Regulation of Sister Chromosome Cohesion by the Replication Fork Tracking Protein SeqA

English version České info

Analogously to chromosome cohesion in eukaryotes, newly replicated DNA in E. coli is held together by inter-sister linkages before partitioning into daughter nucleoids. In both cases, initial joining is apparently mediated by DNA catenation, in which replication-induced positive supercoils diffuse behind the fork, causing newly replicated duplexes to twist around each other. Type-II topoisomerase-catalyzed sister separation is delayed by the well-characterized cohesin complex in eukaryotes, but cohesion control in E. coli is not currently understood. We report that the abundant fork tracking protein SeqA is a strong positive regulator of cohesion, and is responsible for markedly prolonged cohesion observed at “snap” loci. Epistasis analysis suggests that SeqA stabilizes cohesion by antagonizing Topo IV-mediated sister resolution, and possibly also by a direct bridging mechanism. We show that variable cohesion observed along the E. coli chromosome is caused by differential SeqA binding, with oriC and snap loci binding disproportionally more SeqA. We propose that SeqA binding results in loose inter-duplex junctions that are resistant to Topo IV cleavage. Lastly, reducing cohesion by genetic manipulation of Topo IV or SeqA resulted in dramatically slowed sister locus separation and poor nucleoid partitioning, indicating that cohesion has a prominent role in chromosome segregation.

Vyšlo v časopise: Regulation of Sister Chromosome Cohesion by the Replication Fork Tracking Protein SeqA. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003673
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003673

Souhrn

Zdroje

1. SunakoY, OnogiT, HiragaS (2001) Sister chromosome cohesion of Escherichia coli. Mol Microbiol 42 : 1233–1241.

2. BatesD, KlecknerN (2005) Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121 : 899–911.

3. NielsenHJ, LiY, YoungrenB, HansenFG, AustinS (2006) Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 61 : 383–393.

4. WangX, Reyes-LamotheR, SherrattDJ (2008) Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev 22 : 2426–2433.

5. EspeliO, MercierR, BoccardF (2008) DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68 : 1418–1427.

6. JoshiMC, BourniquelA, FisherJ, HoBT, MagnanD, KlecknerN, BatesD (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci U S A 108 : 2765–2770.

7. FisherJK, BourniquelA, WitzG, WeinerB, PrentissM, KlecknerN (2013) Four-Dimensional Imaging of E. coli Nucleoid Organization and Dynamics in Living Cells. Cell 153 : 882–895.

8. NasmythK, HaeringCH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43 : 525–558.

9. GordonGS, SitnikovD, WebbCD, TelemanA, StraightA, LosickR, MurrayAW, WrightA (1997) Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90 : 1113–1121.

10. 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.

11. LesterlinC, GigantE, BoccardF, EspeliO (2012) Sister chromatid interactions in bacteria revealed by a site-specific recombination assay. EMBO J 31 : 3468–3479.

12. DeiblerRW, RahmatiS, ZechiedrichEL (2001) Topoisomerase IV, alone, unknots DNA in E. coli. Genes Dev 15 : 748–761.

13. EspeliO, LevineC, HassingH, MariansKJ (2003) Temporal regulation of topoisomerase IV activity in E. coli. Mol Cell 11 : 189–201.

14. KhodurskyAB, PeterBJ, SchmidMB, DeRisiJ, BotsteinD, BrownPO, CozzarelliNR (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci U S A 97 : 9419–9424.

15. PostowL, CrisonaNJ, PeterBJ, HardyCD, CozzarelliNR (2001) Topological challenges to DNA replication: conformations at the fork. Proc Natl Acad Sci U S A 98 : 8219–8226.

16. LopezV, Martinez-RoblesML, HernandezP, KrimerDB, SchvartzmanJB (2012) Topo IV is the topoisomerase that knots and unknots sister duplexes during DNA replication. Nucleic Acids Res 40 : 3563–3573.

17. PetrushenkoZM, SheW, RybenkovVV (2011) A new family of bacterial condensins. Mol Microbiol 81 : 881–896.

18. Johnson RC, Johnson LM, Schmidt JW, Gardner JF (2005) Major nucleoid proteins in the structure and function of the Eschrichia coli chromosome. In: Higgins NP, editor. The Bacterial Chromosome. Washington, D.C.: ASM Press. pp. 65–132.

19. BrendlerT, SawitzkeJ, SergueevK, AustinS (2000) A case for sliding SeqA tracts at anchored replication forks during Escherichia coli chromosome replication and segregation. EMBO J 19 : 6249–6258.

20. LuM, CampbellJL, BoyeE, KlecknerN (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77 : 413–426.

21. CampbellJL, KlecknerN (1990) E. coli oriC and the dnaA gene promoter are sequestered from Dam methyltransferase following the passage of the chromosomal replication fork. Cell 62 : 967–979.

22. OnogiT, NikiH, YamazoeM, HiragaS (1999) The assembly and migration of SeqA-Gfp fusion in living cells of Escherichia coli. Mol Microbiol 31 : 1775–1782.

23. OdsbuI, KlungsoyrHK, FossumS, SkarstadK (2005) Specific N-terminal interactions of the Escherichia coli SeqA protein are required to form multimers that restrain negative supercoils and form foci. Genes Cells 10 : 1039–1049.

24. KangS, HanJS, ParkJH, SkarstadK, HwangDS (2003) SeqA protein stimulates the relaxing and decatenating activities of topoisomerase IV. J Biol Chem 278 : 48779–48785.

25. HayamaR, MariansKJ (2010) Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc Natl Acad Sci U S A 107 : 18826–18831.

26. LiY, StewartNK, BergerAJ, VosS, SchoefflerAJ, BergerJM, ChaitBT, OakleyMG (2010) Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc Natl Acad Sci U S A 107 : 18832–18837.

27. KatoJ, NishimuraY, ImamuraR, NikiH, HiragaS, SuzukiH (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63 : 393–404.

28. ZechiedrichEL, CozzarelliNR (1995) Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. Genes Dev 9 : 2859–2869.

29. BatesD, EpsteinJ, BoyeE, FahrnerK, BergH, KlecknerN (2005) The Escherichia coli baby cell column: a novel cell synchronization method provides new insight into the bacterial cell cycle. Mol Microbiol 57 : 380–391.

30. 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.

31. WaldminghausT, SkarstadK (2010) ChIP on Chip: surprising results are often artifacts. BMC Genomics 11 : 414.

32. Sanchez-RomeroMA, BusbySJ, DyerNP, OttS, MillardAD, GraingerDC (2010) Dynamic Distribution of SeqA Protein across the Chromosome of Escherichia coli K-12. mBio 1: e00012–10.

33. Lobner-OlesenA, MarinusMG, HansenFG (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci U S A 100 : 4672–4677.

34. ElmoreS, MullerM, VischerN, OdijkT, WoldringhCL (2005) Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli. J Struct Biol 151 : 275–287.

35. PeterBJ, UllspergerC, HiasaH, MariansKJ, CozzarelliNR (1998) The structure of supercoiled intermediates in DNA replication. Cell 94 : 819–827.

36. FossumS, CrookeE, SkarstadK (2007) Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26 : 4514–4522.

37. GuarneA, BrendlerT, ZhaoQ, GhirlandoR, AustinS, YangW (2005) Crystal structure of a SeqA-N filament: implications for DNA replication and chromosome organization. EMBO J 24 : 1502–1511.

38. BachT, KreklingMA, SkarstadK (2003) Excess SeqA prolongs sequestration of oriC and delays nucleoid segregation and cell division. EMBO J 22 : 315–323.

39. WaldminghausT, WeigelC, SkarstadK (2012) Replication fork movement and methylation govern SeqA binding to the Escherichia coli chromosome. Nucleic Acids Res 40 : 5465–5476.

40. LiuZ, ZechiedrichL, ChanHS (2010) Action at hooked or twisted-hooked DNA juxtapositions rationalizes unlinking preference of type-2 topoisomerases. J Mol Biol 400 : 963–982.

41. FarcasAM, UluocakP, HelmhartW, NasmythK (2011) Cohesin's concatenation of sister DNAs maintains their intertwining. Mol Cell 44 : 97–107.

42. WeitaoT, NordstromK, DasguptaS (1999) Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. Mol Microbiol 34 : 157–168.

43. KlecknerN, ZicklerD, JonesGH, DekkerJ, PadmoreR, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101 : 12592–12597.

44. SlaterS, WoldS, LuM, BoyeE, SkarstadK, et al. (1995) E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82 : 927–936.

45. FerulloDJ, LovettST (2008) The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet 4: e1000300.

46. NorrisV, FralickJ, DanchinA (2000) A SeqA hyperstructure and its interactions direct the replication and sequestration of DNA. Mol Microbiol 37 : 696–702.

47. KouzminovaEA, RotmanE, MacomberL, ZhangJ, KuzminovA (2004) RecA-dependent mutants in Escherichia coli reveal strategies to avoid chromosomal fragmentation. Proc Natl Acad Sci U S A 101 : 16262–16267.

48. HansenFG, von MeyenburgK (1979) Characterization of the dnaA, gyrB and other genes in the dnaA region of the Escherichia coli chromosome on specialized transducing phages lambda tna. Mol Gen Genet 175 : 135–144.

49. MarinusMG, CarrawayM, FreyAZ, BrownL, ArrajJA (1983) Insertion mutations in the dam gene of Escherichia coli K-12. Mol Gen Genet 192 : 288–289.

50. HuismanO, FaelenM, GirardD, JaffeA, ToussaintA, et al. (1989) Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol 171 : 3704–3712.

51. YamazoeM, OnogiT, SunakoY, NikiH, YamanakaK, et al. (1999) Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 18 : 5873–5884.

52. JohnsonRC, BallCA, PfefferD, SimonMI (1988) Isolation of the gene encoding the Hin recombinational enhancer binding protein. Proc Natl Acad Sci U S A 85 : 3484–3488.

53. Von FreieslebenU, RasmussenKV, AtlungT, HansenFG (2000) Rifampicin-resistant initiation of chromosome replication from oriC in ihf mutants. Mol Microbiol 37 : 1087–1093.

54. LauIF, FilipeSR, SoballeB, OkstadOA, BarreFX, et al. (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol 49 : 731–743.

55. CronanJE (2006) A family of arabinose-inducible Escherichia coli expression vectors having pBR322 copy control. Plasmid 55 : 152–157.