Early steps of double-strand break repair in Bacillus subtilis

DNA Repair

Volumn 12, Issue 3, 2013, Pages 162-176

  Alonso, Juan C ^a   Cardenas, Paula P ^a   Sanchez, Humberto ^b   Hejna, James ^c   Suzuki, Yuki ^c   Takeyasu, Kunio ^c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

DNA damage induced foci; Double strand break repair; End resection; Non homologous end joining

Indexed keywords

DOUBLE STRANDED DNA;

3' UNTRANSLATED REGION; BACILLUS SUBTILIS; BACTERIAL CHROMOSOME; CHEMICAL STRUCTURE; CHROMOSOME SEGREGATION; CYTOLOGY; DNA DAMAGE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; FIRMICUTES; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR; DNA RESTRICTION ENZYMES; DNA, BACTERIAL; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINATIONAL DNA REPAIR;

BACILLUS SUBTILIS; FIRMICUTES;

EID: 84875364461     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.12.005     Document Type: Review

References (208)

1. Jiricny J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell. Biol. 2006, 7:335-346.
2. Lenhart J.S., Schroeder J.W., Walsh B.W., Simmons L.A. DNA repair and genome maintenance in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 2012, 76:530-564.
3. Selby C.P., Sancar A. Molecular mechanism of transcription-repair coupling. Science 1993, 260:53-58.
4. Ayora S., Rojo F., Ogasawara N., Nakai S., Alonso J.C. The Mfd protein of Bacillus subtilis 168 is involved in both transcription-coupled DNA repair and DNA recombination. J. Mol. Biol. 1996, 256:301-318.
5. Lindahl T., Barnes D.E. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 2000, 65:127-133.
6. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington, DC.
7. Hoeijmakers J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 2009, 361:1475-1485.
8. Moldovan G.L., D'Andrea A.D. How the fanconi anemia pathway guards the genome. Annu. Rev. Genet. 2009, 43:223-249.
9. San Filippo J., Sung P., Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 2008, 77:229-257.
10. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell. Biol. 2003, 4:435-445.
11. Ayora S., Carrasco B., Cardenas P.P., César C.E., Cañas C., Yadav T., Marchisone C., Alonso J.C. Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol. Rev. 2011, 35:1055-1081.
12. Noirot-Gross M.-F., Polard P., Noirot P. Replication of the Bacillus subtilis Chromosome 2012, Caister Academic Press, Norfolk. 2nd ed.
13. Carrasco B., Cardenas P.P., Cañas C., Yadav T., César C.E., Ayora S., Alonso J.C. Dynamics of DNA Double-Strand Break Repair in Bacillus subtilis 2012, Caister Academic Press, Norfolk. 2nd ed.
14. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 2010, 79:181-211.
15. Pitcher R.S., Brissett N.C., Doherty A.J. Nonhomologous end-joining in bacteria: a microbial perspective. Annu. Rev. Microbiol. 2007, 61:259-282.
16. Shuman S., Glickman M.S. Bacterial DNA repair by non-homologous end joining. Nat. Rev. Microbiol. 2007, 5:852-861.
17. Petit M.A., Ehrlich D. Essential bacterial helicases that counteract the toxicity of recombination proteins. EMBO J. 2002, 21:3137-3147.
18. Sanchez H., Carrasco B., Cozar M.C., Alonso J.C. Bacillus subtilis RecG branch migration translocase is required for DNA repair and chromosomal segregation. Mol. Microbiol. 2007, 65:920-935.
19. Sanchez H., Kidane D., Reed P., Curtis F.A., Cozar M.C., Graumann P.L., Sharples G.J., Alonso J.C. The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 2005, 171:873-883.
20. Kuzminov A. Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol. Mol. Biol. Rev. 1999, 63:751-813.
21. McGlynn P., Lloyd R.G. Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell. Biol. 2002, 3:859-870.
22. Courcelle J., Hanawalt P.C. RecA-dependent recovery of arrested DNA replication forks. Annu. Rev. Genet. 2003, 37:611-646.
23. Kreuzer K.N. Interplay between DNA replication and recombination in prokaryotes. Annu. Rev. Microbiol. 2005, 59:43-67.
24. Persky N.S., Lovett S.T. Mechanisms of recombination: lessons from E. coli. Crit. Rev. Biochem. Mol. Biol. 2008, 43:347-370.
25. Michel B., Boubakri H., Baharoglu Z., LeMasson M., Lestini R. Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst.) 2007, 6:967-980.
26. Simmons L.A., Goranov A.I., Kobayashi H., Davies B.W., Yuan D.S., Grossman A.D., Walker G.C. Comparison of responses to double-strand breaks between Escherichia coli and Bacillus subtilis reveals different requirements for SOS induction. J. Bacteriol. 2009, 191:1152-1161.
27. Cromie G.A., Leach D.R. Control of crossing over. Mol. Cell 2000, 6:815-826.
28. Marians K.J. Mechanisms of replication fork restart in Escherichia coli. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2004, 359:71-77.
29. Dillingham M.S., Kowalczykowski S.C. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 2008, 72:642-671.
30. Sanchez H., Carrasco B., Ayora S., Alonso J.C. Dynamics of DNA Double-Strand Break Repair in Bacillus subtilis 2007, Caister Academic Press, Norfolk.
31. Ayora S., Cardenas P., Manfredi C., Cañas C., Carrasco B., Alonso J.C. DNA Double Strand Break Repair in Firmicutes 2012, Horizon Scientific Press, Norwick.
32. Cardenas P.P., Carrasco B., Defeu Soufo C., Cesar C.E., Herr K., Kaufenstein M., Graumann P.L., Alonso J.C. RecX Facilitates Homologous Recombination by Modulating RecA Activities. PLoS Genet 2012, 8:e1003126.
33. Kidane D., Ayora S., Sweasy J.B., Graumann P.L., Alonso J.C. The cell pole: the site of cross talk between the DNA uptake and genetic recombination machinery. Crit. Rev. Biochem. Mol. Biol. 2012, 47:531-555.
34. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
35. Kidane D., Sanchez H., Alonso J.C., 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. 2004, 52:1627-1639.
36. Krishnamurthy M., Tadesse S., Rothmaier K., Graumann P.L. A novel SMC-like protein, SbcE (YhaN), is involved in DNA double-strand break repair and competence in Bacillus subtilis. Nucleic Acids Res. 2010, 38:455-466.
37. Lindow J.C., Kuwano M., Moriya S., Grossman A.D. Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol. Microbiol. 2002, 46:997-1009.
38. Mascarenhas J., Soppa J., Strunnikov A.V., Graumann P.L. Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J. 2002, 21:3108-3118.
39. Mascarenhas J., Sanchez H., Tadesse S., Kidane D., Krishnamurthy M., Alonso J.C., Graumann P.L. Bacillus subtilis SbcC protein plays an important role in DNA inter-strand cross-link repair. BMC Mol. Biol. 2006, 7:20.
40. Sanchez H., Kidane D., Cozar M.C., Graumann P.L., Alonso J.C. Recruitment of Bacillus subtilis RecN to DNA double-strand breaks in the absence of DNA end processing. J. Bacteriol. 2006, 188:353-360.
41. Meile J.C., Wu L.J., Ehrlich S.D., Errington J., Noirot P. Systematic localisation of proteins fused to the green fluorescent protein in Bacillus subtilis: identification of new proteins at the DNA replication factory. Proteomics 2006, 6:2135-2146.
42. Sanchez H., Cardenas P.P., Yoshimura S.H., Takeyasu K., Alonso J.C. Dynamic structures of Bacillus subtilis RecN-DNA complexes. Nucleic Acids Res. 2008, 36:110-120.
43. Shi W.X., Larson R.G. Atomic force microscopic study of aggregation of RecA-DNA nucleoprotein filaments into left-handed supercoiled bundles. Nano Lett. 2005, 5:2476-2481.
44. Sattin B.D., Goh M.C. Direct observation of the assembly of RecA/DNA complexes by atomic force microscopy. Biophys. J. 2004, 87:3430-3436.
45. Manfredi C., Suzuki Y., Yadav T., Takeyasu K., Alonso J.C. RecO-mediated DNA homology search and annealing is facilitated by SsbA. Nucleic Acids Res. 2010, 38:6920-6929.
46. Lushnikov A.Y., Bogdanov A., Lyubchenko Y.L. DNA recombination: Holliday junctions dynamics and branch migration. J. Biol. Chem. 2003, 278:43130-43134.
47. Fernández S., Rojo F., Alonso J.C. The Bacillus subtilis chromatin-associated protein Hbsu is involved in DNA repair and recombination. Mol. Microbiol. 1997, 23:1169-1179.
48. Rimsky S., Travers A. Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins. Curr. Opin. Microbiol. 2011, 14:136-141.
49. Lopez-Torrejon G., Martinez-Jimenez M.I., Ayora S. Role of LrpC from Bacillus subtilis in DNA transactions during DNA repair and recombination. Nucleic Acids Res. 2006, 34:120-129.
50. Thaw P., Sedelnikova S.E., Muranova T., Wiese S., Ayora S., Alonso J.C., Brinkman A.B., Akerboom J., van der Oost J., Rafferty J.B. Structural insight into gene transcriptional regulation and effector binding by the Lrp/AsnC family. Nucleic Acids Res. 2006, 34:1439-1449.
51. Graumann P.L. Chromosome Segregation 2012, Caister Academic Press, Norfolk. 2nd ed.
52. Tadesse S., Graumann P.L. Differential and dynamic localization of topoisomerases in Bacillus subtilis. J. Bacteriol. 2006, 188:3002-3011.
53. 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.
54. Sullivan N.L., Marquis K.A., Rudner D.Z. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 2009, 137:697-707.
55. Mascarenhas J., Weber M.H., Graumann P.L. Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep. 2001, 2:685-689.
56. Ohniwa R.L., Morikawa K., Takeshita S.L., Kim J., Ohta T., Wada C., Takeyasu K. Transcription-coupled nucleoid architecture in bacteria. Genes Cells 2007, 12:1141-1152.
57. Kim J., Yoshimura S.H., Hizume K., Ohniwa R.L., Ishihama A., Takeyasu K. Fundamental structural units of the Escherichia coli nucleoid revealed by atomic force microscopy. Nucleic Acids Res. 2004, 32:1982-1992.
58. Ohniwa R.L., Morikawa K., Kim J., Ohta T., Ishihama A., Wada C., Takeyasu K. Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J. 2006, 25:5591-5602.
59. Morikawa K., Ohniwa R.L., Kim J., Maruyama A., Ohta T., Takeyasu K. Bacterial nucleoid dynamics: oxidative stress response in Staphylococcus aureus. Genes Cells 2006, 11:409-423.
60. Postow L., Hardy C.D., Arsuaga J., Cozzarelli N.R. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 2004, 18:1766-1779.
61. Sherratt D.J. Bacterial chromosome dynamics. Science 2003, 301:780-785.
62. Frenkiel-Krispin D., Minsky A. Nucleoid organization and the maintenance of DNA integrity in E. coli, B. subtilis and D. radiodurans. J. Struct. Biol. 2006, 156:311-319.
63. Witz G., Stasiak A. DNA supercoiling and its role in DNA decatenation and unknotting. Nucleic Acids Res. 2010, 38:2119-2133.
64. Hirano T. How to separate entangled sisters: interplay between condensin and decatenase. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:18749-18750.
65. Sanchez H., Carrasco B., Ayora S., Alonso J.C. Homologous Recombination in Low dC+dG Gram-Positive Bacteria 2007, Springer Berlin/Heidelberg, Berlin/Heidelberg.
66. Graumann P.L., Knust T. Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res. 2009, 17:265-275.
67. Hirano T. At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell. Biol. 2006, 7:311-322.
68. Connelly J.C., Leach D.R. Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 2002, 27:410-418.
69. Berkmen M.B., Grossman A.D. Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol. Microbiol. 2006, 62:57-71.
70. Lemon K.P., Grossman A.D. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 1998, 282:1516-1519.
71. Lemon K.P., Grossman A.D. Movement of replicating DNA through a stationary replisome. Mol. Cell 2000, 6:1321-1330.
72. Britton R.A., Lin D.C., Grossman A.D. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev. 1998, 12:1254-1259.
73. Graumann P.L., Losick R., Strunnikov A.V. Subcellular localization of Bacillus subtilis SMC, a protein involved in chromosome condensation and segregation. J. Bacteriol. 1998, 180:5749-5755.
74. Moriya S., Tsujikawa E., Hassan A.K., Asai K., Kodama T., Ogasawara N. A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol. Microbiol. 1998, 29:179-187.
75. Costes A., Lecointe F., McGovern S., Quevillon-Cheruel S., Polard P. The C-terminal domain of the bacterial SSB protein acts as a DNA maintenance hub at active chromosome replication forks. PLoS Genet. 2010, 6:e1001238.
76. Goranov A.I., Kuester-Schoeck E., Wang J.D., Grossman A.D. Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis. J. Bacteriol. 2006, 188:5595-5605.
77. Khil P.P., Camerini-Otero R.D. Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol. Microbiol. 2002, 44:89-105.
78. Cox M.M. Regulation of bacterial RecA protein function. Crit. Rev. Biochem. Mol. Biol. 2007, 42:41-63.
79. Chiesa M., Cardenas P.P., Oton F., Martinez J., Mas-Torrent M., Garcia F., Alonso J.C., Rovira C., Garcia R. Detection of the early stage of recombinational DNA repair by silicon nanowire transistors. Nano Lett. 2012, 12:1275-1281.
80. Kowalczykowski S.C., Dixon D.A., Eggleston A.K., Lauder S.D., Rehrauer W.M. Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 1994, 58:401-465.
81. Yadav T., Carrasco B., Myers A.R., George N.P., Keck J.L., Alonso J.C. Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res. 2012, 40:5546-5559.
82. Lusetti S.L., Hobbs M.D., Stohl E.A., Chitteni-Pattu S., Inman R.B., Seifert H.S., Cox M.M. The RecF protein antagonizes RecX function via direct interaction. Mol. Cell 2006, 21:41-50.
83. Courcelle J., Khodursky A., Peter B., Brown P.O., Hanawalt P.C. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 2001, 158:41-64.
84. Au N., Kuester-Schoeck E., Mandava V., Bothwell L.E., Canny S.P., Chachu K., Colavito S.A., Fuller S.N., Groban E.S., Hensley L.A., O'Brien T.C., Shah A., Tierney J.T., Tomm L.L., O'Gara T.M., Goranov A.I., Grossman A.D., Lovett C.M. Genetic composition of the Bacillus subtilis SOS system. J. Bacteriol. 2005, 187:7655-7666.
85. Erill I., Campoy S., Barbe J. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 2007, 31:637-656.
86. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408:433-439.
87. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300:1542-1548.
88. Paulsen R.D., Cimprich K.A. The ATR pathway: fine-tuning the fork. DNA Repair (Amst.) 2007, 6:953-966.
89. Harper J.W., Elledge S.J. The DNA damage response: ten years after. Mol. Cell 2007, 28:739-745.
90. Fu Y., Zhu Y., Zhang K., Yeung M., Durocher D., Xiao W. Rad6-Rad18 mediates a eukaryotic SOS response by ubiquitinating the 9-1-1 checkpoint clamp. Cell 2008, 133:601-611.
91. Pohlhaus J.R., Long D.T., O'Reilly E., Kreuzer K.N. The e{open} subunit of DNA polymerase III Is involved in the nalidixic acid-induced SOS response in Escherichia coli. J. Bacteriol. 2008, 190:5239-5247.
92. Cardenas P.P., Carzaniga T., Zangrossi S., Briani F., Garcia-Tirado E., Deho G., Alonso J.C. Polynucleotide phosphorylase exonuclease and polymerase activities on single-stranded DNA ends are modulated by RecN, SsbA and RecA proteins. Nucleic Acids Res. 2011, 39:9250-9261.
93. Schook P.O., Stohl E.A., Criss A.K., Seifert H.S. The DNA-binding activity of the Neisseria gonorrhoeae LexA orthologue NG1427 is modulated by oxidation. Mol. Microbiol. 2011, 79:846-860.
94. Finch P.W., Chambers P., Emmerson P.T. Identification of the Escherichia coli recN gene product as a major SOS protein. J. Bacteriol. 1985, 164:653-658.
95. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
96. Chowdhury D., Keogh M.C., Ishii H., Peterson C.L., Buratowski S., Lieberman J. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 2005, 20:801-809.
97. Lee D.H., Pan Y., Kanner S., Sung P., Borowiec J.A., Chowdhury D. A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nat. Struct. Mol. Biol. 2010, 17:365-372.
98. Elsholz A.K., Turgay K., Michalik S., Hessling B., Gronau K., Oertel D., Mader U., Bernhardt J., Becher D., Hecker M., Gerth U. Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:7451-7456.
99. Soufi B., Kumar C., Gnad F., Mann M., Mijakovic I., Macek B. Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis. J. Proteome Res. 2010, 9:3638-3646.
100. Mijakovic I., Petranovic D., Macek B., Cepo T., Mann M., Davies J., Jensen P.R., Vujaklija D. Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine. Nucleic Acids Res. 2006, 34:1588-1596.
101. D'Amours D., Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell. Biol. 2002, 3:317-327.
102. Stracker T.H., Theunissen J.W., Morales M., Petrini J.H. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst.) 2004, 3:845-854.
103. Lisby M., Rothstein R. DNA damage checkpoint and repair centers. Curr. Opin. Cell Biol. 2004, 16:328-334.
104. Sharples G.J., Leach D.R. Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol. 1995, 17:1215-1217.
105. Hopfner K.P., Tainer J.A. Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 2003, 13:249-255.
106. + and DNA repair-deficient strains. J. Bacteriol. 1988, 170:1467-1474.
107. Gassel M., Alonso J.C. Expression of the recE gene during induction of the SOS response in Bacillus subtilis recombination-deficient strains. Mol. Microbiol. 1989, 3:1269-1276.
108. Kidane D., Graumann P.L. Dynamic formation of RecA filaments at DNA double strand break repair centers in live cells. J. Cell Biol. 2005, 170:357-366.
109. Shintomi K., Hirano T. How are cohesin rings opened and closed?. Trends Biochem. Sci. 2007, 32:154-157.
110. Alonso J.C., Stiege A.C., Luder G. Genetic recombination in Bacillus subtilis 168: effect of recN, recF, recH and addAB mutations on DNA repair and recombination. Mol. Gen. Genet. 1993, 239:129-136.
111. Heitman J., Zinder N.D., Model P. Repair of the Escherichia coli chromosome after in vivo scission by the EcoRI endonuclease. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:2281-2285.
112. Kosa J.L., Zdraveski Z.Z., Currier S., Marinus M.G., Essigmann J.M. RecN and RecG are required for Escherichia coli survival of Bleomycin-induced damage. Mutat. Res. 2004, 554:149-157.
113. Picksley S.M., Attfield P.V., Lloyd R.G. Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product. Mol. Gen. Genet. 1984, 195:267-274.
114. Henner W.D., Rodriguez L.O., Hecht S.M., Haseltine W.A. Gamma ray induced deoxyribonucleic acid strand breaks. 3' Glycolate termini. J. Biol. Chem. 1983, 258:711-713.
115. Neher S.B., Villen J., Oakes E.C., Bakalarski C.E., Sauer R.T., Gygi S.P., Baker T.A. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol. Cell 2006, 22:193-204.
116. Meddows T.R., Savory A.P., Grove J.I., Moore T., Lloyd R.G. RecN protein and transcription factor DksA combine to promote faithful recombinational repair of DNA double-strand breaks. Mol. Microbiol. 2005, 57:97-110.
117. Nagashima K., Kubota Y., Shibata T., Sakaguchi C., Shinagawa H., Hishida T. Degradation of Escherichia coli RecN aggregates by ClpXP protease and its implications for DNA damage tolerance. J. Biol. Chem. 2006, 281:30941-30946.
118. Sanchez H., Alonso J.C. Bacillus subtilis RecN binds and protects 3'-single-stranded DNA extensions in the presence of ATP. Nucleic Acids Res. 2005, 33:2343-2350.
119. 2+ and ATPγS may contain RNA. Mol. Gen. Genet. 1985, 199:415-420.
120. Cardenas P.P., Carrasco B., Sanchez H., Deikus G., Bechhofer D.H., Alonso J.C. Bacillus subtilis polynucleotide phosphorylase 3'→5' DNase activity is involved in DNA repair. Nucleic Acids Res. 2009, 37:4157-4169.
121. Oussenko I.A., Sanchez R., Bechhofer D.H. Bacillus subtilis YhaM, a member of a new family of 3'-to-5' exonucleases in Gram-positive bacteria. J. Bacteriol. 2002, 184:6250-6259.
122. Shida T., Ogawa T., Ogasawara N., Sekiguchi J. Characterization of Bacillus subtilis ExoA protein: a multifunctional DNA-repair enzyme similar to the Escherichia coli exonuclease III. Biosci. Biotechnol. Biochem. 1999, 63:1528-1534.
123. McRobbie A.M., Meyer B., Rouillon C., Petrovic-Stojanovska B., Liu H., White M.F. Staphylococcus aureus DinG, a helicase that has evolved into a nuclease. Biochem J. 2012, 442:77-84.
124. Paull T.T., Gellert M. The 3'→5' exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1998, 1:969-979.
125. Trujillo K.M., Yuan S.S., Lee E.Y., Sung P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 1998, 273:21447-21450.
126. Lengsfeld B.M., Rattray A.J., Bhaskara V., Ghirlando R., Paull T.T. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 2007, 28:638-651.
127. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., Jackson S.P. Human CtIP promotes DNA end resection. Nature 2007, 450:509-514.
128. Mimitou E.P., Symington L.S. Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci. 2009, 34:264-272.
129. Majka J., Alford B., Ausio J., Finn R.M., McMurray C.T. ATP hydrolysis by RAD50 protein switches MRE11 enzyme from endonuclease to exonuclease. J. Biol. Chem. 2012, 287:2328-2341.
130. Rath D., Mangoli S.H., Pagedar A.R., Jawali N. Involvement of pnp in survival of UV radiation in Escherichia coli K-12. Microbiology 2012, 158:1196-1205.
131. Thoms B., Wackernagel W. Interaction of RecBCD enzyme with DNA at double-strand breaks produced in UV-irradiated Escherichia coli: requirement for DNA end processing. J. Bacteriol. 1998, 180:5639-5645.
132. Centore R.C., Lestini R., Sandler S.J. XthA (Exonuclease III) regulates loading of RecA onto DNA substrates in log phase Escherichia coli cells. Mol. Microbiol. 2008, 67:88-101.
133. Zahradka K., Buljubasic M., Petranovic M., Zahradka D. Roles of ExoI and SbcCD nucleases in " reckless" DNA degradation in recA mutants of Escherichia coli. J. Bacteriol. 2009, 191:1677-1687.
134. Rocha E.P., Cornet E., Michel B. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet. 2005, 1:e15.
135. Connelly J.C., de Leau E.S., Leach D.R. DNA cleavage and degradation by the SbcCD protein complex from Escherichia coli. Nucleic Acids Res. 1999, 27:1039-1046.
136. + strains of Escherichia coli and roles of SbcB15 and XonA2 ExoI mutant enzymes. J. Bacteriol. 2008, 190:179-192.
137. Michel B., Grompone G., Flores M.J., Bidnenko V. Multiple pathways process stalled replication forks. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12783-12788.
138. Yeeles J.T., Dillingham M.S. The processing of double-stranded DNA breaks for recombinational repair by helicase-nuclease complexes. DNA Repair (Amst.) 2010, 9:276-285.
139. Yeeles J.T., van Aelst K., Dillingham M.S., Moreno-Herrero F. Recombination hotspots and single-stranded DNA binding proteins couple DNA translocation to DNA unwinding by the AddAB helicase-nuclease. Mol. Cell 2011, 42:806-816.
140. Saikrishnan K., Yeeles J.T., Gilhooly N.S., Krajewski W.W., Dillingham M.S., Wigley D.B. Insights into Chi recognition from the structure of an AddAB-type helicase-nuclease complex. EMBO J. 2012, 31:1568-1578.
141. Chedin F., Noirot P., Biaudet V., Ehrlich S.D. A five-nucleotide sequence protects DNA from exonucleolytic degradation by AddAB, the RecBCD analogue of Bacillus subtilis. Mol. Microbiol. 1998, 29:1369-1377.
142. Touzain F., Petit M.A., Schbath S., El Karoui M. DNA motifs that sculpt the bacterial chromosome. Nat. Rev. Microbiol. 2011, 9:15-26.
143. Yeeles J.T., Cammack R., Dillingham M.S. An iron-sulfur cluster is essential for the binding of broken DNA by AddAB-type helicase-nucleases. J. Biol. Chem. 2009, 284:7746-7755.
144. Fernández S., Sorokin A., Alonso J.C. Genetic recombination in Bacillus subtilis 168: effects of recU and recS mutations on DNA repair and homologous recombination. J. Bacteriol. 1998, 180:3405-3409.
145. Handa N., Morimatsu K., Lovett S.T., Kowalczykowski S.C. Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev. 2009, 23:1234-1245.
146. Umezu K., Nakayama H. RecQ DNA helicase of Escherichia coli. Characterization of the helix-unwinding activity with emphasis on the effect of single-stranded DNA-binding protein. J. Mol. Biol. 1993, 230:1145-1150.
147. Lecointe F., Serena C., Velten M., Costes A., McGovern S., Meile J.C., Errington J., Ehrlich S.D., Noirot P., Polard P. Anticipating chromosomal replication fork arrest: SSB targets repair DNA helicases to active forks. EMBO J. 2007, 26:4239-4251.
148. Gravel S., Chapman J.R., Magill C., Jackson S.P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 2008, 22:2767-2772.
149. Hopkins B.B., Paull T.T. The P. furiosus Mre11/Rad50 complex promotes 5' strand resection at a DNA double-strand break. Cell 2008, 135:250-260.
150. Mimitou E.P., Symington L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008, 455:770-774.
151. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.
152. Rupnik A., Lowndes N.F., Grenon M. MRN and the race to the break. Chromosoma 2010, 119:115-135.
153. Paull T.T., Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 1999, 13:1276-1288.
154. Cejka P., Cannavo E., Polaczek P., Masuda-Sasa T., Pokharel S., Campbell J.L., Kowalczykowski S.C. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 2010, 467:112-116.
155. Niu H., Chung W.H., Zhu Z., Kwon Y., Zhao W., Chi P., Prakash R., Seong C., Liu D., Lu L., Ira G., Sung P. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 2010, 467:108-111.
156. Nimonkar A.V., Genschel J., Kinoshita E., Polaczek P., Campbell J.L., Wyman C., Modrich P., Kowalczykowski S.C. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 2011, 25:350-362.
157. Martin S.G., Laroche T., Suka N., Grunstein M., Gasser S.M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell 1999, 97:621-633.
158. Lisby M., Barlow J.H., Burgess R.C., Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 2004, 118:699-713.
159. Lisby M., Rothstein R. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst.) 2009, 8:1068-1076.
160. Petrini J.H., Stracker T.H. The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol. 2003, 13:458-462.
161. Rupnik A., Grenon M., Lowndes N. The MRN complex. Curr. Biol. 2008, 18:R455-R457.
162. Wu D., Topper L.M., Wilson T.E. Recruitment and dissociation of nonhomologous end joining proteins at a DNA double-strand break in Saccharomyces cerevisiae. Genetics 2008, 178:1237-1249.
163. Pâques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999, 63:349-404.
164. Aguilera A., Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 2008, 9:204-217.
165. Mimitou E.P., Symington L.S. DNA end resection: many nucleases make light work. DNA Repair (Amst.) 2009, 8:983-995.
166. Huertas P., Jackson S.P. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 2009, 284:9558-9565.
167. Koike M., Koike A. Accumulation of Ku80 proteins at DNA double-strand breaks in living cells. Exp. Cell Res. 2008, 314:1061-1070.
168. Sinha K.M., Unciuleac M.C., Glickman M.S., Shuman S. AdnAB: a new DSB-resecting motor-nuclease from mycobacteria. Genes Dev. 2009, 23:1423-1437.
169. Tomita K., Matsuura A., Caspari T., Carr A.M., Akamatsu Y., Iwasaki H., Mizuno K., Ohta K., Uritani M., Ushimaru T., Yoshinaga K., Ueno M. Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol. Cell. Biol. 2003, 23:5186-5197.
170. Wasko B.M., Holland C.L., Resnick M.A., Lewis L.K. Inhibition of DNA double-strand break repair by the Ku heterodimer in mrx mutants of Saccharomyces cerevisiae. DNA Repair (Amst.) 2009, 8:162-169.
171. Barzel A., Kupiec M. Finding a match: how do homologous sequences get together for recombination?. Nat. Rev. Genet. 2008, 9:27-37.
172. Weiner A., Zauberman N., Minsky A. Recombinational DNA repair in a cellular context: a search for the homology search. Nat. Rev. Microbiol. 2009, 7:748-755.
173. Kidane D., Graumann P.L. Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 2005, 122:73-84.
174. Reyes E.D., Patidar P.L., Uranga L.A., Bortoletto A.S., Lusetti S.L. RecN is a cohesin-like protein that stimulates intermolecular DNA interactions in vitro. J. Biol. Chem. 2010, 285:16521-16529.
175. Kim J.I., Sharma A.K., Abbott S.N., Wood E.A., Dwyer D.W., Jambura A., Minton K.W., Inman R.B., Daly M.J., Cox M.M. RecA protein from the extremely radioresistant bacterium Deinococcus radiodurans: expression, purification, and characterization. J. Bacteriol. 2002, 184:1649-1660.
176. Cox M.M. Motoring along with the bacterial RecA protein. Nat. Rev. Mol. Cell. Biol. 2007, 8:127-138.
177. Galletto R., Kowalczykowski S.C. RecA. Curr. Biol. 2007, 17:R395-R397.
178. Simmons L.A., Grossman A.D., Walker G.C. Replication is required for the RecA localization response to DNA damage in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1360-1365.
179. Manfredi C., Carrasco B., Ayora S., Alonso J.C. Bacillus subtilis RecO nucleates RecA onto SsbA-coated single-stranded DNA. J. Biol. Chem. 2008, 283:24837-24847.
180. Anderson D.G., Kowalczykowski S.C. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a chi-regulated manner. Cell 1997, 90:77-86.
181. Hobbs M.D., Sakai A., Cox M.M. SSB protein limits RecOR binding onto single-stranded DNA. J. Biol. Chem. 2007, 282:11058-11067.
182. Sakai A., Cox M.M. RecFOR and RecOR as distinct RecA loading pathways. J. Biol. Chem. 2009, 284:3264-3272.
183. Morimatsu K., Kowalczykowski S.C. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 2003, 11:1337-1347.
184. Umezu K., Chi N.W., Kolodner R.D. 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. 1993, 90:3875-3879.
185. Carrasco B., Manfredi C., Ayora S., Alonso J.C. Bacillus subtilis SsbA and dATP regulate RecA nucleation onto single-stranded DNA. DNA Repair (Amst.) 2008, 7:990-996.
186. Kantake N., Madiraju M.V., Sugiyama T., Kowalczykowski S.C. Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15327-15332.
187. Kidane D., Carrasco B., Manfredi C., Rothmaier K., Ayora S., Tadesse S., Alonso J.C., Graumann P.L. Evidence for different pathways during horizontal gene transfer in competent Bacillus subtilis cells. PLoS Genet. 2009, 5:e1000630.
188. Nimonkar A.V., Sica R.A., Kowalczykowski S.C. Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3077-3082.
189. Wu Y., Sugiyama T., Kowalczykowski S.C. DNA annealing mediated by Rad52 and Rad59 proteins. J. Biol. Chem. 2006, 281:15441-15449.
190. Cheok C.F., Bachrati C.Z., Chan K.L., Ralf C., Wu L., Hickson I.D. Roles of the Bloom's syndrome helicase in the maintenance of genome stability. Biochem. Soc. Trans. 2005, 33:1456-1459.
191. Declais A.C., Lilley D.M. New insight into the recognition of branched DNA structure by junction-resolving enzymes. Curr. Opin. Struct. Biol. 2008, 18:86-95.
192. Schwartz E.K., Heyer W.D. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 2011, 120:109-127.
193. Nassif N., Penney J., Pal S., Engels W.R., Gloor G.B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 1994, 14:1613-1625.
194. Shan Q., Bork J.M., Webb B.L., Inman R.B., Cox M.M. RecA protein filaments: end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins. J. Mol. Biol. 1997, 265:519-540.
195. Niu H., Raynard S., Sung P. Multiplicity of DNA end resection machineries in chromosome break repair. Genes Dev. 2009, 23:1481-1486.
196. Gruenig M.C., Stohl E.A., Chitteni-Pattu S., Seifert H.S., Cox M.M. Less is more: Neisseria gonorrhoeae RecX protein stimulates recombination by inhibiting RecA. J. Biol. Chem. 2010, 285:37188-37197.
197. Adzuma K. No sliding during homology search by RecA protein. J. Biol. Chem. 1998, 273:31565-31573.
198. Forget A.L., Kowalczykowski S.C. Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search. Nature 2012, 482:423-427.
199. Zheng M., Wang X., Templeton L.J., Smulski D.R., LaRossa R.A., Storz G. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 2001, 183:4562-4570.
200. Campoy S., Fontes M., Padmanabhan S., Cortes P., Llagostera M., Barbe J. LexA-independent DNA damage-mediated induction of gene expression in Myxococcus xanthus. Mol. Microbiol. 2003, 49:769-781.
201. Black C.G., Fyfe J.A., Davies J.K. Absence of an SOS-like system in Neisseria gonorrhoeae. Gene 1998, 208:61-66.
202. Sebastian S., Agarwal S., Murphy J.R., Genco C.A. The gonococcal fur regulon: identification of additional genes involved in major catabolic, recombination, and secretory pathways. J. Bacteriol. 2002, 184:3965-3974.
203. Stohl E.A., Criss A.K., Seifert H.S. The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol. Microbiol. 2005, 58:520-532.
204. Grifantini R., Frigimelica E., Delany I., Bartolini E., Giovinazzi S., Balloni S., Agarwal S., Galli G., Genco C., Grandi G. Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes. Mol. Microbiol. 2004, 54:962-979.
205. Jordan P.W., Saunders N.J. Host iron binding proteins acting as niche indicators for Neisseria meningitidis. PLoS ONE 2009, 4:e5198.
206. B regulon. Mol. Microbiol. 1998, 29:1129-1136.
207. Baichoo N., Wang T., Ye R., Helmann J.D. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol. Microbiol. 2002, 45:1613-1629.
208. Helmann J.D., Wu M.F., Gaballa A., Kobel P.A., Morshedi M.M., Fawcett P., Paddon C. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J. Bacteriol. 2003, 185:243-253.