Mu is both a transposable element and a temperate bacteriophage. During lytic growth, it amplifies its genome by replicative transposition. During infection, it integrates into the Escherichia coli chromosome through a mechanism not requiring extensive DNA replication. In the latter pathway, the transposition intermediate is repaired by transposase-mediated resecting of the 5′ flaps attached to the ends of the incoming Mu genome, followed by filling the remaining 5 bp gaps at each end of the Mu insertion. It is widely assumed that the gaps are repaired by a gap-filling host polymerase. Using the E. coli Keio Collection to screen for mutants defective in recovery of stable Mu insertions, we show in this study that the gaps are repaired by the machinery responsible for the repair of double-strand breaks in E. coli—the replication restart proteins PriA-DnaT and homologous recombination proteins RecABC. We discuss alternate models for recombinational repair of the Mu gaps.
Vyšlo v časopise: Mu Insertions Are Repaired by the Double-Strand Break Repair Pathway of. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002642 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002642
1. CraigNLCraigieRGellertMLambowitzAM 2002 Mobile DNA II ASM Press Washington, D.C.
2. SymondsNToussaintAVan de PuttePHoweMM 1987 Phage Mu Cold Spring Harbor, New York Cold Spring Harbor Laboratory
3. ChaconasGHarsheyRM 2002 Transposition of phage Mu DNA. MobileDNAIICraigNLCraigieRGellertMLambowitzAM Washington DC ASM Press 384 402
4. MizuuchiK 1992 Transpositional recombination: mechanistic insights from studies of Mu and other elements. Annu Rev Biochem 61 1011 1051
5. NakaiHDoseevaVJonesJM 2001 Handoff from recombinase to replisome: insights from transposition. Proc Natl Acad Sci U S A 98 8247 8254
6. AkroydJESymondsN 1983 Evidence for a conservative pathway of transposition of bacteriophage Mu. Nature 303 84 86
7. HarsheyRM 1984 Transposition without duplication of infecting bacteriophage Mu DNA. Nature 311 580 581
8. LiebartJCGhelardiniPPaolozziL 1982 Conservative integration of bacteriophage Mu DNA into pBR322 plasmid. Proc Natl Acad Sci U S A 79 4362 4366
9. HarsheyRMBukhariAI 1983 Infecting bacteriophage Mu DNA forms a circular DNA-protein complex. J Mol Biol 167 427 441
10. PuspursAHTrunNJReeveJN 1983 Bacteriophage Mu DNA circularizes following infection of Escherichia coli. EMBO J 2 345 352
11. GloorGChaconasG 1986 The bacteriophage Mu N gene encodes the 64-kDa virion protein which is injected with, and circularizes, infecting Mu DNA. J Biol Chem 261 16682 16688
12. AuTKAgrawalPHarsheyRM 2006 Chromosomal integration mechanism of infecting Mu virion DNA. J Bacteriol 188 1829 1834
13. ChoiWHarsheyRM 2010 DNA repair by the cryptic endonuclease activity of Mu transposase. Proc Natl Acad Sci U S A 107 10014 10019
14. WuZChaconasG 1995 A novel DNA binding and nuclease activity in domain III of Mu transposase: evidence for a catalytic region involved in donor cleavage. EMBO J 14 3835 3843
15. AbdelhakimAHOakesECSauerRTBakerTA 2008 Unique contacts direct high-priority recognition of the tetrameric Mu transposase-DNA complex by the AAA+ unfoldase ClpX. Mol Cell 30 39 50
16. BabaTAraTHasegawaMTakaiYOkumuraY 2006 Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2 2006.0008
17. HigginsNPCollierDAKilpatrickMWKrauseHM 1989 Supercoiling and integration host factor change the DNA conformation and alter the flow of convergent transcription in phage Mu. J Biol Chem 264 3035 3042
18. Mhammedi-AlaouiAPatoMGamaMJToussaintA 1994 A new component of bacteriophage Mu replicative transposition machinery: the Escherichia coli ClpX protein. Mol Microbiol 11 1109 1116
19. ChaconasGGloorGMillerJLKennedyDLGiddensEB 1984 Transposition of bacteriophage Mu DNA: expression of the A and B proteins from lambda pL and analysis of infecting Mu DNA. Cold Spring Harb Symp Quant Biol 49 279 284
20. MannaDBreierAMHigginsNP 2004 Microarray analysis of transposition targets in Escherichia coli: the impact of transcription. Proc Natl Acad Sci U S A 101 9780 9785
21. GeJLouZCuiHShangLHarsheyRM 2011 Analysis of phage Mu DNA transposition by whole-genome Escherichia coli tiling arrays reveals a complex relationship to distribution of target selection protein B, transcription and chromosome architectural elements. J Biosci 36 587 601
22. ChaconasGGiddensEBMillerJLGloorG 1985 A truncated form of the bacteriophage Mu B protein promotes conservative integration, but not replicative transposition, of Mu DNA. Cell 41 857 865
23. O'DayKJSchultzDWEricsenWRawlukkLHoweMM 1978 A search for integration deficient mutants of bacteriophage Mu-1. Microbiology. SchlessingerD Washington, D.C. ASM Publications 48 51
24. JonesJMNakaiH 1997 The φX174-type primosome promotes replisome assembly at the site of recombination in bacteriophage Mu transposition. EMBO J 16 6886 6895
25. MullerKHTrustTJKayWW 1988 Unmasking of bacteriophage Mu lipopolysaccharide receptors in Salmonella enteritidis confers sensitivity to Mu and permits Mu mutagenesis. J Bacteriol 170 1076 1081
26. SandulacheRPrehmPKampD 1984 Cell wall receptor for bacteriophage Mu G(+). J Bacteriol 160 299 303
27. MorganGJHatfullGFCasjensSHendrixRW 2002 Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus. J Mol Biol 317 337 359
28. TaylorAL 1963 Bacteriophage-induced mutations in E. coli. Proc Natl Acad Sci 50 1043 1051
29. 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
30. SandlerSJMariansKJZavitzKHCoutuJParentMA 1999 dnaC mutations suppress defects in DNA replication - and recombination-associated functions in priB and priC double mutants in Escherichia coli K-12. Mol Microbiol 34 91 101
31. JonesJMNakaiH 1999 Duplex opening by primosome protein PriA for replisome assembly on a recombination intermediate. J Mol Biol 289 503 516
32. LeeEHKornbergA 1991 Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n' protein. Proc Natl Acad Sci U S A 88 3029 3032
33. NursePZavitzKHMariansKJ 1991 Inactivation of the Escherichia coli priA DNA replication protein induces the SOS response. J Bacteriol 173 6686 6693
34. McCoolJDFordCCSandlerSJ 2004 A dnaT mutant with phenotypes similar to those of a priA2::kan mutant in Escherichia coli K-12. Genetics 167 569 578
35. McCoolJDLongEPetrosinoJFSandlerHARosenbergSM 2004 Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol 53 1343 1357
36. KuzminovA 1999 Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63 751 813
37. LittleJWEdmistonSHPacelliLZMountDW 1980 Cleavage of the Escherichia coli lexA protein by the recA protease. Proc Natl Acad Sci U S A 77 3225 3229
38. HughesKTOliveraBMRothJR 1987 Rec dependence of Mu transposition from P22-transduced fragments. J Bacteriol 169 403 409
39. SontiRVKeatingDHRothJR 1993 Lethal transposition of Mud phages in Rec - strains of Salmonella typhimurium. Genetics 133 17 28
40. LauderSDKowalczykowskiSC 1993 Negative co-dominant inhibition of recA protein function. Biochemical properties of the recA1, recA13 and recA56 proteins and the effect of recA56 protein on the activities of the wild-type recA protein function in vitro. J Mol Biol 234 72 86
41. YamamotoNNakahigashiKNakamichiTYoshinoMTakaiY 2009 Update on the Keio collection of Escherichia coli single-gene deletion mutants. Mol Syst Biol 5 335
42. SandlerSJ 2005 Requirements for replication restart proteins during constitutive stable DNA replication in Escherichia coli K-12. Genetics 169 1799 1806
43. ZavitzKHMariansKJ 1992 ATPase-deficient mutants of the Escherichia coli DNA replication protein PriA are capable of catalyzing the assembly of active primosomes. J Biol Chem 267 6933 6940
44. ZavitzKHMariansKJ 1993 Helicase-deficient cysteine to glycine substitution mutants of Escherichia coli replication protein PriA retain single-stranded DNA-dependent ATPase activity. Zn2+ stimulation of mutant PriA helicase and primosome assembly activities. J Biol Chem 268 4337 4346
45. SandlerSJMcCoolJDDoTTJohansenRU 2001 PriA mutations that affect PriA-PriC function during replication restart. Mol Microbiol 41 697 704
46. SandlerSJSamraHSClarkAJ 1996 Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. Genetics 143 5 13
47. LiuJXuLSandlerSJMariansKJ 1999 Replication fork assembly at recombination intermediates is required for bacterial growth. Proc Natl Acad Sci U S A 96 3552 3555
48. SmithJADanielR 2006 Following the path of the virus: the exploitation of host DNA repair mechanisms by retroviruses. ACS Chem Biol 1 217 226
49. SuzukiJYamaguchiKKajikawaMIchiyanagiKAdachiN 2009 Genetic evidence that the non-homologous end-joining repair pathway is involved in LINE retrotransposition. PLoS Genet 5 e1000461 doi:10.1371/journal.pgen.1000461
50. GasiorSLWakemanTPXuBDeiningerPL 2006 The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol 357 1383 1393
51. YangYXGuenVRichardJCohenEABerthouxL 2010 Cell context-dependent involvement of ATR in early stages of retroviral replication. Virology 396 272 279
52. MizuuchiK 1984 Mechanism of transposition of bacteriophage Mu: polarity of the strand transfer reaction at the initiation of transposition. Cell 39 395 404
53. NorthSHNakaiH 2005 Host factors that promote transpososome disassembly and the PriA-PriC pathway for restart primosome assembly. Mol Microbiol 56 1601 1616
54. JonesJMNakaiH 2000 PriA and phage T4 gp59: factors that promote DNA replication on forked DNA substrates Mol Microbiol 36 519 527
55. LevchenkoILuoLBakerTA 1995 Disassembly of the Mu transposase tetramer by the Clpx chaperone. Genes Dev 9 2399 2408
56. KruklitisRWeltyDJNakaiH 1996 Clpx protein of Escherichia coli activates bacteriophage Mu transposase in the strand transfer complex for initiation of Mu DNA synthesis. EMBO J 15 935 944
57. AbdelhakimAHSauerRTBakerTA 2010 The AAA+ ClpX machine unfolds a keystone subunit to remodel the Mu transpososome. Proc Natl Acad Sci U S A 107 2437 2442
58. NorthSHKirtlandSENakaiH 2007 Translation factor IF2 at the interface of transposition and replication by the PriA-PriC pathway. Mol Microbiol 66 1566 1578
59. McGlynnPLloydRG 2002 Recombinational repair and restart of damaged replication forks. Nat Rev Mol Cell Biol 3 859 870
60. MichelBGromponeGFloresMJBidnenkoV 2004 Multiple pathways process stalled replication forks. Proc Natl Acad Sci U S A 101 12783 12788
61. NakaiHTaylorAL 1985 Host DNA replication forks are not preferred targets for bacteriophage Mu transposition. J Bacteriol 163 282 290
62. RegisterJC3rdGriffithJ 1985 The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem 260 12308 12312
63. BorkJMCoxMMInmanRB 2001 The RecOR proteins modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J 20 7313 7322
64. Gumbiner-RussoLMRosenbergSM 2007 Physical analyses of E. coli heteroduplex recombination products in vivo: on the prevalence of 5′ and 3′ patches. PLoS ONE 2 e1242 doi:10.1371/journal.pone.0001242
65. McCoolJDSandlerSJ 2001 Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2::kan mutant. Proc Natl Acad Sci U S A 98 8203 8210
66. BoonsombatRYehSPMilneASandlerSJ 2006 A novel dnaC mutation that suppresses priB rep mutant phenotypes in Escherichia coli K-12. Mol Microbiol 60 973 983
67. 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
68. KonradEB 1977 Method for the isolation of Escherichia coli mutants with enhanced recombination between chromosomal duplications. J Bacteriol 130 167 172
69. ZiegJKushnerSR 1977 Analysis of genetic recombination between two partially deleted lactose operons of Escherichia coli K-12. J Bacteriol 131 123 132
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