A soluble RecN homologue provides means for biochemical and genetic analysis of DNA double-strand break repair in Escherichia coli

DNA Repair

Volumn 8, Issue 12, 2009, Pages 1434-1443

  Grove, Jane I ^a   Wood, Stuart R ^a   Briggs, Geoffrey S ^a   Oldham, Neil J ^a   Lloyd, Robert G ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

ATPase; DNA binding; I SceI; SMC; SOS response

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GENOMIC DNA; KANAMYCIN; MITOMYCIN C; RECN PROTEIN;

AQUIFEX AEOLICUS; ARTICLE; BACILLUS SUBTILIS; BACTEROIDES FRAGILIS; DNA BINDING; DNA REPAIR; DNA STRAND BREAKAGE; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; GAMMA IRRADIATION; HAEMOPHILUS INFLUENZAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; THERMOTOGA MARITIMA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA RESTRICTION ENZYMES; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY;

AQUIFEX; AQUIFEX AEOLICUS; BACILLUS SUBTILIS; BACTEROIDES FRAGILIS; ESCHERICHIA COLI; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE;

EID: 70450223126     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.09.015     Document Type: Article

References (57)

1. Kowalczykowski S.C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25 (2000) 156-165
2. Singleton M.R., Dillingham M.S., Gaudier M., Kowalczykowski S.C., and Wigley D.B. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432 (2004) 187-193
3. Marians K.J. PriA-directed replication fork restart in Escherichia coli. Trends Biochem. Sci. 25 (2000) 185-189
4. Meddows T.R., Savory A.P., and Lloyd R.G. RecG helicase promotes DNA double-strand break repair. Mol. Microbiol. 52 (2004) 119-132
5. Grove J.I., Harris L., Buckman C., and Lloyd R.G. DNA double strand break repair and crossing over mediated by RuvABC resolvase and RecG translocase. DNA Repair (Amst) 7 (2008) 1517-1530
6. Picksley S.M., Attfield P.V., and Lloyd R.G. Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product. Mol. Gen. Genet. 195 (1984) 267-274
7. Finch P.W., Chambers P., and Emmerson P.T. Identification of the E. coli recN gene product as a major SOS protein. J. Bacteriol. 164 (1985) 653-658
8. Sargentini N.J., and Smith K.C. Characterization of an Escherichia coli mutant (radB101) sensitive to gamma and UV radiation, and methyl methanesulfonate. Radiat. Res. 93 (1983) 461-478
9. Lloyd R.G., Picksley S.M., and Prescott C. Inducible expression of a gene specific to the RecF pathway for recombination in Escherichia coli K12. Mol. Gen. Genet. 190 (1983) 162-167
10. Meddows T.R., Savory A.P., Grove J.I., Moore T., and Lloyd R.G. RecN protein and transcription factor DksA combine to promote faithful recombinational repair of DNA double-strand breaks. Mol. Microbiol. 57 (2005) 97-110
11. Rostas K., Morton S.J., Picksley S.M., and Lloyd R.G. Nucleotide sequence and LexA regulation of the Escherichia coli recN gene. Nucleic Acids Res. 15 (1987) 5041-5049
12. Picksley S.M., Lloyd R.G., and Buckman C. Genetic analysis and regulation of inducible recombination in Escherichia coli K-12. Cold Spring Harbor Symp. Quant. Biol. 49 (1984) 469-474
13. Courcelle J., Khodursky A., Peter B., Brown P.O., and Hanawalt P.C. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158 (2001) 41-64
14. Nagashima K., Kubota Y., Shibata T., Sakaguchi C., Shinagawa H., and Hishida T. Degradation of Escherichia coli RecN aggregates by ClpXP protease and its implications for DNA damage tolerance. J. Biol. Chem. 281 (2006) 30941-30946
15. Dunman P.M., Ren L., Rahman M.S., Palejwala V.A., Murphy H.S., Volkert M.R., and Humayun M.Z. Escherichia coli cells defective for the recN gene display constitutive elevation of mutagenesis at 3,N(4)-ethenocytosine via an SOS-induced mechanism. Mol. Microbiol. 37 (2000) 680-686
16. Simic D., Vukovic-Gacic B., Ajanovic A., and Knezevic-Vukcevic J. Activation of RecA protein in recombination-deficient strains of Escherichia coli following DNA-damaging treatments. Mutat. Res. 254 (1991) 255-262
17. Zeigler D.R. Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int. J. Syst. Evol. Microbiol. 53 (2003) 1893-1900
18. Sweetman W.A., Moxon E.R., and Bayliss C.D. Induction of the SOS regulon of Haemophilus influenzae does not affect phase variation rates at tetranucleotide or dinucleotide repeats. Microbiology 151 (2005) 2751-2763
19. Alonso J.C., Stiege A.C., and Luder G. Genetic recombination in Bacillus subtilis 168: effect of recN, recF, recH and addAB mutations on DNA repair and recombination. Mol. Gen. Genet. 239 (1993) 129-136
20. Sanchez H., Kidane D., Castillo Cozar M., Graumann P.L., and Alonso J.C. Recruitment of Bacillus subtilis RecN to DNA double-strand breaks in the absence of DNA end processing. J. Bacteriol. 188 (2006) 353-360
21. Jin H., Retallack D.M., Stelman S.J., Hershberger C.D., and Ramseier T. Characterization of the SOS response of Pseudomonas fluorescens strain DC206 using whole-genome transcript analysis. FEMS Microbiol. Lett. 269 (2007) 256-264
22. Alonso J.C., Stiege A.C., Dobrinski B., and Lurz R. Purification and properties of the RecR protein from Bacillus subtilis. J. Biol. Chem. 268 (1993) 1424-1429
23. Funayama T., Narumi I., Kikuchi M., Kitayama S., Watanabe H., and Yamamoto K. Identification and disruption analysis of the recN gene in the extremely radioresistant bacterium Deinococcus radiodurans. Mutat. Res. 435 (1999) 151-161
24. Wang G., and Maier R.J. Critical role of RecN in recombinational DNA repair and survival of Helicobacter pylori. Infect. Immun. 76 (2008) 153-160
25. Wang X., Reyes-Lamothe R., and Sherratt D.J. Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev. 22 (2008) 2426-2433
26. Skaar E.P., Lazio M.P., and Seifert H.S. Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J. Bacteriol. 184 (2002) 919-927
27. Kidane D., Sanchez H., Alonso J.C., and Graumann P.L. 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 (2004) 1627-1639
28. Sanchez H., and Alonso J.C. Bacillus subtilis RecN binds and protects 3'-single-stranded DNA extensions in the presence of ATP. Nucleic Acids Res. 33 (2005) 2343-2350
29. Sanchez H., Cardenas P.P., Yoshimura S.H., Takeyasu K., and Alonso J.C. Dynamic structures of Bacillus subtilis RecN-DNA complexes. Nucleic Acids Res. 36 (2008) 110-120
30. Simmons L.A., Goranov A.I., Kobayashi H., Davies B.W., Yuan D.S., Grossman A.D., and Walker G.C. Comparison of responses to double-strand breaks between Escherichia coli and Bacillus subtilis reveals different requirements for SOS induction. J. Bacteriol. 191 (2009) 1152-1161
31. Sharples G.J., and Leach D.R.F. Structural and functional similarities between SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) proteins of yeast. Mol. Microbiol. 17 (1995) 1215-1220
32. Cobbe N., and Heck M.M. The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21 (2004) 332-347
33. Kinoshita E., van der Linden E., Sanchez H., and Wyman C. RAD50, an SMC family member with multiple roles in DNA break repair: how does ATP affect function?. Chromosome Res. 17 (2009) 277-288
34. Hirano T. The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev. 16 (2002) 399-414
35. Peters J.M., Tedeschi A., and Schmitz J. The cohesin complex and its roles in chromosome biology. Genes Dev. 22 (2008) 3089-3114
36. Haering C.H., Farcas A.M., Arumugam P., Metson J., and Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 454 (2008) 297-301
37. Sjogren C., and Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11 (2001) 991-995
38. Nasmyth K., and Haering C.H. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 74 (2005) 595-648
39. Neher S.B., Villen J., Oakes E.C., Bakalarski C.E., Sauer R.T., Gygi S.P., and Baker T.A. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol. Cell. 22 (2006) 193-204
40. Datsenko K.A., and Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 6640-6645
41. Lau I.F., Filipe S.R., Soballe B., Okstad O.A., Barre F.X., and Sherratt D.J. Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol. Microbiol. 49 (2003) 731-743
42. Al-Deib A.A., Mahdi A.A., and Lloyd R.G. Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12. J. Bacteriol. 178 (1996) 6782-6789
43. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
44. Cole C., Barber J.D., and Barton G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36 (2008) W197-201
45. McGlynn P., Mahdi A.A., and Lloyd R.G. Characterisation of the catalytically active form of RecG helicase. Nucleic Acids Res. 28 (2000) 2324-2332
46. Cadman C.J., Lopper M., Moon P.B., Keck J.L., and McGlynn P. PriB stimulates PriA helicase via an interaction with single-stranded DNA. J. Biol. Chem. 280 (2005) 39693-39700
47. Lloyd R.G., and Sharples G.J. Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J. 12 (1993) 17-22
48. Arumugam P., Nishino T., Haering C.H., Gruber S., and Nasmyth K. Cohesin's ATPase activity is stimulated by the C-terminal Winged-Helix domain of its kleisin subunit. Curr. Biol. 16 (2006) 1998-2008
49. Lowe J., Cordell S.C., and van den Ent F. Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. J. Mol. Biol. 306 (2001) 25-35
50. Briggs G.S., McEwan P.A., Yu J., Moore T., Emsley J., and Lloyd R.G. Ring structure of the Escherichia coli DNA binding protein RdgC associated with recombination and replication fork repair. J. Biol. Chem. 282 (2007) 12353-12357
51. Moore T., Sharples G.J., and Lloyd R.G. DNA binding by the meningococcal RdgC protein, associated with pilin antigenic variation. J. Bacteriol. 186 (2004) 870-874
52. Kidane D., and Graumann P.L. Dynamic formation of RecA filaments at DNA double strand break repair centers in live cells. J. Cell Biol. 170 (2005) 357-366
53. Yamazoe M., Onogi T., Sunako Y., Niki H., Yamanaka K., Ichimura T., and Hiraga S. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J. 18 (1999) 5873-5884
54. Niki H., Jaffe A., Imamura R., Ogura T., and Hiraga S. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 10 (1991) 183-193
55. Rybenkov V.V. Towards the architecture of the chromosomal architects. Nat. Struct. Mol. Biol. 16 (2009) 104-105
56. Woo J.S., Lim J.H., Shin H.C., Suh M.K., Ku B., Lee K.H., Joo K., Robinson H., Lee J., Park S.Y., Ha N.C., and Oh B.H. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 136 (2009) 85-96
57. Kidane D., and Graumann P.L. Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 122 (2005) 73-84