DNA compaction in the early part of the SOS response is dependent on RecN and RecA

Microbiology (United Kingdom)

Volumn 160, Issue PART 5, 2014, Pages 872-882

  Odsbu, Ingvild ^a   Skarstad, Kirsten ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

RECA PROTEIN; RECN PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; DNA DEGRADATION; DNA RECOMBINATION; DNA REPAIR; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; ULTRAVIOLET IRRADIATION;

EID: 84899143807     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.075051-0     Document Type: Article

References (74)

1. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L. & Mori, H. (2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 0008.
2. Blanco, M., Herrera, G., Collado, P., Rebollo, J. E. & Botella, L. M. (1982). Influence of RecA protein on induced mutagenesis. Biochimie 64, 633-636.
3. Branzei, D. & Foiani, M. (2010). Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11, 208-219.
4. 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.
5. Cazaux, C., Larminat, F. & Defais, M. (1991). Site-directed mutagenesis in the Escherichia coli recA gene. Biochimie 73, 281-284.
6. Clark, A. J. (1973). Recombination deficient mutants of E. coli and other bacteria. Annu Rev Genet 7, 67-86.
7. Clark, D. J. & Maaløe, O. (1967). DNA replication and the division cycle in Escherichia coli. J Mol Biol 23, 99-112.
8. Courcelle, J., Khodursky, A., Peter, B., Brown, P. O. & Hanawalt, P. C. (2001). Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158, 41-64.
9. Courcelle, C. T., Belle, J. J. & Courcelle, J. (2005). Nucleotide excision repair or polymerase V-mediated lesion bypass can act to restore UVarrested replication forks in Escherichia coli. J Bacteriol 187, 6953-6961.
10. Devoret, R., Pierre, M. & Moreau, P. L. (1983). Prophage phi 80 is induced in Escherichia coli K12 recA430. Mol Gen Genet 189, 199-206.
11. Dewitt, S. K. & Adelberg, E. A. (1962). The occurrence of a genetic transposition in a strain of Escherichia coli. Genetics 47, 577-585.
12. Dutreix, M., Bailone, A. & Devoret, R. (1985). Efficiency of induction of prophage lambda mutants as a function of recA alleles. J Bacteriol 161, 1080-1085.
13. Fernández De Henestrosa, A. R., Ogi, T., Aoyagi, S., Chafin, D., Hayes, J. J., Ohmori, H. & Woodgate, R. (2000). Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35, 1560-1572.
14. 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.
15. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A. & Ellenberger, T. (2006). DNA Repair and Mutagenesis, 2nd edn. Washington, DC: American Society for Microbiology.
16. Graumann, P. L. & Knust, T. (2009). Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res 17, 265-275.
17. Grove, J. I., Wood, S. R., Briggs, G. S., Oldham, N. J. & Lloyd, R. G. (2009). A soluble RecN homologue provides means for biochemical and genetic analysis of DNA double-strand break repair in Escherichia coli. DNA Repair (Amst) 8, 1434-1443.
18. Hegde, S., Sandler, S. J., Clark, A. J. & Madiraju, M. V. (1995). recO and recR mutations delay induction of the SOS response in Escherichia coli. Mol Gen Genet 246, 254-258.
19. Heller, R. C. & Marians, K. J. (2006). Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7, 932-943.
20. Hendricks, E. C., Szerlong, H., Hill, T. & Kuempel, P. (2000). Cell division, guillotining of dimer chromosomes and SOS induction in resolution mutants (dif, xerC and xerD) of Escherichia coli. Mol Microbiol 36, 973-981.
21. Hiraga, S., Ichinose, C., Niki, H. & Yamazoe, M. (1998). Cell cycledependent duplication and bidirectional migration of SeqA-associated DNA-protein complexes in E. coli. Mol Cell 1, 381-387.
22. Hiraga, S., Ichinose, C., Onogi, T., Niki, H. & Yamazoe, M. (2000). Bidirectional migration of SeqA-bound hemimethylated DNA clusters and pairing of oriC copies in Escherichia coli. Genes Cells 5, 327-341.
23. Hirano, T. (2005). SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360, 507-514.
24. Kidane, D., Sanchez, H., Alonso, J. C. & Graumann, P. L. (2004). Visualization of DNA double-strand break repair in live bacteria reveals dynamic recruitment of Bacillus subtilis RecF, RecO and RecN proteins to distinct sites on the nucleoids. Mol Microbiol 52, 1627-1639.
25. Kowalczykowski, S. C. & Krupp, R. A. (1989). Biochemical events essential to the recombination activity of Escherichia coli RecA protein. II. Co-dominant effects of RecA142 protein on wild-type RecA protein function. J Mol Biol 207, 735-747.
26. Kowalczykowski, S. C., Burk, D. L. & Krupp, R. A. (1989). Biochemical events essential to the recombination activity of Escherichia coli RecA protein. I. Properties of the mutant RecA142 protein. J Mol Biol 207, 719-733.
27. Kuzminov, A. (1995). Collapse and repair of replication forks in Escherichia coli. Mol Microbiol 16, 373-384.
28. Kuzminov, A. (1999). Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63, 751-813.
29. Levin-Zaidman, S., Frenkiel-Krispin, D., Shimoni, E., Sabanay, I., Wolf, S. G. & Minsky, A. (2000). Ordered intracellular RecA-DNA assemblies: a potential site of in vivo RecA-mediated activities. Proc Natl Acad Sci U S A 97, 6791-6796.
30. Lloyd, R. G., Picksley, S. M. & Prescott, C. (1983). Inducible expression of a gene specific to the RecF pathway for recombination in Escherichia coli K12. Mol Gen Genet 190, 162-167.
31. Lukas, C., Bartek, J. & Lukas, J. (2005). Imaging of protein movement induced by chromosomal breakage: tiny 'local' lesions pose great 'global' challenges. Chromosoma 114, 146-154.
32. Mašek, F., Skorvaga, M. & Sedliaková, M. (1989). Repression of damage-inducible (din) genes by the lexA3 mutation or by plasmid carrying the lexA gene; effect on pyrimidine dimer excision in UVirradiated Escherichia coli. Gene 78, 195-199.
33. McGlynn, P. & Lloyd, R. G. (2002). Recombinational repair and restart of damaged replication forks. Nat Rev Mol Cell Biol 3, 859-870.
34. McGlynn, P., Lloyd, R. G. & Marians, K. J. (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. Proc Natl Acad Sci U S A 98, 8235-8240.
35. McGrew, D. A. & Knight, K. L. (2003). Molecular design and functional organization of the RecA protein. Crit Rev Biochem Mol Biol 38, 385-432.
36. Meddows, T. R., Savory, A. P., Grove, J. I., Moore, T. & Lloyd, R. G. (2005). RecN protein and transcription factor DksA combine to promote faithful recombinational repair of DNA double-strand breaks. Mol Microbiol 57, 97-110.
37. Michel, B., Grompone, G., Florès, M. J. & Bidnenko, V. (2004). Multiple pathways process stalled replication forks. Proc Natl Acad Sci U S A 101, 12783-12788.
38. Misteli, T. & Soutoglou, E. (2009). The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 10, 243-254.
39. Molina, F. & Skarstad, K. (2004). Replication fork and SeqA focus distributions in Escherichia coli suggest a replication hyperstructure dependent on nucleotide metabolism. Mol Microbiol 52, 1597-1612.
40. Morigen, O., Odsbu, I. & Skarstad, K. (2009). Growth rate dependent numbers of SeqA structures organize the multiple replication forks in rapidly growing Escherichia coli. Genes Cells 14, 643-657.
41. Morimatsu, K. & Kowalczykowski, S. C. (2003). RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol Cell 11, 1337-1347.
42. Nagashima, K., Kubota, Y., Shibata, T., Sakaguchi, C., Shinagawa, H. & Hishida, T. (2006). Degradation of Escherichia coli RecN aggregates by ClpXP protease and its implications for DNA damage tolerance. J Biol Chem 281, 30941-30946.
43. Neher, S. B., Villén, J., Oakes, E. C., Bakalarski, C. E., Sauer, R. T., Gygi, S. P. & Baker, T. A. (2006). Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol Cell 22, 193-204.
44. Norris, V., den Blaauwen, T., Cabin-Flaman, A., Doi, R. H., Harshey, R., Janniere, L., Jimenez-Sanchez, A., Jin, D. J., Levin, P. A. & other authors (2007). Functional taxonomy of bacterial hyperstructures. Microbiol Mol Biol Rev 71, 230-253.
45. Odsbu, I., Morigen, O. & Skarstad, K. (2009). A reduction in ribonucleotide reductase activity slows down the chromosome replication fork but does not change its localization. PLoS ONE 4, e7617.
46. 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.
47. Opperman, T., Murli, S., Smith, B. T. & Walker, G. C. (1999). A model for a umuDC-dependent prokaryotic DNA damage checkpoint. Proc Natl Acad Sci U S A 96, 9218-9223.
48. Peters, J. M. & Nishiyama, T. (2012). Sister chromatid cohesion. Cold Spring Harb Perspect Biol 4, a011130.
49. Picksley, S. M., Attfield, P. V. & Lloyd, R. G. (1984). Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product. Mol Gen Genet 195, 267-274.
50. Pruteanu, M. & Baker, T. A. (2009). Proteolysis in the SOS response and metal homeostasis in Escherichia coli. Res Microbiol 160, 677-683.
51. Reyes, E. D., Patidar, P. L., Uranga, L. A., Bortoletto, A. S. & Lusetti, S. L. (2010). RecN is a cohesin-like protein that stimulates intermolecular DNA interactions in vitro. J Biol Chem 285, 16521-16529.
52. Roberts, J. W. & Roberts, C. W. (1981). Two mutations that alter the regulatory activity of E. coli recA protein. Nature 290, 422-424.
53. Rudolph, C. J., Upton, A. L. & Lloyd, R. G. (2007). Replication fork stalling and cell cycle arrest in UV-irradiated Escherichia coli. Genes Dev 21, 668-681.
54. Rupp, W. D. & Howard-Flanders, P. (1968). Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J Mol Biol 31, 291-304.
55. Sassanfar, M. & Roberts, J. W. (1990). Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol 212, 79-96.
56. Sedgwick, S. G. (1975). Genetic and kinetic evidence for different types of postreplication repair in Escherichia coli B. J Bacteriol 123, 154-161.
57. Shechter, N., Zaltzman, L., Weiner, A., Brumfeld, V., Shimoni, E., Fridmann-Sirkis, Y. & Minsky, A. (2013). Stress-induced condensation of bacterial genomes results in re-pairing of sister chromosomes: implications for double strand DNA break repair. J Biol Chem 288, 25659-25667.
58. Skarstad, K. & Boye, E. (1988). Perturbed chromosomal replication in recA mutants of Escherichia coli. J Bacteriol 170, 2549-2554.
59. Smith, B. T., Grossman, A. D. & Walker, G. C. (2002). Localization of UvrA and effect of DNA damage on the chromosome of Bacillus subtilis. J Bacteriol 184, 488-493.
60. Stokke, C., Flåtten, I. & Skarstad, K. (2012). An easy-to-use simulation program demonstrates variations in bacterial cell cycle parameters depending on medium and temperature. PLoS ONE 7, e30981.
61. Ström, L., Lindroos, H. B., Shirahige, K. & Sjögren, C. (2004). Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16, 1003-1015.
62. Tessman, E. S. & Peterson, P. K. (1985). Isolation of proteaseproficient, recombinase-deficient recA mutants of Escherichia coli K-12. J Bacteriol 163, 688-695.
63. Thoms, B. & Wackernagel, W. (1987). Regulatory role of recF in the SOS response of Escherichia coli: impaired induction of SOS genes by UV irradiation and nalidixic acid in a recF mutant. J Bacteriol 169, 1731-1736.
64. Torheim, N. K., Boye, E., Løbner-Olesen, A., Stokke, T. & Skarstad, K. (2000). The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37, 629-638.
65. Umezu, K. & Kolodner, R. D. (1994). Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNAbinding protein. J Biol Chem 269, 30005-30013.
66. Umezu, K., Chi, N. W. & Kolodner, R. D. (1993). Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc Natl Acad Sci U S A 90, 3875-3879.
67. Waldminghaus, T. & Skarstad, K. (2009). The Escherichia coli SeqA protein. Plasmid 61, 141-150.
68. 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.
69. Waleh, N. S. & Stocker, B. A. (1979). Effect of host lex, recA, recF, and uvrD genotypes on the ultraviolet light-protecting and related properties of plasmid R46 in Escherichia coli. J Bacteriol 137, 830-838.
70. Watrin, E. & Peters, J. M. (2006). Cohesin and DNA damage repair. Exp Cell Res 312, 2687-2693.
71. Weel-Sneve, R., Kristiansen, K. I., Odsbu, I., Dalhus, B., Booth, J., Rognes, T., Skarstad, K. & Bjørås, M. (2013). Single transmembrane peptide DinQ modulates membrane-dependent activities. PLoS Genet 9, e1003260.
72. Whitby, M. C. & Lloyd, R. G. (1995). Altered SOS induction associated with mutations in recF, recO and recR. Mol Gen Genet 246, 174-179.
73. Yamazoe, M., Adachi, S., Kanaya, S., Ohsumi, K. & Hiraga, S. (2005). Sequential binding of SeqA protein to nascent DNA segments at replication forks in synchronized cultures of Escherichia coli. Mol Microbiol 55, 289-298.
74. Zimmerman, S. B. (2006). Shape and compaction of Escherichia coli nucleoids. J Struct Biol 156, 255-261.