The C-terminal domain of the bacterial SSB protein acts as a DNA maintenance hub at active chromosome replication forks

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-15

  Costes, Audrey ^a   Lecointe, Franc̈ois ^b   McGovern, Stephen ^b   Quevillon Cheruel, Sophie ^c   Polard, Patrice ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UMR1319 MICALIS   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DNA POLYMERASE; DNA POLYMERASE DNA E; DNA POLYMERASE RECS; DNA POLYMERASE YPBB; DNA POLYMERASE YRRC; GREEN FLUORESCENT PROTEIN; PROTEIN PRIA; PROTEIN RARA; PROTEIN SBCC; PROTEIN UNG; PROTEIN XSEA; RECA PROTEIN; RECG HELICASE; RECJ PROTEIN; RECQ HELICASE; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA DETERMINATION; GENE DELETION; GENE INTERACTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN TARGETING; BACTERIAL CHROMOSOME; CHEMISTRY; DNA REPLICATION; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA REPLICATION; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 78650691470     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001238     Document Type: Article

References (54)

1. Michel B, Grompone G, Flores MJ, Bidnenko V (2004) Multiple pathways process stalled replication forks. Proc Natl Acad Sci U S A 101: 12783-12788.
2. Michel B, Boubakri H, Baharoglu Z, LeMasson M, Lestini R (2007) Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst) 6: 967-980.
3. Heller RC, Marians KJ (2006) Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7: 932-943.
4. Kong XP, Onrust R, O'Donnell M, Kuriyan J (1992) Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69: 425-437.
5. Lopez de Saro F (2009) Regulation of interactions with sliding clamps during DNA replication and repair. Curr Genomics 10: 206-215.
6. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol 43: 289-318.
7. Lu D, Keck JL (2008) Structural basis of Escherichia coli single-stranded DNA-binding protein stimulation of exonuclease I. Proc Natl Acad Sci U S A 105: 9169-9174.
8. Lecointe F, Serena C, Velten M, Costes A, McGovern S, et al. (2007) Anticipating chromosomal replication fork arrest: SSB targets repair DNA helicases to active forks. Embo J 26: 4239-4251.
9. Curth U, Genschel J, Urbanke C, Greipel J (1996) In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res 24: 2706-2711.
10. Meile JC, Wu LJ, Ehrlich SD, Errington J, Noirot P (2006) Systematic localisation of proteins fused to the green fluorescent protein in Bacillus subtilis: identification of new proteins at the DNA replication factory. Proteomics 6: 2135-2146.
11. Possoz C, Filipe SR, Grainge I, Sherratt DJ (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. Embo J 25: 2596-2604.
12. Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133: 90-102.
13. Liu J, Marians KJ (1999) PriA-directed assembly of a primosome on D loop DNA. J Biol Chem 274: 25033-25041.
14. Bruand C, Farache M, McGovern S, Ehrlich SD, Polard P (2001) DnaB, DnaD and DnaI proteins are components of the Bacillus subtilis replication restart primosome. Mol Microbiol 42: 245-255.
15. Polard P, Marsin S, McGovern S, Velten M, Wigley DB, et al. (2002) Restart of DNA replication in Gram-positive bacteria: functional characterisation of the Bacillus subtilis PriA initiator. Nucleic Acids Res 30: 1593-1605.
16. Rudolph CJ, Upton AL, Harris L, Lloyd RG (2009) Pathological replication in cells lacking RecG DNA translocase. Mol Microbiol 73: 352-366.
17. Zhang J, Mahdi AA, Briggs GS, Lloyd RG (2010) Promoting and avoiding recombination: contrasting activities of the Escherichia coli RuvABC Holliday junction resolvase and RecG DNA translocase. Genetics 185: 23-37.
18. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
19. Sanchez H, Kidane D, Castillo Cozar M, Graumann PL, Alonso JC (2006) Recruitment of Bacillus subtilis RecN to DNA double-strand breaks in the absence of DNA end processing. J Bacteriol 188: 353-360.
20. Shereda RD, Bernstein DA, Keck JL (2007) A central role for SSB in Escherichia coli RecQ DNA helicase function. J Biol Chem 282: 19247-19258.
21. Shereda RD, Reiter NJ, Butcher SE, Keck JL (2009) Identification of the SSB binding site on E. coli RecQ reveals a conserved surface for binding SSB's C terminus. J Mol Biol 386: 612-625.
22. Petit MA, Dervyn E, Rose M, Entian KD, McGovern S, et al. (1998) PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol Microbiol 29: 261-273.
23. Noirot P, Noirot-Gros MF (2004) Protein interaction networks in bacteria. Curr Opin Microbiol 7: 505-512.
24. Veaute X, Delmas S, Selva M, Jeusset J, Le Cam E, et al. (2005) UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. Embo J 24: 180-189.
25. Anand SP, Zheng H, Bianco PR, Leuba SH, Khan SA (2007) DNA helicase activity of PcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange. J Bacteriol 189: 4502-4509.
26. Boubakri H, de Septenville AL, Viguera E, Michel B (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. Embo J 29: 145-157.
27. Petit MA, Ehrlich D (2002) Essential bacterial helicases that counteract the toxicity of recombination proteins. Embo J 21: 3137-3147.
28. Dervyn E, Suski C, Daniel R, Bruand C, Chapuis J, et al. (2001) Two essential DNA polymerases at the bacterial replication fork. Science 294: 1716-1719.
29. Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282: 1516-1519.
30. Connelly JC, Kirkham LA, Leach DR (1998) The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc Natl Acad Sci U S A 95: 7969-7974.
31. Noirot-Gros MF, Dervyn E, Wu LJ, Mervelet P, Errington J, et al. (2002) An expanded view of bacterial DNA replication. Proc Natl Acad Sci U S A 99: 8342-8347.
32. Lestini R, Michel B (2007) UvrD controls the access of recombination proteins to blocked replication forks. Embo J 26: 3804-3814.
33. Noirot-Gros MF, Velten M, Yoshimura M, McGovern S, Morimoto T, et al. (2006) Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci U S A 103: 2368-2373.
34. Simmons LA, Grossman AD, Walker GC (2007) Replication is required for the RecA localization response to DNA damage in Bacillus subtilis. Proc Natl Acad Sci U S A 104: 1360-1365.
35. Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, et al. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433: 531-537.
36. Handa P, Acharya N, Varshney U (2001) Chimeras between single-stranded DNA-binding proteins from Escherichia coli and Mycobacterium tuberculosis reveal that their C-terminal domains interact with uracil DNA glycosylases. J Biol Chem 276: 16992-16997.
37. Duigou S, Ehrlich SD, Noirot P, Noirot-Gros MF (2004) Distinctive genetic features exhibited by the Y-family DNA polymerases in Bacillus subtilis. Mol Microbiol 54: 439-451.
38. Hobbs MD, Sakai A, Cox MM (2007) SSB protein limits RecOR binding onto single-stranded DNA. J Biol Chem 282: 11058-11067.
39. Mauel C, Karamata D (1984) Prophage induction in thermosensitive DNA mutants of Bacillus subtilis. Mol Gen Genet 194: 451-456.
40. Kaguni JM (2006) DnaA: controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60: 351-375.
41. Yuzhakov A, Kelman Z, O'Donnell M (1999) Trading places on DNA-a threepoint switch underlies primer handoff from primase to the replicative DNA polymerase. Cell 96: 153-163.
42. Suski C, Marians KJ (2008) Resolution of converging replication forks by RecQ and topoisomerase III. Mol Cell 30: 779-789.
43. Glover BP, McHenry CS (1998) The chi psi subunits of DNA polymerase III holoenzyme bind to single-stranded DNA-binding protein (SSB) and facilitate replication of an SSB-coated template. J Biol Chem 273: 23476-23484.
44. Kelman Z, Yuzhakov A, Andjelkovic J, O'Donnell M (1998) Devoted to the lagging strand-the subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. Embo J 17: 2436-2449.
45. Sanders GM, Dallmann HG, McHenry CS (2010) Reconstitution of the B. subtilis replisome with 13 proteins including two distinct replicases. Mol Cell 37: 273-281.
46. Molineux IJ, Gefter ML (1974) Properties of the Escherichia coli in DNA binding (unwinding) protein: interaction with DNA polymerase and DNA. Proc Natl Acad Sci U S A 71: 3858-3862.
47. Bonner CA, Randall SK, Rayssiguier C, Radman M, Eritja R, et al. (1988) Purification and characterization of an inducible Escherichia coli DNA polymerase capable of insertion and bypass at abasic lesions in DNA. J Biol Chem 263: 18946-18952.
48. Le Chatelier E, Becherel OJ, d'Alencon E, Canceill D, Ehrlich SD, et al. (2004) Involvement of DnaE, the second replicative DNA polymerase from Bacillus subtilis, in DNA mutagenesis. J Biol Chem 279: 1757-1767.
49. Webb BL, Cox MM, Inman RB (1997) Recombinational DNA repair: the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell 91: 347-356.
50. Fernandez S, Ayora S, Alonso JC (2000) Bacillus subtilis homologous recombination: genes and products. Res Microbiol 151: 481-486.
51. Arad G, Hendel A, Urbanke C, Curth U, Livneh Z (2008) Single-stranded DNA-binding protein recruits DNA polymerase V to primer termini on RecAcoated DNA. J Biol Chem 283: 8274-8282.
52. Zeghouf M, Li J, Butland G, Borkowska A, Canadien V, et al. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3: 463-468.
53. Msadek T, Kunst F, Henner D, Klier A, Rapoport G, et al. (1990) Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172: 824-834.
54. Davidsen T, Beck E, Ganapathy A, Montgomery R, Zafar N, et al. (2010) The comprehensive microbial resource. Nucleic Acids Res 38: D340-D345. SSB and Replication Fork Maintenance