The chromatin backdrop of DNA replication: Lessons from genetics and genome-scale analyses

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 7, 2012, Pages 794-801

  Conner, Amy L ^a   Aladjem, Mirit I ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cell cycle; Chromatin; DNA replication; Transcription

Indexed keywords

BETA GLOBIN; DNA; ENHANCED GREEN FLUORESCENT PROTEIN; MYC PROTEIN; PROTEIN MYB; RNA POLYMERASE II; SATELLITE DNA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

BINDING SITE; CELL CYCLE; CHROMATIN; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; DNA REPLICATION; DNA SEQUENCE; DROSOPHILA; GENE CLUSTER; GENE INTERACTION; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MODEL; HISTONE MODIFICATION; HUMAN; INSULATOR ELEMENT; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHIZOSACCHAROMYCES POMBE;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES, HUMAN; DNA REPLICATION; GENE SILENCING; GENOME, HUMAN; HUMANS; INSULATOR ELEMENTS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 84861889894     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.01.017     Document Type: Review

References (108)

1. Hiratani I., Takebayashi S., Lu J., Gilbert D.M. Replication timing and transcriptional control: beyond cause and effect - part II. Curr. Opin. Genet. Dev. 2009, 19:142-149.
2. Ryba T., Hiratani I., Sasaki T., Battaglia D., Kulik M., Zhang J., Dalton S., Gilbert D.M. Replication timing: a fingerprint for cell identity and pluripotency. PLoS Comput. Biol. 2010, 7:e1002225.
3. Blow J.J., Dutta A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 2005, 6:476-486.
4. Remus D., Diffley J.F. Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol. 2009, 21:771-777.
5. Gilbert D.M. Making sense of eukaryotic DNA replication origins. Science 2001, 294:96-100.
6. Mechali M. DNA replication origins: from sequence specificity to epigenetics. Nat. Rev. Genet. 2001, 2:640-645.
7. Dimitrova D.S., Gilbert D.M. DNA replication and nuclear organization: prospects for a soluble in vitro system. Crit. Rev. Eukaryot. Gene Expr. 1999, 9:353-361.
8. Mendez J., Stillman B. Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays 2003, 25:1158-1167.
9. Gilbert D.M. Evaluating genome-scale approaches to eukaryotic DNA replication. Nat. Rev. Genet. 2010, 11:673-684.
10. Mendez J. Temporal regulation of DNA replication in mammalian cells. Crit. Rev. Biochem. Mol. Biol. 2009, 44:343-351.
11. DePamphilis M.L. Origins of DNA replication in metazoan chromosomes. J. Biol. Chem. 1993, 268:1-4.
12. Machida Y.J., Hamlin J.L., Dutta A. Right place, right time, and only once: replication initiation in metazoans. Cell 2005, 123:13-24.
13. Jacob F., Brenner S. On the regulation of DNA synthesis in bacteria: the hypothesis of the replicon. C. R. Hebd. Seances Acad. Sci. 1963, 256:298-300.
14. Aladjem M.I. Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat. Rev. Genet. 2007, 8:588-600.
15. Mechali M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 2010, 11:728-738.
16. DePamphilis M.L., Blow J.J., Ghosh S., Saha T., Noguchi K., Vassilev A. Regulating the licensing of DNA replication origins in metazoa. Curr. Opin. Cell Biol. 2006, 18:231-239.
17. DePamphilis M.L. The 'ORC cycle': a novel pathway for regulating eukaryotic DNA replication. Gene 2003, 310:1-15.
18. Gilbert D.M., Takebayashi S.I., Ryba T., Lu J., Pope B.D., Wilson K.A., Hiratani I. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:143-153.
19. Masai H., Matsumoto S., You Z., Yoshizawa-Sugata N., Oda M. Eukaryotic chromosome DNA replication: where, when, and how?. Annu. Rev. Biochem. 2010, 79:89-130.
20. Nieduszynski C.A., Knox Y., Donaldson A.D. Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev. 2006, 20:1874-1879.
21. Muller P., Park S., Shor E., Huebert D.J., Warren C.L., Ansari A.Z., Weinreich M., Eaton M.L., MacAlpine D.M., Fox C.A. The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev. 2010, 24:1418-1433.
22. Casey L., Patterson E.E., Muller U., Fox C.A. Conversion of a replication origin to a silencer through a pathway shared by a Forkhead transcription factor and an S phase cyclin. Mol. Biol. Cell 2008, 19:608-622.
23. Fox C.A., Weinreich M. Beyond heterochromatin: SIR2 inhibits the initiation of DNA replication. Cell Cycle 2008, 7:3330-3334.
24. Crampton A., Chang F., Pappas D.L., Frisch R.L., Weinreich M. An ARS element inhibits DNA replication through a SIR2-dependent mechanism. Mol. Cell 2008, 30:156-166.
25. Vashee S., Cvetic C., Lu W., Simancek P., Kelly T.J., Walter J.C. Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 2003, 17:1894-1908.
26. Remus D., Beall E.L., Botchan M.R. DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J. 2004, 23:897-907.
27. Stefanovic D., Stanojcic S., Vindigni A., Ochem A., Falaschi A. In vitro protein-DNA interactions at the human lamin B2 replication origin. J. Biol. Chem. 2003, 278:42737-42743.
28. Austin R.J., Orr-Weaver T.L., Bell S.P. Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev. 1999, 13:2639-2649.
29. Kong D., Coleman T.R., DePamphilis M.L. Xenopus origin recognition complex (ORC) initiates DNA replication preferentially at sequences targeted by Schizosaccharomyces pombe ORC. EMBO J. 2003, 22:3441-3450.
30. Stanojcic S., Lemaitre J.M., Brodolin K., Danis E., Mechali M. In Xenopus egg extracts, DNA replication initiates preferentially at or near asymmetric AT sequences. Mol. Cell. Biol. 2008, 28:5265-5274.
31. MacAlpine D.M., Rodriguez H.K., Bell S.P. Coordination of replication and transcription along a Drosophila chromosome. Genes Dev. 2004, 18:3094-3105.
32. Kaplan N., Moore I., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., Hughes T.R., Lieb J.D., Widom J., Segal E. Nucleosome sequence preferences influence in vivo nucleosome organization. Nat. Struct. Mol. Biol. 2010, 17:918-920. author reply 920-912.
33. Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., LeProust E.M., Hughes T.R., Lieb J.D., Widom J., Segal E. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366.
34. Cayrou C., Coulombe P., Vigneron A., Stanojcic S., Ganier O., Peiffer I., Rivals E., Puy A., Laurent-Chabalier S., Desprat R., Mechali M. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 2011, 21:1438-1449.
35. Lubelsky Y., Sasaki T., Kuipers M.A., Lucas I., Le Beau M.M., Carignon S., Debatisse M., Prinz J.A., Dennis J.H., Gilbert D.M. Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res. 2011, 39:3141-3155.
36. Lipford J.R., Bell S.P. Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol. Cell 2001, 7:21-30.
37. de Castro E., Soriano I., Marin L., Serrano R., Quintales L., Antequera F. Nucleosomal organization of replication origins and meiotic recombination hotspots in fission yeast. EMBO J. 2012, 31:124-137.
38. Pak D.T., Pflumm M., Chesnokov I., Huang D.W., Kellum R., Marr J., Romanowski P., Botchan M.R. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 1997, 91:311-323.
39. Prasanth S.G., Shen Z., Prasanth K.V., Stillman B. Human origin recognition complex is essential for HP1 binding to chromatin and heterochromatin organization. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15093-15098.
40. Hayashi M.T., Takahashi T.S., Nakagawa T., Nakayama J., Masukata H. The heterochromatin protein Swi6/HP1 activates replication origins at the pericentromeric region and silent mating-type locus. Nat. Cell Biol. 2009, 11:357-362.
41. Schwaiger M., Kohler H., Oakeley E.J., Stadler M.B., Schubeler D. Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. Genome Res. 2010, 20:771-780.
42. Quivy J.P., Gerard A., Cook A.J., Roche D., Almouzni G. The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat. Struct. Mol. Biol. 2008, 15:972-979.
43. Chadha G.S., Blow J.J. Histone acetylation by HBO1 tightens replication licensing. Mol. Cell 2010, 37:5-6.
44. Iizuka M., Matsui T., Takisawa H., Smith M.M. Regulation of replication licensing by acetyltransferase Hbo1. Mol. Cell. Biol. 2006, 26:1098-1108.
45. Unnikrishnan A., Gafken P.R., Tsukiyama T. Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol. 2010, 17:430-437.
46. Iizuka M., Sarmento O.F., Sekiya T., Scrable H., Allis C.D., Smith M.M. Hbo1 links p53-dependent stress signaling to DNA replication licensing. Mol. Cell. Biol. 2008, 28:140-153.
47. DePamphilis M.L. Transcriptional elements as components of eukaryotic origins of DNA replication. Cell 1988, 52:635-638.
48. Kong D., DePamphilis M.L. Site-specific ORC binding, pre-replication complex assembly and DNA synthesis at Schizosaccharomyces pombe replication origins. EMBO J. 2002, 21:5567-5576.
49. Beall E.L., Manak J.R., Zhou S., Bell M., Lipsick J.S., Botchan M.R. Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 2002, 420:833-837.
50. Bosco G., Du W., Orr-Weaver T.L. DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol. 2001, 3:289-295.
51. Aggarwal B.D., Calvi B.R. Chromatin regulates origin activity in Drosophila follicle cells. Nature 2004, 430:372-376.
52. Ghosh M., Liu G., Randall G., Bevington J., Leffak M. Transcription factor binding and induced transcription alter chromosomal c-myc replicator activity. Mol. Cell. Biol. 2004, 24:10193-10207.
53. Danis E., Brodolin K., Menut S., Maiorano D., Girard-Reydet C., Mechali M. Specification of a DNA replication origin by a transcription complex. Nat. Cell Biol. 2004, 6:721-730.
54. Tabancay A.P., Forsburg S.L. Eukaryotic DNA replication in a chromatin context. Curr. Top. Dev. Biol. 2006, 76:129-184.
55. Hiratani I., Ryba T., Itoh M., Yokochi T., Schwaiger M., Chang C.W., Lyou Y., Townes T.M., Schubeler D., Gilbert D.M. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008, 6:e245.
56. Anglana M., Apiou F., Bensimon A., Debatisse M. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 2003, 114:385-394.
57. Cadoret J.C., Meisch F., Hassan-Zadeh V., Luyten I., Guillet C., Duret L., Quesneville H., Prioleau M.N. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15837-15842.
58. Karnani N., Taylor C.M., Malhotra A., Dutta A. Genomic study of replication initiation in human chromosomes reveals the influence of transcription regulation and chromatin structure on origin selection. Mol. Biol. Cell 2009, 393-404.
59. Gomez M., Brockdorff N. Heterochromatin on the inactive X chromosome delays replication timing without affecting origin usage. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6923-6928.
60. Antequera F. Genomic specification and epigenetic regulation of eukaryotic DNA replication origins. EMBO J. 2004, 23:4365-4370.
61. Martin M.M., Ryan M., Kim R., Zakas A.L., Fu H., Lin C.M., Reinhold W.C., Davis S.R., Bilke S., Liu H., Doroshow J.H., Reimers M.A., Valenzuela M.S., Pommier Y., Meltzer P.S., Aladjem M.I. Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res. 2011, 21:1822-1832.
62. Mesner L.D., Valsakumar V., Karnani N., Dutta A., Hamlin J.L., Bekiranov S. Bubble-chip analysis of human origin distributions demonstrates on a genomic scale significant clustering into zones and significant association with transcription. Genome Res. 2011, 21:377-389.
63. Feng Y.Q., Warin R., Li T., Olivier E., Besse A., Lobell A., Fu H., Lin C.M., Aladjem M.I., Bouhassira E.E. The human beta-globin locus control region can silence as well as activate gene expression. Mol. Cell. Biol. 2005, 25:3864-3874.
64. Hansen R.S., Thomas S., Sandstrom R., Canfield T.K., Thurman R.E., Weaver M., Dorschner M.O., Gartler S.M., Stamatoyannopoulos J.A. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. U. S. A. 2009, 107:139-144.
65. Shankavaram U.T., Varma S., Kane D., Sunshine M., Chary K.K., Reinhold W.C., Pommier Y., Weinstein J.N. CellMiner: a relational database and query tool for the NCI-60 cancer cell lines. BMC Genomics 2009, 10:277.
66. Saha S., Shan Y., Mesner L.D., Hamlin J.L. The promoter of the Chinese hamster ovary dihydrofolate reductase gene regulates the activity of the local origin and helps define its boundaries. Genes Dev. 2004, 18:397-410.
67. Hamlin J.L., Mesner L.D., Lar O., Torres R., Chodaparambil S.V., Wang L. A revisionist replicon model for higher eukaryotic genomes. J. Cell. Biochem. 2008, 105:321-329.
68. Simon I., Tenzen T., Mostoslavsky R., Fibach E., Lande L., Milot E., Gribnau J., Grosveld F., Fraser P., Cedar H. Developmental regulation of DNA replication timing at the human beta globin locus. EMBO J. 2001, 20:6150-6157.
69. Dhar V., Skoultchi A.I., Schildkraut C.L. Activation and repression of a beta-globin gene in cell hybrids is accompanied by a shift in its temporal replication. Mol. Cell. Biol. 1989, 9:3524-3532.
70. Mostoslavsky R., Singh N., Tenzen T., Goldmit M., Gabay C., Elizur S., Qi P., Reubinoff B.E., Chess A., Cedar H., Bergman Y. Asynchronous replication and allelic exclusion in the immune system. Nature 2001, 414:221-225.
71. Ermakova O.V., Nguyen L.H., Little R.D., Chevillard C., Riblet R., Ashouian N., Birshtein B.K., Schildkraut C.L. Evidence that a single replication fork proceeds from early to late replicating domains in the IgH locus in a non-B cell line. Mol. Cell 1999, 3:321-330.
72. Cayrou C., Coulombe P., Mechali M. Programming DNA replication origins and chromosome organization. Chromosome Res. 2010, 18:137-145.
73. Aran D., Toperoff G., Rosenberg M., Hellman A. Replication timing-related and gene body-specific methylation of active human genes. Hum. Mol. Genet. 2011, 20:670-680.
74. Suzuki M., Oda M., Ramos M.P., Pascual M., Lau K., Stasiek E., Agyiri F., Thompson R.F., Glass J.L., Jing Q., Sandstrom R., Fazzari M.J., Hansen R.S., Stamatoyannopoulos J.A., McLellan A.S., Greally J.M. Late-replicating heterochromatin is characterized by decreased cytosine methylation in the human genome. Genome Res. 2011, 21:1833-1840.
75. Hansen R.S., Thomas S., Sandstrom R., Canfield T.K., Thurman R.E., Weaver M., Dorschner M.O., Gartler S.M., Stamatoyannopoulos J.A. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:139-144.
76. Vogelauer M., Rubbi L., Lucas I., Brewer B.J., Grunstein M. Histone acetylation regulates the time of replication origin firing. Mol. Cell 2002, 10:1223-1233.
77. Ryba T., Hiratani I., Sasaki T., Battaglia D., Kulik M., Zhang J., Dalton S., Gilbert D.M. Replication timing: a fingerprint for cell identity and pluripotency. PLoS Comput. Biol. 2011, 7:e1002225.
78. Miotto B., Struhl K. HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol. Cell 2010, 37:57-66.
79. Arias E.E., Walter J.C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 2007, 21:497-518.
80. Fu H., Wang L., Lin C.M., Singhania S., Bouhassira E.E., Aladjem M.I. Preventing gene silencing with human replicators. Nat. Biotechnol. 2006, 24:572-576.
81. Huang L., Fu H., Lin C.M., Conner A., Zhang Y., Aladjem M.I. Prevention of transcriptional silencing by a replicator-binding complex consisting of SWI/SNF, MeCP1 and hnRNP C1/C2. Mol. Cell. Biol. 2011, 31:3472-3484.
82. Lu L., Zhang H., Tower J. Functionally distinct, sequence-specific replicator and origin elements are required for Drosophila chorion gene amplification. Genes Dev. 2001, 15:134-146.
83. Chowdhury A., Liu G., Kemp M., Chen X., Katrangi N., Myers S., Ghosh M., Yao J., Gao Y., Bubulya P., Leffak M. The DNA unwinding element binding protein DUE-B interacts with Cdc45 in preinitiation complex formation. Mol. Cell. Biol. 2010, 30:1495-1507.
84. Kalejta R.F., Li X., Mesner L.D., Dijkwel P.A., Lin H.B., Hamlin J.L. Distal sequences, but not ori-beta/OBR-1, are essential for initiation of DNA replication in the Chinese hamster DHFR origin. Mol. Cell 1998, 2:797-806.
85. Aladjem M.I., Groudine M., Brody L.L., Dieken E.S., Fournier R.E., Wahl G.M., Epner E.M. Participation of the human beta-globin locus control region in initiation of DNA replication. Science 1995, 270:815-819.
86. Hayashida T., Oda M., Ohsawa K., Yamaguchi A., Hosozawa T., Locksley R.M., Giacca M., Masai H., Miyatake S. Replication initiation from a novel origin identified in the Th2 cytokine cluster locus requires a distant conserved noncoding sequence. J. Immunol. 2006, 176:5446-5454.
87. Aladjem M., Rodewald L.-W., Kolman J.L., Wahl G.M. Genetic dissection of a mammalian replicator in the human beta-globin locus. Science 1998, 281:1005-1009.
88. Raab J.R., Kamakaka R.T. Insulators and promoters: closer than we think. Nat. Rev. Genet. 2010, 11:439-446.
89. Gaszner M., Felsenfeld G. Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 2006, 7:703-713.
90. Emery D.W. The use of chromatin insulators to improve the expression and safety of integrating gene transfer vectors. Hum. Gene Ther. 2011, 22:761-774.
91. Kamakaka R.T. Chromatin: a connection between loops and barriers?. Curr. Biol. 2002, 12:R535-R537.
92. Emery D.W., Yannaki E., Tubb J., Stamatoyannopoulos G. A chromatin insulator protects retrovirus vectors from chromosomal position effects. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9150-9155.
93. Lin C.M., Fu H., Martinovsky M., Bouhassira E., Aladjem M.I. Dynamic alterations of replication timing in mammalian cells. Curr. Biol. 2003, 13:1019-1028.
94. Wang L., Lin C.M., Lopreiato J.O., Aladjem M.I. Cooperative sequence modules determine replication initiation sites at the human beta-globin locus. Hum. Mol. Genet. 2006, 15:2613-2622.
95. Karmakar S., Mahajan M.C., Schulz V., Boyapaty G., Weissman S.M. A multiprotein complex necessary for both transcription and DNA replication at the beta-globin locus. EMBO J. 2010, 29:3260-3271.
96. Mishiro T., Ishihara K., Hino S., Tsutsumi S., Aburatani H., Shirahige K., Kinoshita Y., Nakao M. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 2009, 28:1234-1245.
97. Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 1994, 371:215-220.
98. Kim J.H., Ebersole T., Kouprina N., Noskov V.N., Ohzeki J., Masumoto H., Mravinac B., Sullivan B.A., Pavlicek A., Dovat S., Pack S.D., Kwon Y.W., Flanagan P.T., Loukinov D., Lobanenkov V., Larionov V. Human gamma-satellite DNA maintains open chromatin structure and protects a transgene from epigenetic silencing. Genome Res. 2009, 19:533-544.
99. Antoniou M., Harland L., Mustoe T., Williams S., Holdstock J., Yague E., Mulcahy T., Griffiths M., Edwards S., Ioannou P.A., Mountain A., Crombie R. Transgenes encompassing dual-promoter CpG islands from the human TBP and HNRPA2B1 loci are resistant to heterochromatin-mediated silencing. Genomics 2003, 82:269-279.
100. Williams S., Mustoe T., Mulcahy T., Griffiths M., Simpson D., Antoniou M., Irvine A., Mountain A., Crombie R. CpG-island fragments from the HNRPA2B1/CBX3 genomic locus reduce silencing and enhance transgene expression from the hCMV promoter/enhancer in mammalian cells. BMC Biotechnol. 2005, 5:17.
101. Emery D.W., Yannaki E., Tubb J., Nishino T., Li Q., Stamatoyannopoulos G. Development of virus vectors for gene therapy of beta chain hemoglobinopathies: flanking with a chromatin insulator reduces gamma-globin gene silencing in vivo. Blood 2002, 100:2012-2019.
102. Ellis J., Yao S. Retrovirus silencing and vector design: relevance to normal and cancer stem cells?. Curr. Gene Ther. 2005, 5:367-373.
103. Mitchell R.S., Beitzel B.F., Schroder A.R., Shinn P., Chen H., Berry C.C., Ecker J.R., Bushman F.D. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2004, 2:E234.
104. Wu X., Li Y., Crise B., Burgess S.M. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003, 300:1749-1751.
105. Diffley J.F. Regulation of early events in chromosome replication. Curr. Biol. 2004, 14:R778-R786.
106. Labib K. How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells?. Genes Dev. 2010, 24:1208-1219.
107. Bell S.P., Dutta A. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 2002, 71:333-374.
108. Mahajan M.C., Narlikar G.J., Boyapaty G., Kingston R.E., Weissman S.M. Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the beta-globin locus control region. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15012-15017.