Roles of Type 1A Topoisomerases in Genome Maintenance in


DNA topoisomerases are ubiquitous enzymes that solve the topological problems associated with replication, transcription and recombination. Eukaryotic enzymes of the type 1A family work with RecQ-like helicases such as BLM and Sgs1 and are involved in genome maintenance. Interestingly, E. coli topo I, a type 1A enzyme and the first topoisomerase to be discovered, appears to have distinct cellular functions that are related to supercoiling regulation and to the inhibition of R-loop formation. Here we present data strongly suggesting that these cellular functions are required to inhibit inappropriate replication originating from either oriC, the normal origin of replication, or R-loops that can otherwise lead to severe chromosome segregation defects. Avoiding such inappropriate replication appears to be a key cellular function for genome maintenance, since the other E. coli type 1A topo, topo III, is also involved. Furthermore, our data suggest that bacterial type 1A topos, like their eukaryotic counterparts, can act with RecQ in genome maintenance. Altogether, our data provide new insight into the role of type 1A topos in genome maintenance and reveal an interplay between these enzymes and R-loops, structures that can also significantly affect the stability of the genome as recently shown in numerous studies.


Vyšlo v časopise: Roles of Type 1A Topoisomerases in Genome Maintenance in. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004543
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004543

Souhrn

DNA topoisomerases are ubiquitous enzymes that solve the topological problems associated with replication, transcription and recombination. Eukaryotic enzymes of the type 1A family work with RecQ-like helicases such as BLM and Sgs1 and are involved in genome maintenance. Interestingly, E. coli topo I, a type 1A enzyme and the first topoisomerase to be discovered, appears to have distinct cellular functions that are related to supercoiling regulation and to the inhibition of R-loop formation. Here we present data strongly suggesting that these cellular functions are required to inhibit inappropriate replication originating from either oriC, the normal origin of replication, or R-loops that can otherwise lead to severe chromosome segregation defects. Avoiding such inappropriate replication appears to be a key cellular function for genome maintenance, since the other E. coli type 1A topo, topo III, is also involved. Furthermore, our data suggest that bacterial type 1A topos, like their eukaryotic counterparts, can act with RecQ in genome maintenance. Altogether, our data provide new insight into the role of type 1A topos in genome maintenance and reveal an interplay between these enzymes and R-loops, structures that can also significantly affect the stability of the genome as recently shown in numerous studies.


Zdroje

1. ChenSH, ChanNL, HsiehTS (2013) New mechanistic and functional insights into DNA topoisomerases. Annu Rev Biochem 82: 139–170.

2. ChampouxJJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369–413.

3. WangJC (1971) Interaction between DNA and an Escherichia coli protein omega. J Mol Biol 55: 523–533.

4. KirkegaardK, WangJC (1985) Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J Mol Biol 185: 625–637.

5. LiuLF, WangJC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84: 7024–7027.

6. GellertM, MizuuchiK, O'DeaMH, NashHA (1976) DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci U S A 73: 3872–3876.

7. DiNardoS, VoelkelKA, SternglanzR, ReynoldsAE, WrightA (1982) Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31: 43–51.

8. PrussGJ, ManesSH, DrlicaK (1982) Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31: 35–42.

9. ChengB, ZhuCX, JiC, AhumadaA, Tse-DinhYC (2003) Direct interaction between Escherichia coli RNA polymerase and the zinc ribbon domains of DNA topoisomerase I. J Biol Chem 278: 30705–30710.

10. DroletM (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59: 723–730.

11. DroletM, PhoenixP, MenzelR, MasseE, LiuLF, et al. (1995) Overexpression of RNase H partially complements the growth defect of an Escherichia coli delta topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc Natl Acad Sci U S A 92: 3526–3530.

12. DroletM, BiX, LiuLF (1994) Hypernegative supercoiling of the DNA template during transcription elongation in vitro. J Biol Chem 269: 2068–2074.

13. PhoenixP, RaymondMA, MasseE, DroletM (1997) Roles of DNA topoisomerases in the regulation of R-loop formation in vitro. J Biol Chem 272: 1473–1479.

14. MasseE, PhoenixP, DroletM (1997) DNA topoisomerases regulate R-loop formation during transcription of the rrnB operon in Escherichia coli. J Biol Chem 272: 12816–12823.

15. MasseE, DroletM (1999) Escherichia coli DNA topoisomerase I inhibits R-loop formation by relaxing transcription-induced negative supercoiling. J Biol Chem 274: 16659–16664.

16. BaakliniI, UsongoV, NolentF, SanscartierP, HraikyC, et al. (2008) Hypernegative supercoiling inhibits growth by causing RNA degradation. J Bacteriol 190: 7346–7356.

17. UsongoV, NolentF, SanscartierP, TanguayC, BroccoliS, et al. (2008) Depletion of RNase HI activity in Escherichia coli lacking DNA topoisomerase I leads to defects in DNA supercoiling and segregation. Mol Microbiol 69: 968–981.

18. ZechiedrichEL, KhodurskyAB, BachellierS, SchneiderR, ChenD, et al. (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275: 8103–8113.

19. HraikyC, RaymondMA, DroletM (2000) RNase H overproduction corrects a defect at the level of transcription elongation during rRNA synthesis in the absence of DNA topoisomerase I in Escherichia coli. J Biol Chem 275: 11257–11263.

20. El HageA, FrenchSL, BeyerAL, TollerveyD (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 24: 1546–1558.

21. WangM, WeissM, SimonovicM, HaertingerG, SchrimpfSP, et al. (2012) PaxDb, a database of protein abundance averages across all three domains of life. Mol Cell Proteomics 11: 492–500.

22. RuiS, Tse-DinhYC (2003) Topoisomerase function during bacterial responses to environmental challenge. Front Biosci 8: d256–263.

23. ChengB, RuiS, JiC, GongVW, Van DykTK, et al. (2003) RNase H overproduction allows the expression of stress-induced genes in the absence of topoisomerase I. FEMS Microbiol Lett 221: 237–242.

24. WeinreichMD, YigitH, ReznikoffWS (1994) Overexpression of the Tn5 transposase in Escherichia coli results in filamentation, aberrant nucleoid segregation, and cell death: analysis of E. coli and transposase suppressor mutations. J Bacteriol 176: 5494–5504.

25. YigitH, ReznikoffWS (1999) Escherichia coli DNA topoisomerase I copurifies with Tn5 transposase, and Tn5 transposase inhibits topoisomerase I. J Bacteriol 181: 3185–3192.

26. DanilovaO, Reyes-LamotheR, PinskayaM, SherrattD, PossozC (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65: 1485–1492.

27. LouarnJ, BoucheJP, PatteJ, LouarnJM (1984) Genetic inactivation of topoisomerase I suppresses a defect in initiation of chromosome replication in Escherichia coli. Mol Gen Genet 195: 170–174.

28. KaguniJM, KornbergA (1984) Topoisomerase I confers specificity in enzymatic replication of the Escherichia coli chromosomal origin. J Biol Chem 259: 8578–8583.

29. DiGateRJ, MariansKJ (1988) Identification of a potent decatenating enzyme from Escherichia coli. J Biol Chem 263: 13366–13373.

30. LopezCR, YangS, DeiblerRW, RaySA, PenningtonJM, et al. (2005) A role for topoisomerase III in a recombination pathway alternative to RuvABC. Mol Microbiol 58: 80–101.

31. LiZ, MondragonA, HiasaH, MariansKJ, DiGateRJ (2000) Identification of a unique domain essential for Escherichia coli DNA topoisomerase III-catalysed decatenation of replication intermediates. Mol Microbiol 35: 888–895.

32. DiGateRJ, MariansKJ (1989) Molecular cloning and DNA sequence analysis of Escherichia coli topB, the gene encoding topoisomerase III. J Biol Chem 264: 17924–17930.

33. Perez-CheeksBA, LeeC, HayamaR, MariansKJ (2012) A role for topoisomerase III in Escherichia coli chromosome segregation. Mol Microbiol 86: 1007–1022.

34. UsongoV, TanguayC, NolentF, BessongJE, DroletM (2013) Interplay between type 1A topoisomerases and gyrase in chromosome segregation in Escherichia coli. J Bacteriol 195: 1758–1768.

35. SuskiC, MariansKJ (2008) Resolution of converging replication forks by RecQ and topoisomerase III. Mol Cell 30: 779–789.

36. HarmonFG, DiGateRJ, KowalczykowskiSC (1999) RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol Cell 3: 611–620.

37. HarmonFG, BrockmanJP, KowalczykowskiSC (2003) RecQ helicase stimulates both DNA catenation and changes in DNA topology by topoisomerase III. J Biol Chem 278: 42668–42678.

38. WallisJW, ChrebetG, BrodskyG, RolfeM, RothsteinR (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409–419.

39. GangloffS, McDonaldJP, BendixenC, ArthurL, RothsteinR (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391–8398.

40. GangloffS, de MassyB, ArthurL, RothsteinR, FabreF (1999) The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J 18: 1701–1711.

41. ShorE, GangloffS, WagnerM, WeinsteinJ, PriceG, et al. (2002) Mutations in homologous recombination genes rescue top3 slow growth in Saccharomyces cerevisiae. Genetics 162: 647–662.

42. WuL, DaviesSL, NorthPS, GoulaouicH, RiouJF, et al. (2000) The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem 275: 9636–9644.

43. ChenSH, WuCH, PlankJL, HsiehTS (2012) Essential functions of C terminus of Drosophila Topoisomerase IIIalpha in double holliday junction dissolution. J Biol Chem 287: 19346–19353.

44. PlankJL, WuJ, HsiehTS (2006) Topoisomerase IIIalpha and Bloom's helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc Natl Acad Sci U S A 103: 11118–11123.

45. WuL, HicksonID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870–874.

46. CejkaP, PlankJL, BachratiCZ, HicksonID, KowalczykowskiSC (2010) Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol 17: 1377–1382.

47. BroccoliS, PhoenixP, DroletM (2000) Isolation of the topB gene encoding DNA topoisomerase III as a multicopy suppressor of topA null mutations in Escherichia coli. Mol Microbiol 35: 58–68.

48. ZhuQ, PongpechP, DiGateRJ (2001) Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli. Proc Natl Acad Sci U S A 98: 9766–9771.

49. MasseE, DroletM (1999) Relaxation of transcription-induced negative supercoiling is an essential function of Escherichia coli DNA topoisomerase I. J Biol Chem 274: 16654–16658.

50. MasseE, DroletM (1999) R-loop-dependent hypernegative supercoiling in Escherichia coli topA mutants preferentially occurs at low temperatures and correlates with growth inhibition. J Mol Biol 294: 321–332.

51. MagnerDB, BlankschienMD, LeeJA, PenningtonJM, LupskiJR, et al. (2007) RecQ promotes toxic recombination in cells lacking recombination intermediate-removal proteins. Mol Cell 26: 273–286.

52. LestiniR, MichelB (2008) UvrD and UvrD252 counteract RecQ, RecJ, and RecFOR in a rep mutant of Escherichia coli. J Bacteriol 190: 5995–6001.

53. SeigneurM, BidnenkoV, EhrlichSD, MichelB (1998) RuvAB acts at arrested replication forks. Cell 95: 419–430.

54. MirandaA, KuzminovA (2003) Chromosomal lesion suppression and removal in Escherichia coli via linear DNA degradation. Genetics 163: 1255–1271.

55. KogomaT (1997) Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev 61: 212–238.

56. Kellenberger-GujerG, PodhajskaAJ, CaroL (1978) A cold sensitive dnaA mutant of E. coli which overinitiates chromosome replication at low temperature. Mol Gen Genet 162: 9–16.

57. StepankiwN, KaidowA, BoyeE, BatesD (2009) The right half of the Escherichia coli replication origin is not essential for viability, but facilitates multi-forked replication. Mol Microbiol 74: 467–479.

58. LeonardAC, GrimwadeJE (2011) Regulation of DnaA assembly and activity: taking directions from the genome. Annu Rev Microbiol 65: 19–35.

59. GabbaiCB, MariansKJ (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.

60. LarkCA, RiaziJ, LarkKG (1978) dnaT, dominant conditional-lethal mutation affecting DNA replication in Escherichia coli. J Bacteriol 136: 1008–1017.

61. SandlerSJ (2005) Requirements for replication restart proteins during constitutive stable DNA replication in Escherichia coli K-12. Genetics 169: 1799–1806.

62. BaakliniI, HraikyC, RalluF, Tse-DinhYC, DroletM (2004) RNase HI overproduction is required for efficient full-length RNA synthesis in the absence of topoisomerase I in Escherichia coli. Mol Microbiol 54: 198–211.

63. GromponeG, EhrlichSD, MichelB (2003) Replication restart in gyrB Escherichia coli mutants. Mol Microbiol 48: 845–854.

64. AnupamaK, LeelaJK, GowrishankarJ (2011) Two pathways for RNase E action in Escherichia coli in vivo and bypass of its essentiality in mutants defective for Rho-dependent transcription termination. Mol Microbiol 82: 1330–1348.

65. BouvierM, CarpousisAJ (2011) A tale of two mRNA degradation pathways mediated by RNase E. Mol Microbiol 82: 1305–1310.

66. NordmanJ, SkovgaardO, WrightA (2007) A novel class of mutations that affect DNA replication in E. coli. Mol Microbiol 64: 125–138.

67. YaoNY, O'DonnellM (2008) Replisome dynamics and use of DNA trombone loops to bypass replication blocks. Mol Biosyst 4: 1075–1084.

68. MarceauAH, BahngS, MassoniSC, GeorgeNP, SandlerSJ, et al. (2011) Structure of the SSB-DNA polymerase III interface and its role in DNA replication. EMBO J 30: 4236–4247.

69. ChuWK, HicksonID (2009) RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer 9: 644–654.

70. WuL, BachratiCZ, OuJ, XuC, YinJ, et al. (2006) BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc Natl Acad Sci U S A 103: 4068–4073.

71. SikderD, UnniramanS, BhaduriT, NagarajaV (2001) Functional cooperation between topoisomerase I and single strand DNA-binding protein. J Mol Biol 306: 669–679.

72. ForterreP, GribaldoS, GadelleD, SerreMC (2007) Origin and evolution of DNA topoisomerases. Biochimie 89: 427–446.

73. WuL, ChanKL, RalfC, BernsteinDA, GarciaPL, et al. (2005) The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J 24: 2679–2687.

74. MichelB, EhrlichSD, UzestM (1997) DNA double-strand breaks caused by replication arrest. EMBO J 16: 430–438.

75. De SeptenvilleAL, DuigouS, BoubakriH, MichelB (2012) Replication fork reversal after replication-transcription collision. PLoS Genet 8: e1002622.

76. FunnellBE, BakerTA, KornbergA (1986) Complete enzymatic replication of plasmids containing the origin of the Escherichia coli chromosome. J Biol Chem 261: 5616–5624.

77. FilutowiczM (1980) Requirement of DNA gyrase for the initiation of chromosome replication in Escherichia coli K-12. Mol Gen Genet 177: 301–309.

78. JohnsenL, WeigelC, von KriesJ, MollerM, SkarstadK (2010) A novel DNA gyrase inhibitor rescues Escherichia coli dnaAcos mutant cells from lethal hyperinitiation. J Antimicrob Chemother 65: 924–930.

79. DuderstadtKE, ChuangK, BergerJM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478: 209–213.

80. OzakiS, KatayamaT (2012) Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation. Nucleic Acids Res 40: 1648–1665.

81. OgawaT, PickettGG, KogomaT, KornbergA (1984) RNase H confers specificity in the dnaA-dependent initiation of replication at the unique origin of the Escherichia coli chromosome in vivo and in vitro. Proc Natl Acad Sci U S A 81: 1040–1044.

82. HongX, CadwellGW, KogomaT (1995) Escherichia coli RecG and RecA proteins in R-loop formation. EMBO J 14: 2385–2392.

83. RudolphCJ, UptonAL, StockumA, NieduszynskiCA, LloydRG (2013) Avoiding chromosome pathology when replication forks collide. Nature 500: 608–611.

84. YangY, McBrideKM, HensleyS, LuY, ChedinF, et al. (2014) Arginine methylation facilitates the recruitment of TOP3B to chromatin to prevent R loop accumulation. Mol Cell 53: 484–497.

85. LarsenRA, WilsonMM, GussAM, MetcalfWW (2002) Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch Microbiol 178: 193–201.

86. KasaharaM, ClikemanJA, BatesDB, KogomaT (2000) RecA protein-dependent R-loop formation in vitro. Genes Dev 14: 360–365.

87. ZaitsevEN, KowalczykowskiSC (2000) A novel pairing process promoted by Escherichia coli RecA protein: inverse DNA and RNA strand exchange. Genes Dev 14: 740–749.

88. DugginIG, WakeRG, BellSD, HillTM (2008) The replication fork trap and termination of chromosome replication. Mol Microbiol 70: 1323–1333.

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