Mechanisms for chromosome segregation

Current Opinion in Microbiology

Volumn 22, Issue , 2014, Pages 60-65

  Bouet, Jean Yves ^a,b   Stouf, Mathieu ^c   Lebailly, Elise ^a,b   Cornet, François ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL DNA;

BACTERIAL CHROMOSOME; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CENTROMERE; CHROMATID; CHROMOSOME SEGREGATION; CONFORMATIONAL TRANSITION; DNA BINDING; DNA REPLICATION ORIGIN; INTRACELLULAR SPACE; METHYLATION; NONHUMAN; PLASMID; POLYMERIZATION; REPLICON; REVIEW; SPOROGENESIS; BACTERIUM; GENETICS; METABOLISM;

BACTERIA; CELL DIVISION; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; PLASMIDS; REPLICATION ORIGIN;

EID: 84907960269     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.09.013     Document Type: Review

References (85)

1. Niki H., Yamaichi Y., Hiraga S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 2000, 14:212-223.
2. Bates D., Kleckner N. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 2005, 121:899-911.
3. Nielsen H.J., Li Y., Youngren B., Hansen F.G., Austin S. Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 2006, 61:383-393.
4. Wang X., Liu X., Possoz C., Sherratt D.J. The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 2006, 20:1727-1731.
5. Viollier P.H., Thanbichler M., McGrath P.T., West L., Meewan M., McAdams H.H., Shapiro L. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA 2004, 101:9257-9262.
6. Youngren B., Nielsen H.J., Jun S., Austin S. The multifork Escherichia coli chromosome is a self-duplicating and self-segregating thermodynamic ring polymer. Genes Dev 2014, 28:71-84.
7. Adachi S., Fukushima T., Hiraga S. Dynamic events of sister chromosomes in the cell cycle of Escherichia coli. Genes Cells 2008, 13:181-197.
8. Joshi M.C., Magnan D., Montminy T.P., Lies M., Stepankiw N., Bates D. Regulation of sister chromosome cohesion by the replication fork tracking protein SeqA. PLoS Genet 2013, 9:e1003673.
9. Danilova O., Reyes-Lamothe R., Pinskaya M., Sherratt D., Possoz C. MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 2007, 65:1485-1492.
10. Wang X., Reyes-Lamothe R., Sherratt D.J. Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev 2008, 22:2426-2433.
11. Lesterlin C., Gigant E., Boccard F., Espéli O. Sister chromatid interactions in bacteria revealed by a site-specific recombination assay. EMBO J 2012, 31:3468-3479.
12. Joshi M.C., Bourniquel A., Fisher J., Ho B.T., Magnan D., Kleckner N., Bates D. Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci USA 2011, 108:2765-2770.
13. Vallet-Gely I., Boccard F. Chromosomal organization and segregation in Pseudomonas aeruginosa. PLoS Genet 2013, 9:e1003492.
14. Wang X., Possoz C., Sherratt D.J. Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev 2005, 19:2367-2377.
15. Lesterlin C., Pages C., Dubarry N., Dasgupta S., Cornet F. Asymmetry of chromosome replichores renders the DNA translocase activity of FtsK essential for cell division and cell shape maintenance in Escherichia coli. PLoS Genet 2008, 4:e1000288.
16. Jun S., Mulder B. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 2006, 103:12388-12393.
17. Wiggins P.A., Cheveralls K.C., Martin J.S., Lintner R., Kondev J. Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. Proc Natl Acad Sci USA 2010, 107:4991-4995.
18. Junier I., Boccard F., Espéli O. Polymer modeling of the E. coli genome reveals the involvement of locus positioning and macrodomain structuring for the control of chromosome conformation and segregation. Nucleic Acids Res 2013, 10.1093/nar/gkt1005.
19. Pelletier J., Halvorsen K., Ha B.-Y., Paparcone R., Sandler S.J., Woldringh C.L., Wong W.P., Jun S. Physical manipulation of the Escherichia coli chromosome reveals its soft nature. Proc Natl Acad Sci USA 2012, 109:E2649-E2656.
20. Valens M., Penaud S., Rossignol M., Cornet F., Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J 2004, 23:4330-4341.
21. Fisher J.K., Bourniquel A., Witz G., Weiner B., Prentiss M., Kleckner N. Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell 2013, 153:882-895.
22. Salje J. Plasmid segregation: how to survive as an extra piece of DNA. Crit Rev Biochem Mol Biol 2010, 45:296-317.
23. Godfrin-Estevenon A.M., Pasta F., Lane D. The parAB gene products of Pseudomonas putida exhibit partition activity in both P. putida and Escherichia coli. Mol Microbiol 2002, 43:39-49.
24. Ireton K., Gunther N.W., Grossman A.D. spoOJ is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 1994, 176:5320-5329.
25. Yamaichi Y., Fogel M.A., Waldor M.K. par genes and the pathology of chromosome loss in Vibrio cholerae. Proc Natl Acad Sci USA 2007, 104:630-635.
26. Passot F.M., Calderon V., Fichant G., Lane D., Pasta F. Centromere binding and evolution of chromosomal partition systems in the Burkholderiales. J Bacteriol 2012, 194:3426-3436.
27. Lin D.C.-H., Grossman A.D. Identification and characterization of a bacterial chromosome partitioning site. Cell 1998, 92:675-685.
28. Yamaichi Y., Niki H. Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc Natl Acad Sci USA 2000, 97:14656-14661.
29. Fogel M.A., Waldor M.K. Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 2005, 55:125-136.
30. Webb C.D., Teleman A., Gordon S., Straight A., Belmont A., Lin D.C.-H., Grossman A.D., Wright A., Losick R. Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell 1997, 88:667-674.
31. Gordon G.S., Sitnikov D., Webb C.D., Teleman A., Straight A., Losick R., Murray A.W., Wright A. Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 1997, 90:1113-1121.
32. Niki H., Hiraga S. Subcellular distribution of actively partitioning F plasmid during the cell division cycle in E. coli. Cell 1997, 90:951-957.
33. Fogel M.A., Waldor M.K. A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 2006, 20:3269-3282.
34. Bowman G.R., Comolli L.R., Zhu J., Eckart M., Koenig M., Downing K.H., Moerner W.E., Earnest T., Shapiro L. A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 2008, 134:945-955.
35. Harms A., Treuner-Lange A., Schumacher D., Sogaard-Andersen L. Tracking of chromosome and replisome dynamics in Myxococcus xanthus reveals a novel chromosome arrangement. PLoS Genet 2013, 9:e1003802.
36. Livny J., Yamaichi Y., Waldor M.K. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 2007, 189:8693-8703.
37. Toro E., Hong S.H., McAdams H.H., Shapiro L. Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc Natl Acad Sci USA 2008, 105:15435-15440.
38. Sanchez A., Rech J., Gasc C., Bouet J.Y. Insight into centromere-binding properties of ParB proteins: a secondary binding motif is essential for bacterial genome maintenance. Nucleic Acids Res 2013, 41:3094-3103.
39. Pillet F., Sanchez A., Lane D., Anton Leberre V., Bouet J.Y. Centromere binding specificity in assembly of the F plasmid partition complex. Nucleic Acids Res 2011, 39:7477-7486.
40. Bouet J.Y., Rech J., Egloff S., Biek D.P., Lane D. Probing plasmid partition with centromere-based incompatibility. Mol Microbiol 2005, 55:511-525.
41. Funnell B.E., Gagnier L. P1 plasmid partition: binding of P1 ParB protein and Escherichia coli integration host factor to altered parS sites. Biochimie 1994, 76:924-932.
42. Graham T.G., Wang X., Song D., Etson C.M., van Oijen A.M., Rudner D.Z., Loparo J.J. ParB spreading requires DNA bridging. Genes Dev 2014, 28:1228-1238.
43. Lynch A.S., Wang J.C. SopB protein-meditated silencing of genes linked to the sopC locus of Escherichia coli F plasmid. Proc Natl Acad Sci USA 1995, 92:1896-1900.
44. Murray H., Ferreira H., Errington J. The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 2006, 61:1352-1361.
45. Rodionov O., Lobocka M., Yarmolinsky M. Silencing of genes flanking the P1 plasmid centromere. Science 1999, 283:546-549.
46. Broedersz C.P., Wang X., Meir Y., Loparo J.J., Rudner D.Z., Wingreen N.S. Condensation and localization of the partitioning protein ParB on the bacterial chromosome. Proc Natl Acad Sci USA 2014, 111:8809-8814.
47. Watanabe E., Wachi M., Yamasaki M., Nagai K. ATPase activity of SopA, a protein essential for active partitioning of F plasmid. Mol Gen Genet 1992, 234:346-352.
48. Davis M.A., Martin K.A., Austin S.J. Biochemical activities of the parA partition protein of the P1 plasmid. Mol Microbiol 1992, 6:1141-1147.
49. Ah-Seng Y., Lopez F., Pasta F., Lane D., Bouet J.-Y. Dual role of DNA in regulating ATP hydrolysis by the SopA partition protein. J Biol Chem 2009, 284:30067-30075.
50. Ah-Seng Y., Rech J., Lane D., Bouet J.Y. Defining the role of ATP hydrolysis in mitotic segregation of bacterial plasmids. PLoS Genet 2013, 9:e1003956.
51. Murray H., Errington J. Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 2008, 135:74-84.
52. Gruber S., Errington J. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 2009, 137:685-696.
53. Gruber S., Veening J.-W., Bach J., Blettinger M., Bramkamp M., Errington J. Interlinked sister chromosomes arise in the absence of condensin during fast replication in B. subtilis. Curr Biol 2014, 24:293-298.
54. Wang X., Tang O.W., Riley E.P., Rudner D.Z. The SMC condensin complex is required for origin segregation in Bacillus subtilis. Curr Biol 2014, 24:287-292.
55. Vecchiarelli A.G., Mizuuchi K., Funnell B.E. Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 2012, 86:513-523.
56. Davey M.J., Funnell B.E. Modulation of the P1 plasmid partition protein ParA by ATP, ADP, and P1 ParB. J Biol Chem 1997, 272:15286-15292.
57. Bouet J.Y., Funnell B.E. P1 ParA interacts with the P1 partition complex at parS and an ATP-ADP switch controls ParA activities. EMBO J 1999, 18:1415-1424.
58. Fung E., Bouet J.Y., Funnell B.E. Probing the ATP-binding site of P1 ParA: partition and repression have different requirements for ATP binding and hydrolysis. EMBO J 2001, 20:4901-4911.
59. Barillà D., Rosenberg M.F., Nobbmann U., Hayes F. Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J 2005, 24:1453-1464.
60. Bouet J.Y., Ah-Seng Y., Benmeradi N., Lane D. Polymerization of SopA partition ATPase: regulation by DNA binding and SopB. Mol Microbiol 2007, 63:468-481.
61. Hui M.P., Galkin V.E., Yu X., Stasiak A.Z., Stasiak A., Waldor M.K., Egelman E.H. ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci USA 2010, 107:4590-4595.
62. Ptacin J.L., Lee S.F., Garner E.C., Toro E., Eckart M., Comolli L.R., Moerner W.E., Shapiro L. A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 2010, 12:791-798.
63. Castaing J.P., Bouet J.Y., Lane D. F plasmid partition depends on interaction of SopA with non-specific DNA. Mol Microbiol 2008, 70:1000-1011.
64. Hester C.M., Lutkenhaus J. Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 2007, 104:20326-20331.
65. Vecchiarelli A.G., Han Y.W., Tan X., Mizuuchi M., Ghirlando R., Biertumpfel C., Funnell B.E., Mizuuchi K. ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 2010, 78:78-91.
66. Ringgaard S., van Zon J., Howard M., Gerdes K. Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 2009, 106:19369-19374.
67. Hwang L.C., Vecchiarelli A.G., Han Y.W., Mizuuchi M., Harada Y., Funnell B.E., Mizuuchi K. ParA-mediated plasmid partition driven by protein pattern self-organization. EMBO J 2013, 10.1038/emboj.2013.34.
68. Vecchiarelli A.G., Neuman K.C., Mizuuchi K. A propagating ATPase gradient drives transport of surface-confined cellular cargo. Proc Natl Acad Sci USA 2014, 111:4880-4885.
69. Lim H.C., Surovtsev I.V., Beltran B.G., Huang F., Bewersdorf J., Jacobs-Wagner C. Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. eLife 2014, 10.7554/eLife.02758.
70. Reyes-Lamothe R., Possoz C., Danilova O., Sherratt D.J. Independent positioning and action of Escherichia coli replisomes in live cells. Cell 2008, 133:90-102.
71. Stouf M., Meile J.-C., Cornet F. FtsK actively segregates sister chromosomes in Escherichia coli. Proc Natl Acad Sci USA 2013, 110:11157-11162.
72. Mercier R., Petit M.-A., Schbath S., Robin S., Karoui El M., Boccard F., Espéli O. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 2008, 135:475-485.
73. Dupaigne P., Tonthat N.K., Espéli O., Whitfill T., Boccard F., Schumacher M.A. Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell 2012, 48:560-571.
74. Espéli O., Borne R., Dupaigne P., Thiel A., Gigant E., Mercier R., Boccard F. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 2012, 31:3198-3211.
75. Sherratt D.J., Arciszewska L.K., Crozat E., Graham J.E., Grainge I. The Escherichia coli DNA translocase FtsK. Biochem Soc Trans 2010, 38:395-398.
76. Massey T.H., Mercogliano C.P., Yates J., Sherratt D.J., Löwe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 2006, 23:457-469.
77. Deghorain M., Pages C., Meile J.-C., Stouf M., Capiaux H., Mercier R., Lesterlin C., Hallet B., Cornet F. A defined terminal region of the E. coli chromosome shows late segregation and high FtsK activity. PLoS ONE 2011, 6:e22164.
78. Graham J.E., Sivanathan V., Sherratt D.J., Arciszewska L.K. FtsK translocation on DNA stops at XerCD-dif. Nucleic Acids Res 2010, 38:72-81.
79. Marquis K.A., Burton B.M., Nöllmann M., Ptacin J.L., Bustamante C., Ben-Yehuda S., Rudner D.Z. SpoIIIE strips proteins off the DNA during chromosome translocation. Genes Dev 2008, 22:1786-1795.
80. Bigot S., Saleh O.A., Lesterlin C., Pages C., Karoui El M., Dennis C., Grigoriev M., Allemand J.-F., Barre F.-X., Cornet F. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 2005, 24:3770-3780.
81. Levy O., Ptacin J.L., Pease P.J., Gore J., Eisen M.B., Bustamante C., Cozzarelli N.R. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci USA 2005, 102:17618-17623.
82. Diagne C.T., Salhi M., Crozat E., Salomé L., Cornet F., Rousseau P., Tardin C. TPM analyses reveal that FtsK contributes both to the assembly and the activation of the XerCD-dif recombination synapse. Nucleic Acids Res 2013, 10.1093/nar/gkt1024.
83. Zawadzki P., May P.F.J., Baker R.A., Pinkney J.N.M., Kapanidis A.N., Sherratt D.J., Arciszewska L.K. Conformational transitions during FtsK translocase activation of individual XerCD-dif recombination complexes. Proc Natl Acad Sci USA 2013, 110:17302-17307.
84. Fiche J.-B., Cattoni D.I., Diekmann N., Langerak J.M., Clerte C., Royer C.A., Margeat E., Doan T., Nöllmann M. Recruitment, assembly, and molecular architecture of the SpoIIIE DNA pump revealed by superresolution microscopy. PLoS Biol 2013, 11:e1001557.
85. Bisicchia P., Steel B., Mariam Debela M.H., Löwe J., Sherratt D. The N-terminal membrane-spanning domain of the Escherichia coli DNA translocase FtsK hexamerizes at midcell. MBio 2013, 4:e00800-e813.