#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Link between ORC-Origin Binding Mechanisms and Origin Activation Time Revealed in Budding Yeast


Eukaryotic DNA replication origins are selected in G1-phase when the origin recognition complex (ORC) binds chromosomal positions and triggers molecular events culminating in the initiation of DNA replication (a.k.a. origin firing) during S-phase. Each chromosome uses multiple origins for its duplication, and each origin fires at a characteristic time during S-phase, creating a cell-type specific genome replication pattern relevant to differentiation and genome stability. It is unclear whether ORC-origin interactions are relevant to origin activation time. We applied a novel genome-wide strategy to classify origins in the model eukaryote Saccharomyces cerevisiae based on the types of molecular interactions used for ORC-origin binding. Specifically, origins were classified as DNA-dependent when the strength of ORC-origin binding in vivo could be explained by the affinity of ORC for origin DNA in vitro, and, conversely, as ‘chromatin-dependent’ when the ORC-DNA interaction in vitro was insufficient to explain the strength of ORC-origin binding in vivo. These two origin classes differed in terms of nucleosome architecture and dependence on origin-flanking sequences in plasmid replication assays, consistent with local features of chromatin promoting ORC binding at ‘chromatin-dependent’ origins. Finally, the ‘chromatin-dependent’ class was enriched for origins that fire early in S-phase, while the DNA-dependent class was enriched for later firing origins. Conversely, the latest firing origins showed a positive association with the ORC-origin DNA paradigm for normal levels of ORC binding, whereas the earliest firing origins did not. These data reveal a novel association between ORC-origin binding mechanisms and the regulation of origin activation time.


Vyšlo v časopise: A Link between ORC-Origin Binding Mechanisms and Origin Activation Time Revealed in Budding Yeast. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003798
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003798

Souhrn

Eukaryotic DNA replication origins are selected in G1-phase when the origin recognition complex (ORC) binds chromosomal positions and triggers molecular events culminating in the initiation of DNA replication (a.k.a. origin firing) during S-phase. Each chromosome uses multiple origins for its duplication, and each origin fires at a characteristic time during S-phase, creating a cell-type specific genome replication pattern relevant to differentiation and genome stability. It is unclear whether ORC-origin interactions are relevant to origin activation time. We applied a novel genome-wide strategy to classify origins in the model eukaryote Saccharomyces cerevisiae based on the types of molecular interactions used for ORC-origin binding. Specifically, origins were classified as DNA-dependent when the strength of ORC-origin binding in vivo could be explained by the affinity of ORC for origin DNA in vitro, and, conversely, as ‘chromatin-dependent’ when the ORC-DNA interaction in vitro was insufficient to explain the strength of ORC-origin binding in vivo. These two origin classes differed in terms of nucleosome architecture and dependence on origin-flanking sequences in plasmid replication assays, consistent with local features of chromatin promoting ORC binding at ‘chromatin-dependent’ origins. Finally, the ‘chromatin-dependent’ class was enriched for origins that fire early in S-phase, while the DNA-dependent class was enriched for later firing origins. Conversely, the latest firing origins showed a positive association with the ORC-origin DNA paradigm for normal levels of ORC binding, whereas the earliest firing origins did not. These data reveal a novel association between ORC-origin binding mechanisms and the regulation of origin activation time.


Zdroje

1. StillmanB (2005) Origin recognition and the chromosome cycle. FEBS Lett 579: 877–884.

2. BellSP, DuttaA (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333–374.

3. SclafaniRA, HolzenTM (2007) Cell cycle regulation of DNA replication. Annu Rev Genet 41: 237–280.

4. RemusD, DiffleyJF (2009) Eukaryotic DNA replication control: lock and load, then fire. Curr Opin Cell Biol 21: 771–777.

5. BoosD, FrigolaJ, DiffleyJF (2012) Activation of the replicative DNA helicase: breaking up is hard to do. Curr Opin Cell Biol 24: 423–430.

6. TakaraTJ, BellSP (2009) Putting two heads together to unwind DNA. Cell 139: 652–654.

7. LabibK (2011) Building a double hexamer of DNA helicase at eukaryotic replication origins. EMBO J 30: 4853–4855.

8. DiffleyJF (2011) Quality control in the initiation of eukaryotic DNA replication. Philos Trans R Soc Lond B Biol Sci 366: 3545–3553.

9. van BrabantAJ, BuchananCD, CharboneauE, FangmanWL, BrewerBJ (2001) An origin-deficient yeast artificial chromosome triggers a cell cycle checkpoint. Mol Cell 7: 705–713.

10. TheisJF, IreneC, DershowitzA, BrostRL, TobinML, et al. (2010) The DNA damage response pathway contributes to the stability of chromosome III derivatives lacking efficient replicators. PLoS Genet 6: e1001227.

11. KawabataT, LuebbenSW, YamaguchiS, IlvesI, MatiseI, et al. (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol Cell 41: 543–553.

12. IbarraA, SchwobE, MendezJ (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 105: 8956–8961.

13. GeXQ, JacksonDA, BlowJJ (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 21: 3331–3341.

14. RybaT, HirataniI, SasakiT, BattagliaD, KulikM, et al. (2011) Replication timing: a fingerprint for cell identity and pluripotency. PLoS Comput Biol 7: e1002225.

15. DebatisseM, Le TallecB, LetessierA, DutrillauxB, BrisonO (2012) Common fragile sites: mechanisms of instability revisited. Trends Genet 28: 22–32.

16. WatanabeY, MaekawaM (2010) Spatiotemporal regulation of DNA replication in the human genome and its association with genomic instability and disease. Curr Med Chem 17: 222–233.

17. SmithL, PlugA, ThayerM (2001) Delayed replication timing leads to delayed mitotic chromosome condensation and chromosomal instability of chromosome translocations. Proc Natl Acad Sci U S A 98: 13300–13305.

18. TiengweC, MarcelloL, FarrH, DickensN, KellyS, et al. (2012) Genome-wide analysis reveals extensive functional interaction between DNA replication initiation and transcription in the genome of Trypanosoma brucei. Cell Rep 2: 185–197.

19. MullerCA, NieduszynskiCA (2012) Conservation of replication timing reveals global and local regulation of replication origin activity. Genome Res 22: 1953–1962.

20. Di RienziSC, LindstromKC, MannT, NobleWS, RaghuramanMK, et al. (2012) Maintaining replication origins in the face of genomic change. Genome Res 22: 1940–1952.

21. KorenA, TsaiHJ, TiroshI, BurrackLS, BarkaiN, et al. (2010) Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6: e1001068.

22. KnottSR, PeaceJM, OstrowAZ, GanY, RexAE, et al. (2012) Forkhead transcription factors establish origin timing and long-range clustering in S. cerevisiae. Cell 148: 99–111.

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

24. TanakaS, NakatoR, KatouY, ShirahigeK, ArakiH (2011) Origin association of Sld3, Sld7, and Cdc45 proteins is a key step for determination of origin-firing timing. Curr Biol 21: 2055–2063.

25. PohlTJ, BrewerBJ, RaghuramanMK (2012) Functional centromeres determine the activation time of pericentric origins of DNA replication in Saccharomyces cerevisiae. PLoS Genet 8: e1002677.

26. LookeM, KristjuhanK, VarvS, KristjuhanA (2013) Chromatin-dependent and -independent regulation of DNA replication origin activation in budding yeast. EMBO Rep 14: 191–198.

27. NatsumeT, MullerCA, KatouY, RetkuteR, GierlinskiM, et al. (2013) Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. Mol Cell 50: 661–674.

28. KnottSR, ViggianiCJ, TavareS, AparicioOM (2009) Genome-wide replication profiles indicate an expansive role for Rpd3L in regulating replication initiation timing or efficiency, and reveal genomic loci of Rpd3 function in Saccharomyces cerevisiae. Genes Dev 23: 1077–1090.

29. DonaldsonAD, RaghuramanMK, FriedmanKL, CrossFR, BrewerBJ, et al. (1998) CLB5-dependent activation of late replication origins in S. cerevisiae. Mol Cell 2: 173–182.

30. McCuneHJ, DanielsonLS, AlvinoGM, CollingwoodD, DelrowJJ, et al. (2008) The temporal program of chromosome replication: genomewide replication in clb5{Delta} Saccharomyces cerevisiae. Genetics 180: 1833–1847.

31. FriedmanKL, DillerJD, FergusonBM, NylandSV, BrewerBJ, et al. (1996) Multiple determinants controlling activation of yeast replication origins late in S phase. Genes Dev 10: 1595–1607.

32. FergusonBM, FangmanWL (1992) A position effect on the time of replication origin activation in yeast. Cell 68: 333–339.

33. StevensonJB, GottschlingDE (1999) Telomeric chromatin modulates replication timing near chromosome ends. Genes Dev 13: 146–151.

34. LiuJ, McConnellK, DixonM, CalviBR (2012) Analysis of model replication origins in Drosophila reveals new aspects of the chromatin landscape and its relationship to origin activity and the prereplicative complex. Mol Biol Cell 23: 200–212.

35. VogelauerM, RubbiL, LucasI, BrewerBJ, GrunsteinM (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10: 1223–1233.

36. AggarwalBD, CalviBR (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature 430: 372–376.

37. DouglasME, DiffleyJF (2012) Replication timing: the early bird catches the worm. Curr Biol 22: R81–82.

38. NieduszynskiCA, KnoxY, DonaldsonAD (2006) Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev 20: 1874–1879.

39. ChastainPD2nd, BowersJL, LeeDG, BellSP, GriffithJD (2004) Mapping subunit location on the Saccharomyces cerevisiae origin recognition complex free and bound to DNA using a novel nanoscale biopointer. J Biol Chem 279: 36354–36362.

40. WuPY, NurseP (2009) Establishing the program of origin firing during S phase in fission Yeast. Cell 136: 852–864.

41. Palacios DeBeerMA, MullerU, FoxCA (2003) Differential DNA affinity specifies roles for the origin recognition complex in budding yeast heterochromatin. Genes Dev 17: 1817–1822.

42. FoxCA, McConnellKH (2005) Toward biochemical understanding of a transcriptionally silenced chromosomal domain in Saccharomyces cerevisiae. J Biol Chem 280: 8629–8632.

43. MullerP, ParkS, ShorE, HuebertDJ, WarrenCL, et al. (2010) The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev 24: 1418–1433.

44. EatonML, GalaniK, KangS, BellSP, MacAlpineDM (2010) Conserved nucleosome positioning defines replication origins. Genes Dev 24: 748–753.

45. BerbenetzNM, NislowC, BrownGW (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet 6.

46. NoguchiK, VassilevA, GhoshS, YatesJL, DePamphilisML (2006) The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo. Embo J 25: 5372–5382.

47. KuoAJ, SongJ, CheungP, Ishibe-MurakamiS, YamazoeS, et al. (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature

48. ChangF, TheisJF, MillerJ, NieduszynskiCA, NewlonCS, et al. (2008) Analysis of chromosome III replicators reveals an unusual structure for the ARS318 silencer origin and a conserved WTW sequence within the origin recognition complex binding site. Mol Cell Biol 28: 5071–5081.

49. TheisJF, NewlonCS (1997) The ARS309 chromosomal replicator of Saccharomyces cerevisiae depends on an exceptional ARS consensus sequence. Proc Natl Acad Sci U S A 94: 10786–10791.

50. ChangF, MayCD, HoggardT, MillerJ, FoxCA, et al. (2011) High-resolution analysis of four efficient yeast replication origins reveals new insights into the ORC and putative MCM binding elements. Nucleic Acids Res 39: 6523–6535.

51. ShorE, WarrenCL, TietjenJ, HouZ, MullerU, et al. (2009) The origin recognition complex interacts with a subset of metabolic genes tightly linked to origins of replication. PLoS Genet 5: e1000755.

52. ShimadaK, PaseroP, GasserSM (2002) ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev 16: 3236–3252.

53. SiowCC, NieduszynskaSR, MullerCA, NieduszynskiCA (2012) OriDB, the DNA replication origin database updated and extended. Nucleic Acids Res 40: D682–686.

54. NieduszynskiCA, BlowJJ, DonaldsonAD (2005) The requirement of yeast replication origins for pre-replication complex proteins is modulated by transcription. Nucleic Acids Res 33: 2410–2420.

55. DonatoJJ, ChungSC, TyeBK (2006) Genome-wide hierarchy of replication origin usage in Saccharomyces cerevisiae. PLoS Genet 2: e141.

56. IrlbacherH, FrankeJ, MankeT, VingronM, Ehrenhofer-MurrayAE (2005) Control of replication initiation and heterochromatin formation in Saccharomyces cerevisiae by a regulator of meiotic gene expression. Genes Dev 19: 1811–1822.

57. WeberJM, IrlbacherH, Ehrenhofer-MurrayAE (2008) Control of replication initiation by the Sum1/Rfm1/Hst1 histone deacetylase. BMC Mol Biol 9: 100.

58. LynchPJ, FraserHB, SevastopoulosE, RineJ, RuscheLN (2005) Sum1p, the origin recognition complex, and the spreading of a promoter-specific repressor in Saccharomyces cerevisiae. Mol Cell Biol 25: 5920–5932.

59. LeeW, TilloD, BrayN, MorseRH, DavisRW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244.

60. OnishiM, LiouGG, BuchbergerJR, WalzT, MoazedD (2007) Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol Cell 28: 1015–1028.

61. ArmacheKJ, GarlickJD, CanzioD, NarlikarGJ, KingstonRE Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334: 977–982.

62. KaplanN, MooreIK, Fondufe-MittendorfY, GossettAJ, TilloD, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362–366.

63. GibsonDG, BellSP, AparicioOM (2006) Cell cycle execution point analysis of ORC function and characterization of the checkpoint response to ORC inactivation in Saccharomyces cerevisiae. Genes Cells 11: 557–573.

64. YabukiN, TerashimaH, KitadaK (2002) Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 7: 781–789.

65. SantocanaleC, DiffleyJF (1998) A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395: 615–618.

66. FengW, CollingwoodD, BoeckME, FoxLA, AlvinoGM, et al. (2006) Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat Cell Biol 8: 148–155.

67. CrabbeL, ThomasA, PantescoV, De VosJ, PaseroP, et al. (2010) Analysis of replication profiles reveals key role of RFC-Ctf18 in yeast replication stress response. Nat Struct Mol Biol 17: 1391–1397.

68. RaghuramanMK, WinzelerEA, CollingwoodD, HuntS, WodickaL, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115–121.

69. BellSP, KobayashiR, StillmanB (1993) Yeast origin recognition complex functions in transcription silencing and DNA replication. Science 262: 1844–1849.

70. Heidinger-PauliJM, MertO, DavenportC, GuacciV, KoshlandD Systematic reduction of cohesin differentially affects chromosome segregation, condensation, and DNA repair. Curr Biol 20: 957–963.

71. MechaliM (2001) DNA replication origins: from sequence specificity to epigenetics. Nat Rev Genet 2: 640–645.

72. MechaliM (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728–738.

73. AladjemMI (2007) Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8: 588–600.

74. KlemmRD, AustinRJ, BellSP (1997) Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88: 493–502.

75. RandellJC, BowersJL, RodriguezHK, BellSP (2006) Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol Cell 21: 29–39.

76. SpeckC, ChenZ, LiH, StillmanB (2005) ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat Struct Mol Biol 12: 965–971.

77. LiangC, WeinreichM, StillmanB (1995) ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 81: 667–676.

78. BowersJL, RandellJC, ChenS, BellSP (2004) ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol Cell 16: 967–978.

79. RaghuramanMK, BrewerBJ, FangmanWL (1997) Cell cycle-dependent establishment of a late replication program. Science 276: 806–809.

80. TsakraklidesV, BellSP (2010) Dynamics of pre-replicative complex assembly. J Biol Chem 285: 9437–9443.

81. MendezJ, Zou-YangXH, KimSY, HidakaM, TanseyWP, et al. (2002) Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol Cell 9: 481–491.

82. RhindN, YangSC, BechhoeferJ (2010) Reconciling stochastic origin firing with defined replication timing. Chromosome Res 18: 35–43.

83. YangSC, RhindN, BechhoeferJ (2010) Modeling genome-wide replication kinetics reveals a mechanism for regulation of replication timing. Mol Syst Biol 6: 404.

84. LangGI, MurrayAW (2011) Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biol Evol 3: 799–811.

85. StamatoyannopoulosJA, AdzhubeiI, ThurmanRE, KryukovGV, MirkinSM, et al. (2009) Human mutation rate associated with DNA replication timing. Nat Genet 41: 393–395.

86. ChenCL, RappaillesA, DuquenneL, HuvetM, GuilbaudG, et al. (2010) Impact of replication timing on non-CpG and CpG substitution rates in mammalian genomes. Genome Res 20: 447–457.

87. BuckMJ, NobelAB, LiebJD (2005) ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6: R97.

88. HomannOR, JohnsonAD (2010) MochiView: versatile software for genome browsing and DNA motif analysis. BMC Biol 8: 49.

89. MarahrensY, StillmanB (1994) Replicator dominance in a eukaryotic chromosome. Embo J 13: 3395–3400.

90. ZhuC, ByersKJ, McCordRP, ShiZ, BergerMF, et al. (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19: 556–566.

91. ShirahigeK, IwasakiT, RashidMB, OgasawaraN, YoshikawaH (1993) Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae. Mol Cell Biol 13: 5043–5056.

92. XuW, AparicioJG, AparicioOM, TavareS (2006) Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae. BMC Genomics 7: 276.

93. CelnikerSE, SwederK, SriencF, BaileyJE, CampbellJL (1984) Deletion mutations affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae. Mol Cell Biol 4: 2455–2466.

94. BreierAM, ChatterjiS, CozzarelliNR (2004) Prediction of Saccharomyces cerevisiae replication origins. Genome Biol 5: R22.

95. HuangRY, KowalskiD (1993) A DNA unwinding element and an ARS consensus comprise a replication origin within a yeast chromosome. EMBO J 12: 4521–4531.

96. HuangRY, KowalskiD (1996) Multiple DNA elements in ARS305 determine replication origin activity in a yeast chromosome. Nucleic Acids Res 24: 816–823.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#