DNA double strand break end-processing and RecA induce RecN expression levels in Bacillus subtilis

DNA Repair

Volumn 14, Issue 1, 2014, Pages 1-8

  Cardenas, Paula P ^a   Gándara, Carolina ^a   Alonso, Juan C ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

AddAB; DNA damage response; Double strand breaks; LexA; RecA; RecJ; RecN; SOS response

Indexed keywords

DOUBLE STRANDED DNA; LEXA PROTEIN; RECA PROTEIN; RECN PROTEIN; RECO PROTEIN; SOS PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; CONTROLLED STUDY; DNA DETERMINATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; TURNOVER TIME;

BACILLUS SUBTILIS;

ADDAB; DNA DAMAGE RESPONSE; DOUBLE STRAND BREAKS; LEXA; RECA; RECJ; RECN; SOS RESPONSE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA RESTRICTION ENZYMES; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ARCHAEAL; HYDROGEN PEROXIDE; MITOMYCIN; REC A RECOMBINASES;

EID: 84892831433     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.12.001     Document Type: Article

References (70)

1. 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.
2. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
3. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408:433-439.
4. Cimprich K.A., Cortez D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 2008, 9:616-627.
5. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
6. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
7. Ditch S., Paull T.T. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 2012, 37:15-22.
8. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47:497-510.
9. Radman M. SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis. Basic Life Sci. 1975, 5A:355-367.
10. Sassanfar M., Roberts J.W. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J. Mol. Biol. 1990, 212:79-96.
11. Little J.W. Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease. Biochimie 1991, 73:411-421.
12. Erill I., Campoy S., Barbe J. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 2007, 31:637-656.
13. Butala M., Zgur-Bertok D., Busby S.J. The bacterial LexA transcriptional repressor. Cell. Mol. Life Sci. 2009, 66:82-93.
14. 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.
15. Alonso J.C., Cardenas P.P., Sanchez H., Hejna J., Suzuki Y., Takeyasu K. Early steps of double-strand break repair in Bacillus subtilis. DNA Repair 2013, 12:162-176.
16. Ayora S., Carrasco B., Cardenas P.P., Cesar C.E., Canas 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.
17. 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.
18. Fernandez De Henestrosa A.R., Ogi T., Aoyagi S., Chafin D., Hayes J.J., Ohmori H., Woodgate R. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 2000, 35:1560-1572.
19. 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.
20. 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.
21. 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.
22. Moeller R., Stackebrandt E., Douki T., Cadet J., Rettberg P., Mollenkopf H.J., Reitz G., Horneck G. DNA bipyrimidine photoproduct repair and transcriptional response of UV-C irradiated Bacillus subtilis. Arch. Microbiol. 2007, 188:421-431.
23. 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.
24. Cardenas P.P., Carrasco B., Sanchez H., Deikus G., Bechhofer D.H., Alonso J.C. Bacillus subtilis polynucleotide phosphorylase 3'-to-5' DNase activity is involved in DNA repair. Nucleic Acids Res. 2009, 37:4157-4169.
25. Nicolas P., Mader U., Dervyn E., Rochat T., Leduc A., Pigeonneau N., Bidnenko E., Marchadier E., Hoebeke M., Aymerich S., Becher D., Bisicchia P., Botella E., Delumeau O., Doherty G., Denham E.L., Fogg M.J., Fromion V., Goelzer A., Hansen A., Hartig E., Harwood C.R., Homuth G., Jarmer H., Jules M., Klipp E., Le Chat L., Lecointe F., Lewis P., Liebermeister W., March A., Mars R.A., Nannapaneni P., Noone D., Pohl S., Rinn B., Rugheimer F., Sappa P.K., Samson F., Schaffer M., Schwikowski B., Steil L., Stulke J., Wiegert T., Devine K.M., Wilkinson A.J., van Dijl J.M., Hecker M., Volker U., Bessieres P., Noirot P. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 2012, 335:1103-1106.
26. Marchadier E., Carballido-Lopez R., Brinster S., Fabret C., Mervelet P., Bessieres P., Noirot-Gros M.F., Fromion V., Noirot P. An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: exploration by an integrative approach. Proteomics 2011, 11:2981-2991.
27. Condon C. RNA processing and degradation in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 2003, 67:157-174.
28. Paull T.T., Gellert M. The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1998, 1:969-979.
29. 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.
30. 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.
31. 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.
32. Sanchez H., Carrasco B., Ayora S., Alonso J.C. Dynamics of DNA Double-Strand Break Repair in Bacillus subtilis 2007, Caister Academic Press, Norfolk.
33. Yeeles J.T., Dillingham M.S. A dual-nuclease mechanism for DNA break processing by AddAB-type helicase-nucleases. J. Mol. Biol. 2007, 371:66-78.
34. 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.
35. 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.
36. 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.
37. Ceglowski P., Luder G., Alonso J.C. Genetic analysis of recE activities in Bacillus subtilis. Mol. Gen. Genet. 1990, 222:441-445.
38. 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.
39. Fernandez S., Kobayashi Y., Ogasawara N., Alonso J.C. Analysis of the Bacillus subtilis recO gene: RecO forms part of the RecFLOR function. Mol. Gen. Genet. 1999, 261:567-573.
40. Lioy V.S., Martin M.T., Camacho A.G., Lurz R., Antelmann H., Hecker M., Hitchin E., Ridge Y., Wells J.M., Alonso J.C. pSM19035-encoded zeta toxin induces stasis followed by death in a subpopulation of cells. Microbiology 2006, 152:2365-2379.
41. 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.
42. 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.
43. Carrasco B., Ayora S., Lurz R., Alonso J.C. Bacillus subtilis RecU holliday-junction resolvase modulates RecA activities. Nucleic Acids Res. 2005, 33:3942-3952.
44. 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.
45. 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.
46. 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.
47. + and DNA repair-deficient strains. J. Bacteriol. 1988, 170:1467-1474.
48. 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.
49. Imlay J.A., Chin S.M., Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988, 240:640-642.
50. 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.
51. B-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J. Bacteriol. 1999, 181:3942-3948.
52. Hecker M., Pane-Farre J., Volker U. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 2007, 61:215-236.
53. Belda E., Sekowska A., Le Fevre F., Morgat A., Mornico D., Ouzounis C., Vallenet D., Medigue C., Danchin A. An updated metabolic view of the Bacillus subtilis 168 genome. Microbiology 2013, 159:757-770.
54. 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.
55. 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.
56. Radding C.M. Helical interactions in homologous pairing and strand exchange driven by RecA protein. J. Biol. Chem. 1991, 266:5355-5358.
57. 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.
58. Cox M.M. Regulation of bacterial RecA protein function. Crit. Rev. Biochem. Mol. Biol. 2007, 42:41-63.
59. Fernandez S., Ayora S., Alonso J.C. Bacillus subtilis homologous recombination: genes and products. Res. Microbiol. 2000, 151:481-486.
60. 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.
61. 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.
62. Vlašić I., Mertens R., Seco E.M., Carrasco B., Ayora S., Reitz G., Commichau F.M., Alonso J.C., Moeller R. Bacillus subtilis RecA and its accessory factors, RecF, RecO, RecR and RecX, are required for spore resistance to DNA double strand break. Nucleic Acids Res. 2013, (in press) [Epub ahead of print].
63. Gomez-Gomez J.M., Manfredi C., Alonso J.C., Blazquez J. A novel role for RecA under non-stress: promotion of swarming motility in Escherichia coli K-12. BMC Biol. 2007, 5:14.
64. McInerney P., O'Donnell M. Replisome fate upon encountering a leading strand block and clearance from DNA by recombination proteins. J. Biol. Chem. 2007, 282:25903-25916.
65. Indiani C., Patel M., Goodman M.F., O'Donnell M.E. RecA acts as a switch to regulate polymerase occupancy in a moving replication fork. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:5410-5415.
66. Lia G., Rigato A., Long E., Chagneau C., Le Masson M., Allemand J.F., Michel B. RecA-promoted, RecFOR-independent progressive disassembly of replisomes stalled by helicase inactivation. Mol. Cell 2013, 49:547-557.
67. 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.
68. 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.
69. 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.
70. 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.