Regulation of Sister Chromosome Cohesion by the Replication Fork Tracking Protein SeqA

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Joshi, Mohan C ^a   Magnan, David ^a   Montminy, Timothy P ^a   Lies, Mark ^a   Stepankiw, Nicholas ^a,b   Bates, David ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE IV; REGULATOR PROTEIN; SEQA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BINDING AFFINITY; CELL ADHESION; CELL ASSAY; CELL JUNCTION; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DETERMINATION; DNA REPLICATION; EPISTASIS; ESCHERICHIA COLI; GENE LOCUS; GENETIC MANIPULATION; NONHUMAN; ORIC GENE; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQA GENE; SISTER CHROMATID; SNAP GENE; TOPO IV GENE;

BACTERIAL OUTER MEMBRANE PROTEINS; CHROMOSOME SEGREGATION; CHROMOSOMES; DNA REPLICATION; DNA TOPOISOMERASE IV; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ORIGIN RECOGNITION COMPLEX; PROTEIN BINDING; SISTER CHROMATID EXCHANGE;

EID: 84884621139     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003673     Document Type: Article

References (55)

1. Sunako Y, Onogi T, Hiraga S, (2001) Sister chromosome cohesion of Escherichia coli. Mol Microbiol 42: 1233-1241.
2. Bates D, Kleckner N, (2005) Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121: 899-911.
3. Nielsen HJ, Li Y, Youngren B, Hansen FG, Austin S, (2006) Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 61: 383-393.
4. Wang X, Reyes-Lamothe R, Sherratt DJ, (2008) Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev 22: 2426-2433.
5. Espeli O, Mercier R, Boccard F, (2008) DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68: 1418-1427.
6. Joshi MC, Bourniquel A, Fisher J, Ho BT, Magnan D, Kleckner N, Bates D, (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci U S A 108: 2765-2770.
7. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N, (2013) Four-Dimensional Imaging of E. coli Nucleoid Organization and Dynamics in Living Cells. Cell 153: 882-895.
8. Nasmyth K, Haering CH, (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525-558.
9. Gordon GS, Sitnikov D, Webb CD, Teleman A, Straight A, Losick R, Murray AW, Wright A, (1997) Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90: 1113-1121.
10. Danilova O, Reyes-Lamothe R, Pinskaya M, Sherratt D, Possoz C, (2007) 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: 1485-1492.
11. Lesterlin C, Gigant E, Boccard F, Espeli O, (2012) Sister chromatid interactions in bacteria revealed by a site-specific recombination assay. EMBO J 31: 3468-3479.
12. Deibler RW, Rahmati S, Zechiedrich EL, (2001) Topoisomerase IV, alone, unknots DNA in E. coli. Genes Dev 15: 748-761.
13. Espeli O, Levine C, Hassing H, Marians KJ, (2003) Temporal regulation of topoisomerase IV activity in E. coli. Mol Cell 11: 189-201.
14. Khodursky AB, Peter BJ, Schmid MB, DeRisi J, Botstein D, Brown PO, Cozzarelli NR, (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci U S A 97: 9419-9424.
15. Postow L, Crisona NJ, Peter BJ, Hardy CD, Cozzarelli NR, (2001) Topological challenges to DNA replication: conformations at the fork. Proc Natl Acad Sci U S A 98: 8219-8226.
16. Lopez V, Martinez-Robles ML, Hernandez P, Krimer DB, Schvartzman JB, (2012) Topo IV is the topoisomerase that knots and unknots sister duplexes during DNA replication. Nucleic Acids Res 40: 3563-3573.
17. Petrushenko ZM, She W, Rybenkov VV, (2011) A new family of bacterial condensins. Mol Microbiol 81: 881-896.
18. Johnson RC, Johnson LM, Schmidt JW, Gardner JF (2005) Major nucleoid proteins in the structure and function of the Eschrichia coli chromosome. In: Higgins NP, editor. The Bacterial Chromosome. Washington, D.C.: ASM Press. pp. 65-132.
19. Brendler T, Sawitzke J, Sergueev K, Austin S, (2000) A case for sliding SeqA tracts at anchored replication forks during Escherichia coli chromosome replication and segregation. EMBO J 19: 6249-6258.
20. Lu M, Campbell JL, Boye E, Kleckner N, (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77: 413-426.
21. Campbell JL, Kleckner N, (1990) E. coli oriC and the dnaA gene promoter are sequestered from Dam methyltransferase following the passage of the chromosomal replication fork. Cell 62: 967-979.
22. Onogi T, Niki H, Yamazoe M, Hiraga S, (1999) The assembly and migration of SeqA-Gfp fusion in living cells of Escherichia coli. Mol Microbiol 31: 1775-1782.
23. Odsbu I, Klungsoyr HK, Fossum S, Skarstad K, (2005) Specific N-terminal interactions of the Escherichia coli SeqA protein are required to form multimers that restrain negative supercoils and form foci. Genes Cells 10: 1039-1049.
24. Kang S, Han JS, Park JH, Skarstad K, Hwang DS, (2003) SeqA protein stimulates the relaxing and decatenating activities of topoisomerase IV. J Biol Chem 278: 48779-48785.
25. Hayama R, Marians KJ, (2010) Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc Natl Acad Sci U S A 107: 18826-18831.
26. Li Y, Stewart NK, Berger AJ, Vos S, Schoeffler AJ, Berger JM, Chait BT, Oakley MG, (2010) Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc Natl Acad Sci U S A 107: 18832-18837.
27. Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H, (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63: 393-404.
28. Zechiedrich EL, Cozzarelli NR, (1995) Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. Genes Dev 9: 2859-2869.
29. Bates D, Epstein J, Boye E, Fahrner K, Berg H, Kleckner N, (2005) The Escherichia coli baby cell column: a novel cell synchronization method provides new insight into the bacterial cell cycle. Mol Microbiol 57: 380-391.
30. Stepankiw N, Kaidow A, Boye E, Bates D, (2009) The right half of the Escherichia coli replication origin is not essential for viability, but facilitates multi-forked replication. Mol Microbiol 74: 467-479.
31. Waldminghaus T, Skarstad K, (2010) ChIP on Chip: surprising results are often artifacts. BMC Genomics 11: 414.
32. Sanchez-Romero MA, Busby SJ, Dyer NP, Ott S, Millard AD, Grainger DC, (2010) Dynamic Distribution of SeqA Protein across the Chromosome of Escherichia coli K-12. mBio 1: e00012-10.
33. Lobner-Olesen A, Marinus MG, Hansen FG, (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci U S A 100: 4672-4677.
34. Elmore S, Muller M, Vischer N, Odijk T, Woldringh CL, (2005) Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli. J Struct Biol 151: 275-287.
35. Peter BJ, Ullsperger C, Hiasa H, Marians KJ, Cozzarelli NR, (1998) The structure of supercoiled intermediates in DNA replication. Cell 94: 819-827.
36. Fossum S, Crooke E, Skarstad K, (2007) Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26: 4514-4522.
37. Guarne A, Brendler T, Zhao Q, Ghirlando R, Austin S, Yang W, (2005) Crystal structure of a SeqA-N filament: implications for DNA replication and chromosome organization. EMBO J 24: 1502-1511.
38. Bach T, Krekling MA, Skarstad K, (2003) Excess SeqA prolongs sequestration of oriC and delays nucleoid segregation and cell division. EMBO J 22: 315-323.
39. Waldminghaus T, Weigel C, Skarstad K, (2012) Replication fork movement and methylation govern SeqA binding to the Escherichia coli chromosome. Nucleic Acids Res 40: 5465-5476.
40. Liu Z, Zechiedrich L, Chan HS, (2010) Action at hooked or twisted-hooked DNA juxtapositions rationalizes unlinking preference of type-2 topoisomerases. J Mol Biol 400: 963-982.
41. Farcas AM, Uluocak P, Helmhart W, Nasmyth K, (2011) Cohesin's concatenation of sister DNAs maintains their intertwining. Mol Cell 44: 97-107.
42. Weitao T, Nordstrom K, Dasgupta S, (1999) Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. Mol Microbiol 34: 157-168.
43. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592-12597.
44. Slater S, Wold S, Lu M, Boye E, Skarstad K, et al. (1995) E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82: 927-936.
45. Ferullo DJ, Lovett ST, (2008) The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet 4: e1000300.
46. Norris V, Fralick J, Danchin A, (2000) A SeqA hyperstructure and its interactions direct the replication and sequestration of DNA. Mol Microbiol 37: 696-702.
47. Kouzminova EA, Rotman E, Macomber L, Zhang J, Kuzminov A, (2004) RecA-dependent mutants in Escherichia coli reveal strategies to avoid chromosomal fragmentation. Proc Natl Acad Sci U S A 101: 16262-16267.
48. Hansen FG, von Meyenburg K, (1979) Characterization of the dnaA, gyrB and other genes in the dnaA region of the Escherichia coli chromosome on specialized transducing phages lambda tna. Mol Gen Genet 175: 135-144.
49. Marinus MG, Carraway M, Frey AZ, Brown L, Arraj JA, (1983) Insertion mutations in the dam gene of Escherichia coli K-12. Mol Gen Genet 192: 288-289.
50. Huisman O, Faelen M, Girard D, Jaffe A, Toussaint A, et al. (1989) Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol 171: 3704-3712.
51. Yamazoe M, Onogi T, Sunako Y, Niki H, Yamanaka K, et al. (1999) Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 18: 5873-5884.
52. Johnson RC, Ball CA, Pfeffer D, Simon MI, (1988) Isolation of the gene encoding the Hin recombinational enhancer binding protein. Proc Natl Acad Sci U S A 85: 3484-3488.
53. Von Freiesleben U, Rasmussen KV, Atlung T, Hansen FG, (2000) Rifampicin-resistant initiation of chromosome replication from oriC in ihf mutants. Mol Microbiol 37: 1087-1093.
54. Lau IF, Filipe SR, Soballe B, Okstad OA, Barre FX, et al. (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol 49: 731-743.
55. Cronan JE, (2006) A family of arabinose-inducible Escherichia coli expression vectors having pBR322 copy control. Plasmid 55: 152-157.