Replication fork arrest is a recognized source of genetic instability, and transcription is one of the most prominent causes of replication impediment. We analyze here the requirement for recombination proteins in Escherichia coli when replication–transcription head-on collisions are induced at a specific site by the inversion of a highly expressed ribosomal operon (rrn). RecBC is the only recombination protein required for cell viability under these conditions of increased replication-transcription collisions. In its absence, fork breakage occurs at the site of collision, and the resulting linear DNA is not repaired and is slowly degraded by the RecJ exonuclease. Lethal fork breakage is also observed in cells that lack RecA and RecD, i.e. when both homologous recombination and the potent exonuclease V activity of the RecBCD complex are inactivated, with a slow degradation of the resulting linear DNA by the combined action of the RecBC helicase and the RecJ exonuclease. The sizes of the major linear fragments indicate that DNA degradation is slowed down by the encounter with another rrn operon. The amount of linear DNA decreases nearly two-fold when the Holliday junction resolvase RuvABC is inactivated in recB, as well as in recA recD mutants, indicating that part of the linear DNA is formed by resolution of a Holliday junction. Our results suggest that replication fork reversal occurs after replication–transcription head-on collision, and we propose that it promotes the action of the accessory replicative helicases that dislodge the obstacle.
Vyšlo v časopise: Replication Fork Reversal after Replication–Transcription Collision. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002622 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002622
1. BranzeiDFoianiM 2007 Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6 994 1003
2. LambertSFrogetBCarrAM 2007 Arrested replication fork processing: interplay between checkpoints and recombination. DNA Repair (Amst) 6 1042 1061
3. HellerRCMariansKJ 2006 Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7 932 943
4. GabbaiCBMariansKJ 2010 Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair (Amst) 9 202 209
5. MichelBGromponeGFloresMJBidnenkoV 2004 Multiple pathways process stalled replication forks. Proc Natl Acad Sci USA 101 12783 12788
6. MichelBBoubakriHBaharogluZLemassonMLestiniR 2007 Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst) 6 967 980
7. McGlynnP 2011 Helicases that underpin replication of protein-bound DNA in Escherichia coli. Biochem Soc Trans 39 606 610
8. BoubakriHde SeptenvilleALVigueraEMichelB 2010 The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29 145 157
9. FrenchS 1992 Consequences of Replication Fork Movement Through Transcription Units In Vivo. Science 258 1362 1365
10. BrewerBJ 1988 When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53 679 686
11. LiuBAlbertsBM 1995 Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex. Science 267 1131 1137
12. ViletteDUzestMEhrlichSDMichelB 1992 DNA transcription and repressor binding affect deletion formation in Escherichia coli plasmids. EMBO J 11 3629 3634
13. ViletteDEhrlichSDMichelB 1995 Transcription-induced deletions in Escherichia coli plasmids. Mol Microbiol 17 493 504
14. AzvolinskyADunawaySTorresJZBesslerJBZakianVA 2006 The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev 20 3104 3116
15. MirkinEVMirkinSM 2007 Replication fork stalling at natural impediments. Microbiol Mol Biol Rev 71 13 35
16. WangJDBerkmenMBGrossmanAD 2007 Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis. Proc Natl Acad Sci U S A 104 5608 5613
17. MerrikhHMachonCGraingerWHGrossmanADSoultanasP 2011 Co-directional replication-transcription conflicts lead to replication restart. Nature 470 554 557
18. CourcelleJHanawaltPC 2003 RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37 611 646
19. SeigneurMBidnenkoVEhrlichSDMichelB 1998 RuvAB acts at arrested replication forks. Cell 95 419 430
20. GuarinoEJimenez-SanchezAGuzmanEC 2007 Defective ribonucleoside diphosphate reductase impairs replication fork progression in Escherichia coli. J Bacteriol 189 3496 3501
21. SalgueroIGuarinoEGuzmanEC 2011 RecA-dependent replication in the nrdA101(Ts) mutant of Escherichia coli under restrictive conditions. J Bacteriol 193 2851 2860
22. KuzminovA 1999 Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63 751 813
23. LukasLKuzminovA 2006 Chromosomal fragmentation is the major consequence of the rdgB defect in Escherichia coli. Genetics 172 1359 1362
24. TingHKouzminovaEAKuzminovA 2008 Synthetic lethality with the dut defect in Escherichia coli reveals layers of DNA damage of increasing complexity due to uracil incorporation. J Bacteriol 190 5841 5854
25. FloresMJBierneHEhrlichSDMichelB 2001 Impairment of lagging strand synthesis triggers the formation of a RuvABC substrate at replication forks. EMBO J 20 619 629
26. McGlynnPLloydRG 2000 Modulation of RNA polymerase by (P)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell 101 35 45
27. McGlynnPLloydRG 1999 RecG helicase activity at three - and four-strand DNA structures. Nucleic Acids Res 27 3049 3056
28. DonaldsonJRCourcelleCTCourcelleJ 2004 RuvAB and RecG are not essential for the recovery of DNA synthesis following UV-induced DNA damage in Escherichia coli. Genetics 166 1631 1640
29. RudolphCJUptonALHarrisLLloydRG 2009 Pathological replication in cells lacking RecG DNA translocase. Mol Microbiol 73 352 366
30. RudolphCJUptonALBriggsGSLloydRG 2010 Is RecG a general guardian of the bacterial genome? DNA Repair (Amst) 9 210 223
31. KhanSRKuzminovA 2012 Replication forks stalled at UV-lesions are rescued via RecA - and RuvABC-catalyzed disintegration in Escherichia coli. J Biol Chem 287 6250 6265
32. BaharogluZLestiniRDuigouSMichelB 2010 RNA polymerase mutations that facilitate replication progression in the rep uvrD recF mutant lacking two accessory replicative helicases. Mol Microbiol 77 324 336
33. GuyCPAtkinsonJGuptaMKMahdiAAGwynnEJ 2009 Rep provides a second motor at the replisome to promote duplication of protein-bound DNA. Mol Cell 36 654 666
34. LaneHEDenhardtDT 1975 The rep mutation. IV. Slower movement of replication forks in Escherichia coli rep strains. J Mol Biol 97 99 112
35. AtkinsonJGuptaMKRudolphCJBellHLloydRG 2010 Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. Nucleic Acids Res 39 949 957
36. Taucher-ScholtzGAbdel-MonemMHoffmann-BerlingH 1983 Functions of helicases in E. coli. CozzarelliNR Mechanisms of DNA replication and recombination New york Alan Liss Inc 65 76
37. SelbyCPSancarA 1993 Molecular Mechanism of Transcription-Repair Coupling. Science 260 53 58
38. ParkJSMarrMTRobertsJW 2002 E. coli Transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109 757 767
39. PomerantzRTO'DonnellM 2010 Direct restart of a replication fork stalled by a head-on RNA polymerase. Science 327 590 592
40. MasseEPhoenixPDroletM 1997 DNA topoisomerases regulate R-loop formation during transcription of the rrnB operon in Escherichia coli. J Biol Chem 272 12816 12823
41. PostowLUllspergerCKellerRWBustamanteCVologodskiiAV 2001 Positive torsional strain causes the formation of a four-way junction at replication forks. J Biol Chem 276 2790 2796
42. HanESCooperDLPerskyNSSuteraVAJrWhitakerRD 2006 RecJ exonuclease: substrates, products and interaction with SSB. Nucleic Acids Res 34 1084 1091
43. KouzminovaEAKuzminovA 2008 Patterns of chromosomal fragmentation due to uracil-DNA incorporation reveal a novel mechanism of replication-dependent double-stranded breaks. Mol Microbiol 68 202 215
44. BidnenkoVEhrlichSDMichelB 2002 Replication fork collapse at replication terminator sequences. EMBO J 21 3898 3907
45. NordmanJSkovgaardOWrightA 2007 A novel class of mutations that affect DNA replication in E. coli. Mol Microbiol 64 125 138
46. DermicD 2006 Functions of multiple exonucleases are essential for cell viability, DNA repair and homologous recombination in recD mutants of Escherichia coli. Genetics 172 2057 2069
47. RinkenRThomsBWackernagelW 1992 Evidence That recBC-Dependent Degradation of Duplex DNA in Escherichia-Coli recD Mutants Involves DNA Unwinding. Journal of Bacteriology 174 5424 5429
48. HandaNMorimatsuKLovettSTKowalczykowskiSC 2009 Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev 23 1234 1245
49. SpiesMAmitaniIBaskinRJKowalczykowskiSC 2007 RecBCD enzyme switches lead motor subunits in response to chi recognition. Cell 131 694 705
50. GromponeGSeigneurMEhrlichSDMichelB 2002 Replication fork reversal in DNA polymerase III mutants of Escherichia coli: a role for the beta clamp. Mol Microbiol 44 1331 1339
51. WashburnRSGottesmanME 2011 Transcription termination maintains chromosome integrity. Proc Natl Acad Sci U S A 108 792 797
52. SkarstadKBoyeE 1993 Degradation of Individual Chromosomes in RecA Mutants of Escherichia-coli. J Bacteriol 175 5505 5509
53. GanWGuanZLiuJGuiTShenK 2011 R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25 2041 2056
54. Gomez-GonzalezBGarcia-RubioMBermejoRGaillardHShirahigeK 2011 Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J 30 3106 3119
55. VoloshinONCamerini-OteroRD 2007 The DinG protein from Escherichia coli is a structure-specific helicase. J Biol Chem 282 18437 18447
56. BaharogluZPetranovicMFloresMJMichelB 2006 RuvAB is essential for replication forks reversal in certain replication mutants. EMBO J 25 596 604
57. BidnenkoVLestiniRMichelB 2006 The Escherichia coli UvrD helicase is essential for Tus removal during recombination-dependent replication restart from Ter sites. Mol Microbiol 62 382 396
58. DatsenkoKAWannerBL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 6640 6645
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
