Chromosome I Controls Chromosome II Replication in


Control of chromosome replication involves a common set of regulators in eukaryotes, whereas bacteria with divided genomes use chromosome-specific regulators. How bacterial chromosomes might communicate for replication is not known. In Vibrio cholerae, which has two chromosomes (chrI and chrII), replication initiation is controlled by DnaA in chrI and by RctB in chrII. DnaA has binding sites at the chrI origin of replication as well as outside the origin. RctB likewise binds at the chrII origin and, as shown here, to external sites. The binding to the external sites in chrII inhibits chrII replication. A new kind of site was found in chrI that enhances chrII replication. Consistent with its enhancing activity, the chrI site increased RctB binding to those chrII origin sites that stimulate replication and decreased binding to other sites that inhibit replication. The differential effect on binding suggests that the new site remodels RctB. The chaperone-like activity of the site is supported by the finding that it could relieve the dependence of chrII replication on chaperone proteins DnaJ and DnaK. The presence of a site in chrI that specifically controls chrII replication suggests a mechanism for communication between the two chromosomes for replication.


Vyšlo v časopise: Chromosome I Controls Chromosome II Replication in. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004184
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004184

Souhrn

Control of chromosome replication involves a common set of regulators in eukaryotes, whereas bacteria with divided genomes use chromosome-specific regulators. How bacterial chromosomes might communicate for replication is not known. In Vibrio cholerae, which has two chromosomes (chrI and chrII), replication initiation is controlled by DnaA in chrI and by RctB in chrII. DnaA has binding sites at the chrI origin of replication as well as outside the origin. RctB likewise binds at the chrII origin and, as shown here, to external sites. The binding to the external sites in chrII inhibits chrII replication. A new kind of site was found in chrI that enhances chrII replication. Consistent with its enhancing activity, the chrI site increased RctB binding to those chrII origin sites that stimulate replication and decreased binding to other sites that inhibit replication. The differential effect on binding suggests that the new site remodels RctB. The chaperone-like activity of the site is supported by the finding that it could relieve the dependence of chrII replication on chaperone proteins DnaJ and DnaK. The presence of a site in chrI that specifically controls chrII replication suggests a mechanism for communication between the two chromosomes for replication.


Zdroje

1. JhaJK, BaekJH, Venkova-CanovaT, ChattorajDK (2012) Chromosome dynamics in multichromosome bacteria. Biochim Biophys Acta 1819: 826–829.

2. HarrisonPW, LowerRP, KimNK, YoungJP (2010) Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid. Trends Microbiol 18: 141–148.

3. KawakamiH, KatayamaT (2010) DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversity. Biochem Cell Biol 88: 49–62.

4. GiraldoR (2003) Common domains in the initiators of DNA replication in Bacteria, Archaea and Eukarya: combined structural, functional and phylogenetic perspectives. FEMS Microbiol Rev 26: 533–554.

5. EganES, FogelMA, WaldorMK (2005) Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56: 1129–1138.

6. RasmussenT, JensenRB, SkovgaardO (2007) The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J 26: 3124–3131.

7. DuigouS, KnudsenKG, SkovgaardO, EganES, Lφbner-OlesenA, et al. (2006) Independent Control of Replication Initiation of the Two Vibrio cholerae Chromosomes by DnaA and RctB. J Bacteriol 188: 6419–6424.

8. MantieroD, MackenzieA, DonaldsonA, ZegermanP (2011) Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30: 4805–4814.

9. EganES, WaldorMK (2003) Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell 114: 521–530.

10. FogelMA, WaldorMK (2005) Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 55: 125–136.

11. DubarryN, PastaF, LaneD (2006) ParABS systems of the four replicons of Burkholderia cenocepacia: new chromosome centromeres confer partition specificity. J Bacteriol 188: 1489–1496.

12. JacobF (1993) The replicon: thirty years later. Cold Spring Harb Symp Quant Biol 58: 383–387.

13. AtlungT, HansenFG (1993) Three distinct chromosome replication states are induced by increasing concentrations of DnaA protein in Escherichia coli. J Bacteriol 175: 6537–6545.

14. RothA, MesserW (1998) High-affinity binding sites for the initiator protein DnaA on the chromosome of Escherichia coli. Mol Microbiol 28: 395–401.

15. HansenFG, ChristensenBB, AtlungT (1991) The initiator titration model: computer simulation of chromosome and minichromosome control. Res Microbiol 142: 161–167.

16. KitagawaR, OzakiT, MoriyaS, OgawaT (1998) Negative control of replication initiation by a novel chromosomal locus exhibiting exceptional affinity for Escherichia coli DnaA protein. Genes Dev 12: 3032–3043.

17. KashoK, KatayamaT (2013) DnaA binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation. Proc Natl Acad Sci U S A 110: 936–941.

18. KatayamaT, KubotaT, KurokawaK, CrookeE, SekimizuK (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94: 61–71.

19. FujimitsuK, SenriuchiT, KatayamaT (2009) Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev 23: 1221–1233.

20. IshikawaS, OguraY, YoshimuraM, OkumuraH, ChoE, et al. (2007) Distribution of stable DnaA-binding sites on the Bacillus subtilis genome detected using a modified ChIP-chip method. DNA Res 14: 155–168.

21. KatayamaT, OzakiS, KeyamuraK, FujimitsuK (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8: 163–170.

22. CollierJ (2012) Regulation of chromosomal replication in Caulobacter crescentus. Plasmid 67: 76–87.

23. CollierJ, ShapiroL (2009) Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191: 5706–5716.

24. DasN, Valjavec-GratianM, BasurayAN, FeketeRA, PappPP, et al. (2005) Multiple homeostatic mechanisms in the control of P1 plasmid replication. Proc Natl Acad Sci U S A 102: 2856–2861.

25. HeidelbergJF, EisenJA, NelsonWC, ClaytonRA, GwinnML, et al. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477–483.

26. Venkova-CanovaT, ChattorajDK (2011) Transition from a plasmid to a chromosomal mode of replication entails additional regulators. Proc Natl Acad Sci U S A 108: 6199–6204.

27. ValME, SkovgaardO, Ducos-GalandM, BlandMJ, MazelD (2012) Genome Engineering in Vibrio cholerae: A Feasible Approach to Address Biological Issues. PLoS Genet 8: e1002472.

28. KitagawaR, MitsukiH, OkazakiT, OgawaT (1996) A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol Microbiol 19: 1137–1147.

29. DemarreG, ChattorajDK (2010) DNA adenine methylation is required to replicate both Vibrio cholerae chromosomes once per cell cycle. PLoS Genet 6: e1000939.

30. JhaJK, DemarreG, Venkova-CanovaT, ChattorajDK (2012) Replication regulation of Vibrio cholerae chromosome II involves initiator binding to the origin both as monomer and as dimer. Nucleic Acids Res 40: 6026–6038.

31. Venkova-CanovaT, SahaA, ChattorajDK (2012) A 29-mer site regulates transcription of the initiator gene as well as function of the replication origin of Vibrio cholerae chromosome II. Plasmid 67: 102–110.

32. EganES, DuigouS, WaldorMK (2006) Autorepression of RctB, an initiator of Vibrio cholerae chromosome II replication. J Bacteriol 188: 789–793.

33. SrivastavaP, ChattorajDK (2007) Selective chromosome amplification in Vibrio cholerae. Mol Microbiol 66: 1016–1028.

34. DuigouS, YamaichiY, WaldorMK (2008) ATP negatively regulates the initiator protein of Vibrio cholerae chromosome II replication. Proc Natl Acad Sci U S A 105: 10577–10582.

35. BoyeE, Lφbner-OlesenA, SkarstadK (2000) Limiting DNA replication to once and only once. EMBO Rep 1: 479–483.

36. YamaichiY, FogelMA, WaldorMK (2007) par genes and the pathology of chromosome loss in Vibrio cholerae. Proc Natl Acad Sci U S A 104: 630–635.

37. KadoyaR, ChattorajDK (2012) Insensitivity of Chromosome I and the Cell Cycle to Blockage of Replication and Segregation of Vibrio cholerae Chromosome II. MBio 3: 00067–00012.

38. Venkova-CanovaT, BaekJH, FitzgeraldPC, BlokeschM, ChattorajDK (2013) Evidence for Two Different Regulatory Mechanisms Linking Replication and Segregation of Vibrio cholerae Chromosome II. PLoS Genet 9: e1003579.

39. YamaichiY, FogelMA, McLeodSM, HuiMP, WaldorMK (2007) Distinct centromere-like parS sites on the two chromosomes of Vibrio spp. J Bacteriol 189: 5314–5324.

40. ValME, KennedySP, El KarouiM, BonneL, ChevalierF, et al. (2008) FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet 4: e1000201.

41. LeonardAC, HelmstetterCE (1988) Replication patterns of multiple plasmids coexisting in Escherichia coli. J Bacteriol 170: 1380–1383.

42. MeijsingSH, PufallMA, SoAY, BatesDL, ChenL, et al. (2009) DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 324: 407–410.

43. HollenhorstPC, ChandlerKJ, PoulsenRL, JohnsonWE, SpeckNA, et al. (2009) DNA specificity determinants associate with distinct transcription factor functions. PLoS Genet 5: e1000778.

44. Diaz-LopezT, Lages-GonzaloM, Serrano-LopezA, AlfonsoC, RivasG, et al. (2003) Structural changes in RepA, a plasmid replication initiator, upon binding to origin DNA. J Biol Chem 278: 18606–18616.

45. AbhyankarMM, ReddyJM, SharmaR, BullesbachE, BastiaD (2004) Biochemical investigations of control of replication initiation of plasmid R6K. J Biol Chem 279: 6711–6719.

46. PalD, Venkova-CanovaT, SrivastavaP, ChattorajDK (2005) Multipartite regulation of rctB, the replication initiator gene of Vibrio cholerae chromosome II. J Bacteriol 187: 7167–7175.

47. WicknerS, HoskinsJ, McKenneyK (1991) Monomerization of RepA dimers by heat shock proteins activates binding to DNA replication origin. Proc Natl Acad Sci U S A 88: 7903–7907.

48. ManenD, Upegui-GonzalezLC, CaroL (1992) Monomers and dimers of the RepA protein in plasmid pSC101 replication: domains in RepA. Proc Natl Acad Sci U S A 89: 8923–8927.

49. KomoriH, MatsunagaF, HiguchiY, IshiaiM, WadaC, et al. (1999) Crystal structure of a prokaryotic replication initiator protein bound to DNA at 2.6 A resolution. Embo J 18: 4597–4607.

50. KochB, MaX, Lφbner-OlesenA (2012) rctB mutations that increase copy number of Vibrio cholerae oriCII in Escherichia coli. Plasmid 68: 159–169.

51. HuJC, O'SheaEK, KimPS, SauerRT (1990) Sequence requirements for coiled-coils: analysis with lambda repressor-GCN4 leucine zipper fusions. Science 250: 1400–1403.

52. KarimovaG, PidouxJ, UllmannA, LadantD (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95: 5752–5756.

53. FanucchiS, ShibayamaY, BurdS, WeinbergMS, MhlangaMM (2013) Chromosomal Contact Permits Transcription between Coregulated Genes. Cell 155: 606–620.

54. SinghSK, SabatinosS, ForsburgS, BastiaD (2010) Regulation of replication termination by Reb1 protein-mediated action at a distance. Cell 142: 868–878.

55. GennaroML, NovickRP (1986) cmp, a cis-acting plasmid locus that increases interaction between replication origin and initiator protein. J Bacteriol 168: 160–166.

56. ConleyDL, CohenSN (1995) Effects of the pSC101 partition (par) locus on in vivo DNA supercoiling near the plasmid replication origin. Nucleic Acids Res 23: 701–707.

57. Venkova-CanovaT, SrivastavaP, ChattorajDK (2006) Transcriptional inactivation of a regulatory site for replication of Vibrio cholerae chromosome II. Proc Natl Acad Sci U S A 103: 12051–12056.

58. Miller JH (1992) A Short Course In Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.

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