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Regulatory Mechanisms That Prevent Re-initiation of DNA Replication Can Be Locally Modulated at Origins by Nearby Sequence Elements


Eukaryotic organisms have hundreds to thousands of DNA replication origins distributed throughout their genomes. Faithful duplication of these genomes requires a multitude of global controls that ensure that every replication origin initiates at most once per cell cycle. Disruptions in these controls can result in re-initiation of origins and localized re-replication of the surrounding genome. Such re-replicated genomic segments are converted to stable chromosomal alterations with extraordinarily efficiency and could provide a potential source of genomic alterations associated with cancer cells. This publication establishes the existence of a local layer of replication control by identifying new genetic elements, termed re-initiation promoters (RIPs) that can locally override some of the global mechanisms preventing re-initiation. Origins adjacent to RIP elements are not as tightly controlled and thus more susceptible to re-initiation, especially when these global controls are compromised. We speculate that RIP elements contribute to genomic variability in origin control and make some regions of the genome more susceptible to re-replication induced genomic instability.


Vyšlo v časopise: Regulatory Mechanisms That Prevent Re-initiation of DNA Replication Can Be Locally Modulated at Origins by Nearby Sequence Elements. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004358
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004358

Souhrn

Eukaryotic organisms have hundreds to thousands of DNA replication origins distributed throughout their genomes. Faithful duplication of these genomes requires a multitude of global controls that ensure that every replication origin initiates at most once per cell cycle. Disruptions in these controls can result in re-initiation of origins and localized re-replication of the surrounding genome. Such re-replicated genomic segments are converted to stable chromosomal alterations with extraordinarily efficiency and could provide a potential source of genomic alterations associated with cancer cells. This publication establishes the existence of a local layer of replication control by identifying new genetic elements, termed re-initiation promoters (RIPs) that can locally override some of the global mechanisms preventing re-initiation. Origins adjacent to RIP elements are not as tightly controlled and thus more susceptible to re-initiation, especially when these global controls are compromised. We speculate that RIP elements contribute to genomic variability in origin control and make some regions of the genome more susceptible to re-replication induced genomic instability.


Zdroje

1. BlowJJ, LaskeyRA (1988) A Role for the Nuclear Envelope in Controlling DNA Replication within the Cell Cycle. Nature 332: 546–548.

2. GreenBM, FinnKJ, LiJJ (2010) Loss of DNA Replication Control Is a Potent Inducer of Gene Amplification. Science 329: 943–946.

3. DiffleyJFX (2011) Quality Control in the Initiation of Eukaryotic DNA Replication. Philos Trans R Soc Lond B Biol Sci 366: 3545–3553.

4. RemusD, BeuronF, TolunG, GriffithJD, MorrisEP, et al. (2009) Concerted Loading of Mcm2-7 Double Hexamers around DNA During DNA Replication Origin Licensing. Cell 139: 719–730.

5. AriasEE, WalterJC (2007) Strength in Numbers: Preventing Rereplication Via Multiple Mechanisms in Eukaryotic Cells. Genes Dev 21: 497–518.

6. RemusD, DiffleyJFX (2009) Eukaryotic DNA Replication Control: Lock and Load, Then Fire. Curr Opin Cell Biol 21: 771–777.

7. NguyenVQ, CoC, LiJJ (2001) Cyclin-Dependent Kinases Prevent DNA Re-Replication through Multiple Mechanisms. Nature 411: 1068–1073.

8. DruryLS, DiffleyJFX (2009) Factors Affecting the Diversity of DNA Replication Licensing Control in Eukaryotes. Curr Biol 19: 530–535.

9. McGarryTJ (2002) Geminin Deficiency Causes a Chk1-Dependent G2 Arrest in Xenopus. Mol Biol Cell 13: 3662–3671.

10. TatsumiY, SugimotoN, YugawaT, Narisawa-SaitoM, KiyonoT, et al. (2006) Deregulation of Cdt1 Induces Chromosomal Damage without Rereplication and Leads to Chromosomal Instability. J Cell Sci 119: 3128–3140.

11. ZhuW, ChenY, DuttaA (2004) Rereplication by Depletion of Geminin Is Seen Regardless of P53 Status and Activates a G2/M Checkpoint. Mol Cell Biol 24: 7140–7150.

12. GreenBM, MorrealeRJ, OzaydinB, DerisiJL, LiJJ (2006) Genome-Wide Mapping of DNA Synthesis in Saccharomyces Cerevisiae Reveals That Mechanisms Preventing Reinitiation of DNA Replication Are Not Redundant. Mol Biol Cell 17: 2401–2414.

13. TannyRE, MacAlpineDM, BlitzblauHG, BellSP (2006) Genome-Wide Analysis of Re-Replication Reveals Inhibitory Controls That Target Multiple Stages of Replication Initiation. Mol Biol Cell 17: 2415–2423.

14. AparicioOM (2013) Location, Location, Location: It's All in the Timing for Replication Origins. Genes Dev 27: 117–128.

15. LabibK, DiffleyJF, KearseySE (1999) G1-Phase and B-Type Cyclins Exclude the DNA-Replication Factor Mcm4 from the Nucleus. Nat Cell Biol 1: 415–422.

16. NguyenVQ, CoC, IrieK, LiJJ (2000) Clb/Cdc28 Kinases Promote Nuclear Export of the Replication Initiator Proteins Mcm2-7. Curr Biol 10: 195–205.

17. TanakaS, DiffleyJFX (2002) Interdependent Nuclear Accumulation of Budding Yeast Cdt1 and Mcm2-7 During G1 Phase. Nat Cell Biol 4: 198–207.

18. PiattiS, LengauerC, NasmythK (1995) Cdc6 Is an Unstable Protein Whose De Novo Synthesis in G1 Is Important for the Onset of S Phase and for Preventing a ‘Reductional’ Anaphase in the Budding Yeast Saccharomyces Cerevisiae. EMBO J 14: 3788–3799.

19. DruryLS, PerkinsG, DiffleyJF (2000) The Cyclin-Dependent Kinase Cdc28p Regulates Distinct Modes of Cdc6p Proteolysis During the Budding Yeast Cell Cycle. Curr Biol 10: 231–240.

20. PerkinsG, DruryLS, DiffleyJF (2001) Separate Scf(Cdc4) Recognition Elements Target Cdc6 for Proteolysis in S Phase and Mitosis. EMBO J 20: 4836–4845.

21. MimuraS, SekiT, TanakaS, DiffleyJFX (2004) Phosphorylation-Dependent Binding of Mitotic Cyclins to Cdc6 Contributes to DNA Replication Control. Nature 431: 1118–1123.

22. WilmesGM, ArchambaultV, AustinRJ, JacobsonMD, BellSP, et al. (2004) Interaction of the S-Phase Cyclin Clb5 with an “Rxl” Docking Sequence in the Initiator Protein Orc6 Provides an Origin-Localized Replication Control Switch. Genes Dev 18: 981–991.

23. RhindN, GilbertDM (2013) DNA Replication Timing. Cold Spring Harb Perspect Biol 5: a010132.

24. PoloumienkoA, DershowitzA, DeJ, NewlonCS (2001) Completion of Replication Map of Saccharomyces Cerevisiae Chromosome III. Mol Biol Cell 12: 3317–3327.

25. NieduszynskiCA, KnoxY, DonaldsonAD (2006) Genome-Wide Identification of Replication Origins in Yeast by Comparative Genomics. Genes Dev 20: 1874–1879.

26. GrunsteinM, GasserSM (2013) Epigenetics in Saccharomyces Cerevisiae. Cold Spring Harb Perspect Biol 5: a017491.

27. AbrahamJ, NasmythKA, StrathernJN, KlarAJ, HicksJB (1984) Regulation of Mating-Type Information in Yeast. Negative Control Requiring Sequences Both 5′ and 3′ to the Regulated Region. J Mol Biol 176: 307–331.

28. BrandAH, MicklemG, NasmythK (1987) A Yeast Silencer Contains Sequences That Can Promote Autonomous Plasmid Replication and Transcriptional Activation. Cell 51: 709–719.

29. DingQ, MacalpineDM (2011) Defining the Replication Program through the Chromatin Landscape. Crit Rev Biochem Mol Biol 46: 165–179.

30. KnottSRV, PeaceJM, OstrowAZ, GanY, RexAE, et al. (2012) Forkhead Transcription Factors Establish Origin Timing and Long-Range Clustering in S. Cerevisiae. Cell 148: 99–111.

31. OstrowAZ, NellimoottilT, KnottSRV, FoxCA, TavaréS, et al. (2014) Fkh1 and Fkh2 Bind Multiple Chromosomal Elements in the S. Cerevisiae Genome with Distinct Specificities and Cell Cycle Dynamics. PLoS ONE 9: e87647.

32. ZhuC, ByersK, MccordR, ShiZ, BergerM, et al. (2009) High-Resolution DNA Binding Specificity Analysis of Yeast Transcription Factors. Genome Res 19(4): 556–66.

33. Palacios DebeerMA, MüllerU, FoxCA (2003) Differential DNA Affinity Specifies Roles for the Origin Recognition Complex in Budding Yeast Heterochromatin. Genes Dev 17: 1817–1822.

34. BellSP, DuttaA (2002) DNA Replication in Eukaryotic Cells. Annu Rev Biochem 71: 333–374.

35. EatonML, GalaniK, KangS, BellSP, MacAlpineDM (2010) Conserved Nucleosome Positioning Defines Replication Origins. Genes Dev 24: 748–753.

36. 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.

37. SwederK, RhodeP, CampbellJ (1988) Purification and Characterization of Proteins That Bind to Yeast Arss. J Biol Chem 263: 17270–17277.

38. PalzkillTG, OliverSG, NewlonCS (1986) DNA Sequence Analysis of Ars Elements from Chromosome Iii of Saccharomyces Cerevisiae: Identification of a New Conserved Sequence. Nucleic Acids Res 14: 6247–6264.

39. StinchcombDT, StruhlK, DavisRW (1979) Isolation and Characterisation of a Yeast Chromosomal Replicator. Nature 282: 39–43.

40. Chisamore-RobertP, PeetersS, ShostakK, YankulovK (2012) Directional Telomeric Silencing and Lack of Canonical B1 Elements in Two Silencer Autonomously Replicating Sequences in S. Cerevisiae. BMC Mol Biol 13: 34.

41. LeeDG, BellSP (1997) Architecture of the Yeast Origin Recognition Complex Bound to Origins of DNA Replication. Mol Cell Biol 17: 7159–7168.

42. SegalE, WidomJ (2009) What Controls Nucleosome Positions? Trends Genet 25: 335–343.

43. HuangRY, KowalskiD (1993) A DNA Unwinding Element and an Ars Consensus Comprise a Replication Origin within a Yeast Chromosome. EMBO J 12: 4521–4531.

44. XiL, Fondufe-MittendorfY, XiaL, FlatowJ, WidomJ, et al. (2010) Predicting Nucleosome Positioning Using a Duration Hidden Markov Model. BMC Bioinformatics 11: 346.

45. HuangY, KowalskiD (2003) Web-Thermodyn: Sequence Analysis Software for Profiling DNA Helical Stability. Nucleic Acids Res 31: 3819–3821.

46. FoxCA, LooS, DillinA, RineJ (1995) The Origin Recognition Complex Has Essential Functions in Transcriptional Silencing and Chromosomal Replication. Genes Dev 9: 911–924.

47. RivierDH, RineJ (1992) An Origin of DNA Replication and a Transcription Silencer Require a Common Element. Science 256: 659–663.

48. BellSP, KaguniJM (2013) Helicase Loading at Chromosomal Origins of Replication. Cold Spring Harb Perspect Biol 5: a010124.

49. MuramatsuS, HiraiK, TakY-S, KamimuraY, ArakiH (2010) Cdk-Dependent Complex Formation between Replication Proteins Dpb11, Sld2, Pol (Epsilon}, and GINS in Budding Yeast. Genes Dev 24: 602–612.

50. TanakaS, UmemoriT, HiraiK, MuramatsuS, KamimuraY, et al. (2007) Cdk-Dependent Phosphorylation of Sld2 and Sld3 Initiates DNA Replication in Budding Yeast. Nature 445: 328–332.

51. ZegermanP, DiffleyJFX (2007) Phosphorylation of Sld2 and Sld3 by Cyclin-Dependent Kinases Promotes DNA Replication in Budding Yeast. Nature 445: 281–285.

52. AparicioOM, WeinsteinDM, BellSP (1997) Components and Dynamics of DNA Replication Complexes in S. Cerevisiae: Redistribution of Mcm Proteins and Cdc45p During S Phase. Cell 91: 59–69.

53. TilloD, HughesTR (2009) G+C Content Dominates Intrinsic Nucleosome Occupancy. BMC Bioinformatics 10: 442.

54. ThurtleDM, RineJ (2014) The Molecular Topography of Silenced Chromatin in Saccharomyces Cerevisiae. Genes Dev 28: 245–258.

55. ZouY, YuQ, BiX (2006) Asymmetric Positioning of Nucleosomes and Directional Establishment of Transcriptionally Silent Chromatin by Saccharomyces Cerevisiae Silencers. Mol Cell Biol 26: 7806–7819.

56. MacisaacKD, WangT, GordonDB, GiffordDK, StormoGD, et al. (2006) An Improved Map of Conserved Regulatory Sites for Saccharomyces Cerevisiae. BMC Bioinformatics 7: 113.

57. NewburgerDE, BulykML (2009) Uniprobe: An Online Database of Protein Binding Microarray Data on Protein-DNA Interactions. Nucleic Acids Res 37: D77–82.

58. ChenS, BellSP (2011) Cdk Prevents Mcm2-7 Helicase Loading by Inhibiting Cdt1 Interaction with Orc6. Genes Dev 25: 363–372.

59. WilmesGM, BellSP (2002) The B2 Element of the Saccharomyces Cerevisiae Ars1 Origin of Replication Requires Specific Sequences to Facilitate Pre-Rc Formation. Proc Natl Acad Sci U S A 99: 101–106.

60. NordmanJ, Orr-WeaverTL (2012) Regulation of DNA Replication During Development. Development 139: 455–464.

61. ArentsonE, FaloonP, SeoJ, MoonE, StudtsJM, et al. (2002) Oncogenic Potential of the DNA Replication Licensing Protein Cdt1. Oncogene 21: 1150–1158.

62. LiontosM, KoutsamiM, SideridouM, EvangelouK, KletsasD, et al. (2007) Deregulated Overexpression of Hcdt1 and Hcdc6 Promotes Malignant Behavior. Cancer Res 67: 10899–10909.

63. SeoJ, ChungYS, SharmaGG, MoonE, BurackWR, et al. (2005) Cdt1 Transgenic Mice Develop Lymphoblastic Lymphoma in the Absence of P53. Oncogene 24: 8176–8186.

64. HerrickJ, ContiC, TeissierS, ThierryF, CouturierJ, et al. (2005) Genomic Organization of Amplified Myc Genes Suggests Distinct Mechanisms of Amplification in Tumorigenesis. Cancer Res 65: 1174–1179.

65. KuwaharaY, TanabeC, IkeuchiT, AoyagiK, NishigakiM, et al. (2004) Alternative Mechanisms of Gene Amplification in Human Cancers. Genes Chromosomes Cancer 41: 125–132.

66. O'NeilJ, TchindaJ, GutierrezA, MoreauL, MaserRS, et al. (2007) Alu Elements Mediate Myb Gene Tandem Duplication in Human T-All. J Exp Med 204: 3059–3066.

67. StroutMP, MarcucciG, BloomfieldCD, CaligiuriMA (1998) The Partial Tandem Duplication of All1 (Mll) Is Consistently Generated by Alu-Mediated Homologous Recombination in Acute Myeloid Leukemia. Proc Natl Acad Sci U S A 95: 2390–2395.

68. SantariusT, ShipleyJ, BrewerD, StrattonMR, CooperCS (2010) A Census of Amplified and Overexpressed Human Cancer Genes. Nature Rev Cancer 10: 59–64.

69. GajduskovaP, SnijdersAM, KwekS, RoydasguptaR, FridlyandJ, et al. (2007) Genome Position and Gene Amplification. Genome Biol 8: R120.

70. Ohno S (1970) Evolution by Gene Duplication. Berlin, New York: Springer-Verlag. xv, 160 p.

71. McConnellMJ, LindbergMR, BrennandKJ, PiperJC, VoetT, et al. (2013) Mosaic Copy Number Variation in Human Neurons. Science 342: 632–637.

72. GoldsteinAL, McCuskerJH (1999) Three New Dominant Drug Resistance Cassettes for Gene Disruption in Saccharomyces Cerevisiae. Yeast 15: 1541–1553.

73. KoshlandD, KentJC, HartwellLH (1985) Genetic Analysis of the Mitotic Transmission of Minichromosomes. Cell 40: 393–403.

74. DetweilerCS, LiJJ (1998) Ectopic Induction of Clb2 in Early G1 Phase Is Sufficient to Block Prereplicative Complex Formation in Saccharomyces Cerevisiae. Proc Natl Acad Sci U S A 95: 2384–2389.

75. ChristiansonTW, SikorskiRS, DanteM, SheroJH, HieterP (1992) Multifunctional Yeast High-Copy-Number Shuttle Vectors. Gene 110: 119–122.

76. GiaeverG, ChuAM, NiL, ConnellyC, RilesL, et al. (2002) Functional Profiling of the Saccharomyces Cerevisiae Genome. Nature 418: 387–391.

77. ShermanF., Getting started with yeast. Methods Enzymol, 2002. 350: p. 3–41.

78. HaaseSB, LewDJ (1997) Flow Cytometric Analysis of DNA Content in Budding Yeast. Methods Enzymol 283: 322–332.

79. HoffmanCS, WinstonF (1987) A Ten-Minute DNA Preparation from Yeast Efficiently Releases Autonomous Plasmids for Transformation of Escherichia Coli. Gene 57: 267–272.

80. PleissJA, WhitworthGB, BergkesselM, GuthrieC (2007) Transcript Specificity in Yeast Pre-Mrna Splicing Revealed by Mutations in Core Spliceosomal Components. PLoS Biol 5: e90.

81. RaghuramanMK, BrewerBJ, FangmanWL (1997) Cell Cycle-Dependent Establishment of a Late Replication Program. Science 276: 806–809.

82. MacalpineDM, BellSP (2005) A Genomic View of Eukaryotic DNA Replication. Chromosome Res 13: 309–326.

83. LeeTI, JohnstoneSE, YoungRA (2006) Chromatin Immunoprecipitation and Microarray-Based Analysis of Protein Location. Nature Prot 1: 729–748.

84. Aparicio O, Geisberg JV, Sekinger E, Yang A, Moqtaderi Z, et al.. (2005) Chromatin Immunoprecipitation for Determining the Association of Proteins with Specific Genomic Sequences in Vivo. Curr Prot Mol Biol Unit 21.23.

85. LivakKJ, SchmittgenTD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative Pcr and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.

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