partitioning site. Cell, 92(5), 675-85 (1998). (Pubitemid 28141516)
64. S. Ben-Yehuda, D. Z. Rudner and R. Losick: RacA, a bacterial protein that anchors chromosomes to the cell poles. Science, 299(5606), 532-6 (2003). (Pubitemid 36135143)
65. L. J. Wu and J. Errington: RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol, 49(6), 1463- 75 (2003). (Pubitemid 37153510)
66. K. P. Lemon and A. D. Grossman: The extrusioncapture model for chromosome partitioning in bacteria. Genes Dev, 15(16), 2031-41 (2001). (Pubitemid 32762046)
67. K. P. Lemon and A. D. Grossman: Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science, 282(5393), 1516-9 (1998). (Pubitemid 28538618)
68. K. P. Lemon and A. D. Grossman: Movement of replicating DNA through a stationary replisome. Mol Cell, 6(6), 1321-30 (2000). (Pubitemid 32045925)
69. M. A. White, J. K. Eykelenboom, M. A. Lopez- Vernaza, E. Wilson and D. R. Leach: Non-random segregation of sister chromosomes in Escherichia coli. Nature, 455(7217), 1248-50 (2008).
70. E. Esnault, M. Valens, O. Espeli and F. Boccard: Chromosome structuring limits genome plasticity in Escherichia coli. PLoS Genet, 3(12), e226 (2007).
71. C. Lesterlin, C. Pages, N. Dubarry, S. Dasgupta and F. Cornet: Asymmetry of chromosome Replichores renders the DNA translocase activity of FtsK essential for cell division and cell shape maintenance in Escherichia coli. PLoS Genet, 4(12), e1000288 (2008).
72. M. B. Berkmen and A. D. Grossman: Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol Microbiol, 62(1), 57-71 (2006). (Pubitemid 44386550)
73. O. Danilova, R. Reyes-Lamothe, M. Pinskaya, D. Sherratt and C. Possoz: MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol, 65(6), 1485-92 (2007). (Pubitemid 47347830)
74. R. B. Jensen, S. C. Wang and L. Shapiro: A moving DNA replication factory in Caulobacter crescentus. EMBO J, 20(17), 4952-63 (2001). (Pubitemid 32848647)
75. D. Bates: The bacterial replisome: back on track? Mol Microbiol, 69(6), 1341-8 (2008).
76. I. A. Berlatzky, A. Rouvinski and S. Ben-Yehuda: Spatial organization of a replicating bacterial chromosome. Proc Natl Acad Sci USA, 105(37), 14136-40 (2008).
77. M. D. Wang, M. J. Schnitzer, H. Yin, R. Landick, J. Gelles and S. M. Block: Force and velocity measured for single molecules of RNA polymerase. Science, 282(5390), 902-7 (1998). (Pubitemid 28507515)
78. J. Gelles, H. Yin, L. Finzi, O. K. Wong and R. Landick: Single-molecule kinetic studies on DNA transcription and transcriptional regulation. Biophys J, 68(4 Suppl), 73S (1995).
79. J. E. Cabrera, C. Cagliero, S. Quan, C. L. Squires and D. J. Jin: Active transcription of rRNA operons condenses the nucleoid in Escherichia coli: examining the effect of transcription on nucleoid structure in the absence of transertion. J Bacteriol, 191(13), 4180-5 (2009).
80. J. Dworkin and R. Losick: Does RNA polymerase help drive chromosome segregation in bacteria? Proc Natl Acad Sci USA, 99(22), 14089-94 (2002). (Pubitemid 35257629)
81. X. Wang and D. J. Sherratt: Independent segregation of the two arms of the Escherichia coli ori region requires neither RNA synthesis nor MreB dynamics. J Bacteriol, 192(23), 6143-53 (2010).
82. E. P. Rocha: The organization of the bacterial genome. Annu Rev Genet, 42, 211-33 (2008).
83. V. Norris and I. Fishov: Hypothesis: membrane domains and hyperstructures control bacterial division. Biochimie, 83(1), 91-7 (2001). (Pubitemid 32181529)
84. I. Fishov and C. L. Woldringh: Visualization of membrane domains in Escherichia coli. Mol Microbiol, 32(6), 1166-72 (1999). (Pubitemid 29286657)
85. A. Aranovich, G. Y. Gdalevsky, R. Cohen-Luria, I. Fishov and A. H. Parola: Membrane-catalyzed nucleotide exchange on DnaA. Effect of surface molecular crowding. J Biol Chem, 281(18), 12526-34 (2006). (Pubitemid 43855340)
86. E. Mileykovskaya, I. Fishov, X. Fu, B. D. Corbin, W. Margolin and W. Dowhan: Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem, 278(25), 22193-8 (2003). (Pubitemid 36830264)
87. C. L. Woldringh: The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol, 45(1), 17-29 (2002). (Pubitemid 35025930)
88. S. Gruber and J. Errington: Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell, 137(4), 685-96 (2009).
89. N. L. Sullivan, K. A. Marquis and D. Z. Rudner: Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell, 137(4), 697-707 (2009).
90. T. Cui, N. Moro-oka, K. Ohsumi, K. Kodama, T. Ohshima, N. Ogasawara, H. Mori, B. Wanner, H. Niki and T. Horiuchi: Escherichia coli with a linear genome. EMBO Rep, 8(2), 181-7 (2007). (Pubitemid 46420847)
91. R. Hayama and K. J. Marians: Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc Natl Acad Sci USA, 107(44), 18826-31 (2010).
92. S. Bigot, V. Sivanathan, C. Possoz, F. X. Barre and F. Cornet: FtsK, a literate chromosome segregation machine. Mol Microbiol, 64(6), 1434-41 (2007). (Pubitemid 46889905)
93. M. E. Val, S. P. Kennedy, M. El Karoui, L. Bonne, F. Chevalier and F. X. Barre: FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet, 4(9), e1000201 (2008).
94. S. P. Kennedy, F. Chevalier and F. X. Barre: Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol Microbiol, 68(4), 1018-28 (2008). (Pubitemid 351581068)
95. N. Dubarry and F. X. Barre: Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J, 29(3), 597-605.
96. N. Dubarry, C. Possoz and F. X. Barre: Multiple regions along the Escherichia coli FtsK protein are implicated in cell division. Mol Microbiol, 78(5), 1088-100.
97. W. W. Steiner and P. L. Kuempel: Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J Bacteriol, 180(23), 6269-75 (1998). (Pubitemid 28544258)
98. X. C. Yu, E. K. Weihe and W. Margolin: Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J Bacteriol, 180(23), 6424-8 (1998). (Pubitemid 28544282)
99. S. C. Wang, L. West and L. Shapiro: The bifunctional FtsK protein mediates chromosome partitioning and cell division in Caulobacter. J Bacteriol, 188(4), 1497-508 (2006). (Pubitemid 43228683)
100. T. H. Massey, C. P. Mercogliano, J. Yates, D. J. Sherratt and J. Lowe: Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell, 23(4), 457-69 (2006). (Pubitemid 44205486)
101. O. A. Saleh, C. Perals, F. X. Barre and J. F. Allemand: Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment. EMBO J, 23(12), 2430-9 (2004). (Pubitemid 38954850)
102. S. Bigot, O. A. Saleh, C. Lesterlin, C. Pages, M. El Karoui, C. Dennis, M. Grigoriev, J. F. Allemand, F. X. Barre and F. Cornet: KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J, 24(21), 3770-80 (2005). (Pubitemid 41581693)
103. O. Espeli, C. Lee and K. J. Marians: A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J Biol Chem, 278(45), 44639-44 (2003). (Pubitemid 37377219)
104. I. Grainge, M. Bregu, M. Vazquez, V. Sivanathan, S. C. Ip and D. J. Sherratt: Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J, 26(19), 4228-38 (2007). (Pubitemid 47525160)
105. X. Wang, R. Reyes-Lamothe and D. J. Sherratt: Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev, 22(17), 2426-33 (2008).
106. E. L. Zechiedrich, A. B. Khodursky and N. R. Cozzarelli: Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev, 11(19), 2580-92 (1997). (Pubitemid 27438838)
107. B. J. Peter, C. Ullsperger, H. Hiasa, K. J. Marians and N. R. Cozzarelli: The structure of supercoiled intermediates in DNA replication. Cell, 94(6), 819-27 (1998). (Pubitemid 28436013)
108. J. Kato, Y. Nishimura, M. Yamada, H. Suzuki and Y. Hirota: Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli. J Bacteriol, 170(9), 3967-77 (1988).
109. O. Espeli, C. Levine, H. Hassing and K. J. Marians: Temporal regulation of topoisomerase IV activity in E. coli. Mol Cell, 11(1), 189-201 (2003). (Pubitemid 36126600)