Home LiteratureArticle Details
PMID: 19856119 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Spatial regulation and organization of DNA replication within the nucleus.

Chromosome research : an international journal on the molecular, supramolecular and evolutionary aspects of chromosome biology ·Vol. 18 ·No. 1 ·2010-01-00 ·Pages 7-17

Natsume T, Tanaka TU

Abstract

Duplication of chromosomal DNA is a temporally and spatially regulated process. The timing of DNA replication initiation at various origins is highly coordinated; some origins fire early and others late during S phase. Moreover, inside the nuclei, the bulk of DNA replication is physically organized in replication factories, consisting of DNA polymerases and other replication proteins. In this review article, we discuss how DNA replication is organized and regulated spatially within the nucleus and how this spatial organization is linked to temporal regulation. We focus on DNA replication in budding yeast and fission yeast and, where applicable, compare yeast DNA replication with that in bacteria and metazoans.

MeSH Terms
Cell Nucleus/metabolism DNA Replication DNA, Fungal/biosynthesis
Chemicals
DNA, Fungal
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Natsume Toyoaki
Wellcome Trust Centre for Gene Regulation and Expression, University of Dundee, Dundee, DD1 5EH, UK.
Tanaka Tomoyuki U
References (97)
97 references, click to expand
  1. DNA replication: a complex matter.
    EMBO Rep. 2003 Jul;4(7):666-70 PMID: 12835753
  2. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells.
    J Cell Biol. 1998 Mar 23;140(6):1285-95 PMID: 9508763
  3. A replication fork barrier at the 3' end of yeast ribosomal RNA genes.
    Cell. 1988 Nov 18;55(4):637-43 PMID: 3052854
  4. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast.
    EMBO J. 2007 Mar 7;26(5):1327-39 PMID: 17304213
  5. Monitoring S phase progression globally and locally using BrdU incorporation in TK(+) yeast strains.
    Nucleic Acids Res. 2001 Apr 1;29(7):1433-42 PMID: 11266543
  6. The checkpoint response to replication stress.
    DNA Repair (Amst). 2009 Sep 2;8(9):1038-46 PMID: 19482564
  7. The DNA replication fork in eukaryotic cells.
    Annu Rev Biochem. 1998;67:721-51 PMID: 9759502
  8. Eukaryotic DNA replication: a model for a fixed double replisome.
    Trends Genet. 2000 Feb;16(2):88-92 PMID: 10652536
  9. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription.
    Cell. 2005 Nov 18;123(4):581-92 PMID: 16286007
  10. Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae.
    Genes Dev. 2007 Dec 15;21(24):3319-30 PMID: 18079178
  11. Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast.
    Curr Biol. 2002 Dec 23;12(24):2076-89 PMID: 12498682
  12. Organization of replication of ribosomal DNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 1988 Nov;8(11):4927-35 PMID: 3062373
  13. Replication timing and transcriptional control: beyond cause and effect--part II.
    Curr Opin Genet Dev. 2009 Apr;19(2):142-9 PMID: 19345088
  14. Mcm2, but not RPA, is a component of the mammalian early G1-phase prereplication complex.
    J Cell Biol. 1999 Aug 23;146(4):709-22 PMID: 10459007
  15. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation.
    Cell. 2005 Jun 17;121(6):899-911 PMID: 15960977
  16. Coordination of replication and transcription along a Drosophila chromosome.
    Genes Dev. 2004 Dec 15;18(24):3094-105 PMID: 15601823
  17. Expression of the Herpes simplex virus thymidine kinase gene in Saccharomyces cerevisiae.
    Mol Gen Genet. 1981;184(3):386-93 PMID: 6278252
  18. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins.
    Science. 2001 Dec 14;294(5550):2357-60 PMID: 11743203
  19. Division of labor at the eukaryotic replication fork.
    Mol Cell. 2008 Apr 25;30(2):137-44 PMID: 18439893
  20. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication.
    Cell. 1993 Sep 24;74(6):979-92 PMID: 8402887
  21. Polymerases and the replisome: machines within machines.
    Cell. 1998 Feb 6;92(3):295-305 PMID: 9476890
  22. Visualization of replication factories attached to nucleoskeleton.
    Cell. 1993 Apr 23;73(2):361-73 PMID: 8097433
  23. Preventing re-replication of chromosomal DNA.
    Nat Rev Mol Cell Biol. 2005 Jun;6(6):476-86 PMID: 15928711
  24. An analysis of the regulation of DNA synthesis by cdk2, Cip1, and licensing factor.
    J Cell Biol. 1995 Apr;129(1):1-15 PMID: 7698977
  25. Limiting DNA replication to once and only once.
    EMBO Rep. 2000 Dec;1(6):479-83 PMID: 11263490
  26. ORC-dependent and origin-specific initiation of DNA replication at defined foci in isolated yeast nuclei.
    Genes Dev. 1997 Jun 15;11(12):1504-18 PMID: 9203578
  27. Localization of bacterial DNA polymerase: evidence for a factory model of replication.
    Science. 1998 Nov 20;282(5393):1516-9 PMID: 9822387
  28. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters.
    Cell. 1997 May 2;89(3):365-71 PMID: 9150136
  29. Temporal separation of replication and recombination requires the intra-S checkpoint.
    J Cell Biol. 2005 Feb 14;168(4):537-44 PMID: 15716375
  30. Temporally coordinated assembly and disassembly of replication factories in the absence of DNA synthesis.
    Nat Cell Biol. 2000 Oct;2(10):686-94 PMID: 11025658
  31. A DNA polymerase alpha accessory protein, Mcl1, is required for propagation of centromere structures in fission yeast.
    PLoS One. 2008 May 21;3(5):e2221 PMID: 18493607
  32. High-resolution statistical mapping reveals gene territories in live yeast.
    Nat Methods. 2008 Dec;5(12):1031-7 PMID: 18978785
  33. Replication dynamics of the yeast genome.
    Science. 2001 Oct 5;294(5540):115-21 PMID: 11588253
  34. A position effect on the time of replication origin activation in yeast.
    Cell. 1992 Jan 24;68(2):333-9 PMID: 1733502
  35. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids.
    Cell. 1997 Oct 3;91(1):35-45 PMID: 9335333
  36. Replicon dynamics, dormant origin firing, and terminal fork integrity after double-strand break formation.
    Cell. 2009 Apr 17;137(2):247-58 PMID: 19361851
  37. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication.
    Nat Cell Biol. 2006 Feb;8(2):148-55 PMID: 16429127
  38. Global regulation of genome duplication in eukaryotes: an overview from the epifluorescence microscope.
    Chromosoma. 2008 Jun;117(3):243-60 PMID: 18197411
  39. The structure and function of yeast ARS elements.
    Curr Opin Genet Dev. 1993 Oct;3(5):752-8 PMID: 8274858
  40. Replication foci dynamics: replication patterns are modulated by S-phase checkpoint kinases in fission yeast.
    EMBO J. 2007 Mar 7;26(5):1315-26 PMID: 17304223
  41. Replication fork movement sets chromatin loop size and origin choice in mammalian cells.
    Nature. 2008 Sep 25;455(7212):557-60 PMID: 18716622
  42. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress.
    Genes Dev. 2007 Dec 15;21(24):3331-41 PMID: 18079179
  43. Mapping replicational sites in the eucaryotic cell nucleus.
    J Cell Biol. 1989 Jan;108(1):1-11 PMID: 2910875
  44. DNA replication origins in the Schizosaccharomyces pombe genome.
    Proc Natl Acad Sci U S A. 2005 Jan 11;102(2):337-42 PMID: 15623550
  45. Cell cycle-dependent establishment of a late replication program.
    Science. 1997 May 2;276(5313):806-9 PMID: 9115207
  46. A moving DNA replication factory in Caulobacter crescentus.
    EMBO J. 2001 Sep 3;20(17):4952-63 PMID: 11532959
  47. Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories.
    Cell. 2006 Jun 30;125(7):1297-308 PMID: 16814716
  48. Multiple determinants controlling activation of yeast replication origins late in S phase.
    Genes Dev. 1996 Jul 1;10(13):1595-607 PMID: 8682291
  49. Time of replication of yeast centromeres and telomeres.
    Cell. 1988 Aug 12;54(4):505-13 PMID: 3042152
  50. The dynamics of yeast telomeres and silencing proteins through the cell cycle.
    J Struct Biol. 2000 Apr;129(2-3):159-74 PMID: 10806066
  51. Ku complex controls the replication time of DNA in telomere regions.
    Genes Dev. 2002 Oct 1;16(19):2485-90 PMID: 12368259
  52. The DNA damage response during DNA replication.
    Curr Opin Cell Biol. 2005 Dec;17(6):568-75 PMID: 16226452
  53. Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus.
    J Cell Biochem. 2001;81(1):56-67 PMID: 11180397
  54. Study of the cell cycle-dependent assembly of the DNA pre-replication centres in Xenopus egg extracts.
    EMBO J. 1994 Sep 1;13(17):4153-64 PMID: 8076611
  55. The temporal program of chromosome replication: genomewide replication in clb5{Delta} Saccharomyces cerevisiae.
    Genetics. 2008 Dec;180(4):1833-47 PMID: 18832352
  56. Release of yeast telomeres from the nuclear periphery is triggered by replication and maintained by suppression of Ku-mediated anchoring.
    Genes Dev. 2008 Dec 1;22(23):3363-74 PMID: 19056887
  57. Yeast DNA polymerase epsilon participates in leading-strand DNA replication.
    Science. 2007 Jul 6;317(5834):127-30 PMID: 17615360
  58. Multiple pathways for telomere tethering: functional implications of subnuclear position for heterochromatin formation.
    Biochim Biophys Acta. 2004 Mar 15;1677(1-3):120-8 PMID: 15020053
  59. Organization of human replicon: singles or zipping couples?
    J Struct Biol. 2009 Mar;165(3):204-13 PMID: 19063972
  60. The Ctf18 RFC-like complex positions yeast telomeres but does not specify their replication time.
    EMBO J. 2006 Apr 5;25(7):1505-14 PMID: 16525505
  61. Dynamics of DNA replication factories in living cells.
    J Cell Biol. 2000 Apr 17;149(2):271-80 PMID: 10769021
  62. Replication fork density increases during DNA synthesis in X. laevis egg extracts.
    J Mol Biol. 2000 Jul 28;300(5):1133-42 PMID: 10903859
  63. Histone acetylation regulates the time of replication origin firing.
    Mol Cell. 2002 Nov;10(5):1223-33 PMID: 12453428
  64. Early events in DNA replication require cyclin E and are blocked by p21CIP1.
    J Cell Biol. 1995 Aug;130(4):755-69 PMID: 7642695
  65. Termination of DNA replication of bacterial and plasmid chromosomes.
    Mol Microbiol. 1999 Mar;31(6):1611-8 PMID: 10209736
  66. Replication fork velocities at adjacent replication origins are coordinately modified during DNA replication in human cells.
    Mol Biol Cell. 2007 Aug;18(8):3059-67 PMID: 17522385
  67. Bidirectional chromosome replication: some topological considerations.
    J Theor Biol. 1974 Jan;43(1):187-95 PMID: 4813535
  68. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion.
    Curr Biol. 1996 Dec 1;6(12):1599-608 PMID: 8994824
  69. Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein A.
    J Cell Biol. 1992 Oct;119(1):1-15 PMID: 1527163
  70. Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis.
    Int Rev Cytol. 1980;64:1-80 PMID: 20815116
  71. Control of replication timing by a transcriptional silencer.
    Curr Biol. 2002 Jun 4;12(11):869-75 PMID: 12062049
  72. Genome-wide identification of replication origins in yeast by comparative genomics.
    Genes Dev. 2006 Jul 15;20(14):1874-9 PMID: 16847347
  73. The midcell replication factory in Bacillus subtilis is highly mobile: implications for coordinating chromosome replication with other cell cycle events.
    Mol Microbiol. 2004 Oct;54(2):452-63 PMID: 15469516
  74. Mapping of early firing origins on a replication profile of budding yeast.
    Genes Cells. 2002 Aug;7(8):781-9 PMID: 12167157
  75. Independent positioning and action of Escherichia coli replisomes in live cells.
    Cell. 2008 Apr 4;133(1):90-102 PMID: 18394992
  76. Cellular DNA replicases: components and dynamics at the replication fork.
    Annu Rev Biochem. 2005;74:283-315 PMID: 15952889
  77. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters.
    Mol Cell. 2002 Dec;10(6):1355-65 PMID: 12504011
  78. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus.
    Exp Cell Res. 1986 Aug;165(2):291-7 PMID: 3720850
  79. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci.
    Chromosoma. 2000 Mar;108(8):471-84 PMID: 10794569
  80. Origins of DNA replication in the three domains of life.
    FEBS J. 2005 Aug;272(15):3757-66 PMID: 16045748
  81. Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication.
    J Virol. 1992 Feb;66(2):804-15 PMID: 1309914
  82. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex.
    Cell. 2005 Nov 18;123(4):593-605 PMID: 16286008
  83. DNA replication in eukaryotic cells.
    Annu Rev Biochem. 2002;71:333-74 PMID: 12045100
  84. Where it all starts: eukaryotic origins of DNA replication.
    J Cell Sci. 2001 Feb;114(Pt 4):643-51 PMID: 11171369
  85. 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. 2009 May 1;23(9):1077-90 PMID: 19417103
  86. Chk1 regulates the density of active replication origins during the vertebrate S phase.
    EMBO J. 2007 Jun 6;26(11):2719-31 PMID: 17491592
  87. DNA polymerases alpha, delta, and epsilon localize and function together at replication forks in Saccharomyces cerevisiae.
    Genes Cells. 2005 Apr;10(4):297-309 PMID: 15773893
  88. Dynamic molecular combing: stretching the whole human genome for high-resolution studies.
    Science. 1997 Sep 5;277(5331):1518-23 PMID: 9278517
  89. Movement of replicating DNA through a stationary replisome.
    Mol Cell. 2000 Dec;6(6):1321-30 PMID: 11163206
  90. Telomeric chromatin modulates replication timing near chromosome ends.
    Genes Dev. 1999 Jan 15;13(2):146-51 PMID: 9925638
  91. Stable chromosomal units determine the spatial and temporal organization of DNA replication.
    J Cell Sci. 2004 Oct 15;117(Pt 22):5353-65 PMID: 15466893
  92. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae.
    Mol Cell Biol. 2004 Jun;24(11):4769-80 PMID: 15143171
  93. The positioning and dynamics of origins of replication in the budding yeast nucleus.
    J Cell Biol. 2001 Jan 22;152(2):385-400 PMID: 11266454
  94. Reconstitution of an efficient thymidine salvage pathway in Saccharomyces cerevisiae.
    Nucleic Acids Res. 2003 Oct 1;31(19):e120 PMID: 14500848
  95. Spatial and temporal dynamics of DNA replication sites in mammalian cells.
    J Cell Biol. 1998 Dec 14;143(6):1415-25 PMID: 9852140
  96. The DNA polymerase domain of pol(epsilon) is required for rapid, efficient, and highly accurate chromosomal DNA replication, telomere length maintenance, and normal cell senescence in Saccharomyces cerevisiae.
    J Biol Chem. 2002 Aug 2;277(31):28099-108 PMID: 12015307
  97. Replication timing and transcriptional control: beyond cause and effect.
    Curr Opin Cell Biol. 2002 Jun;14(3):377-83 PMID: 12067662
Article Info
Journal
Chromosome research : an international journal on the molecular, supramolecular and evolutionary aspects of chromosome biology
Abbr.
Chromosome Res
ISSN
1573-6849
DOI
10.1007/s10577-009-9088-0
Published
2010-01-00
Pages
7-17
Language
English
Region
Netherlands
NLM ID
9313452
PMCID
PMC2826631
Subset
IM
Grants
Wellcome Trust · United Kingdom
Cancer Research UK · United Kingdom
External Links
PubMed source DOI: 10.1007/s10577-009-9088-0 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2