Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem

BioEssays

Volumn 25, Issue 2, 2003, Pages 116-125

  Hyrien, Olivier ^a   Marheineke, Kathrin ^a   Goldar, Arach ^b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CEA SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MINICHROMOSOME MAINTENANCE PROTEIN;

CELL CYCLE S PHASE; CHROMATIN; CHROMOSOME REPLICATION; DNA REPLICATION; EUKARYOSIS; FLY; FROG; GENOME; NONHUMAN; REVIEW; SEQUENCE HOMOLOGY;

ANIMALS; CHROMATIN; DNA REPLICATION; EUKARYOTIC CELLS; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; REPLICATION ORIGIN; REPLICON;

ANURA; EUKARYOTA;

EID: 0037319618     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.10208     Document Type: Review

References (84)

1. Bell SP, Dutta A. DNA replication in eukaryotic cells. Annu Rev Biochem 2002;71:333-374.
2. Canman CE. Replication checkpoint: preventing mitotic catastrophe. Curr Biol 2001;11:R121-R124.
3. Hyrien O, Méchali M. Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos. EMBO J 1993;12:4511-4520.
4. Shinomiya T, Ina S. Analysis of chromosomal replicons in early embryos of Drosophila melanogaster by two-dimensional gel electrophoresis. Nucleic Acids Res 1991;19:3935-3941.
5. Kimelman D, Kirschner M, Scherson T. The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 1987;48:399-407.
6. Raff JW, Glover DM. Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J Cell Biol 1988;107:2009-2019.
7. Ishimi Y. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J Biol Chem 1997;272:24508-24513.
8. Schwacha A, Bell SP. Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. Mol Cell 2001;8:1093-1104
9. Labib K, Diffley JF. Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Curr Opin Genet Dev 2001;11:64-70.
10. Bell SP, Stillman B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 1992;357:128-134.
11. Diffley JF, Cocker JH. Protein-DNA interactions at a yeast replication origin. Nature 1992;357:169-172.
12. Bell SP. The origin recognition complex: from simple origins to complex functions. Genes Dev 2002;16:659-672.
13. Coleman TR, Carpenter PB, Dunphy WG. The Xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell 1996;87:53-63.
14. Maiorano D, Moreau J, Mechali M. XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature 2000;404:622-625.
15. Nishitani H, Lygorou Z, Nishimoto T, Nurse P. The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 2000;404:625-628.
16. Hua XH, Newport J. Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J Cell Biol 1998;140:271-281.
17. Rowles A, Tada S, Blow JJ. Changes in association of the Xenopus origin recognition complex with chromatin on licensing of replication origins. J Cell Sci 1999;112:2011-2018.
18. Mimura S, Takisawa H. Xenopus Cdc45-dependent loading of DNA polymerase alpha onto chromatin under the control of S-phase Cdk. EMBO J 1998;17:5699-5707.
19. Walter J, Newport J. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol Cell 2000;5:617-627.
20. Aparicio OM, Weinstein DM, Bell SP. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 1997;91:59-69.
21. Tanaka T, Knapp D, Nasmyth K. Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 1997;90:649-660.
22. Santocanale C, Sharma K, Diffley JF. Activation of dormant origins of DNA replication in budding yeast. Genes Dev 1999;13:2360-2364
23. Tadokoro R, Fujita M, Miura H, Shirahige K, Yoshikawa H, Tsurimoto T, Obuse C. Scheduled conversion of replication complex architecture at replication origins of Saccharomyces cerevisiae during the cell cycle. J Biol Chem 2002;277:15881-15889.
24. Madine MA, Khoo CY, Mills AD, Laskey RA. MCM3 complex required for cell cycle regulation of DNA replication in vertebrate cells. Nature 1995;375:421-424.
25. Chong JP, Mahbubani HM, Khoo CY, Blow JJ. Purification of an MCM-containing complex as a component of the DNA replication licensing system. Nature 1995;375:418-421.
26. 1-phase prereplication complex. J Cell Biol 1999;146:709-722.
27. Todorov IT, Attaran A, Kearsey SE. BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. J Cell Biol 1995;129:1433-1445.
28. Krude T, Musahl C, Laskey RA, Knippers R. Human replication proteins hCdc21, hCdc46 and P1Mcm3 bind chromatin uniformly before S-phase and are displaced locally during DNA replication. J Cell Sci 1996;109:309-318
29. Romanowski P, Madine MA, Laskey RA. XMCM7, a novel member of the Xenopus MCM family, interacts with XMCM3 and colocalizes with it throughout replication. Proc Natl Acad Sci USA 1996;93:10189-10194
30. Nguyen VQ, Co C, Li JJ. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 2001;411:1068-1073.
31. McGarry TJ, Kirschner MW. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998;93:1043-1053.
32. Tada S, Li A, Maiorano D, Mechali M, Blow JJ. Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat Cell Biol 2001;3:107-113.
33. Ritzi M, Baack M, Musahl C, Romanowski P, Laskey RA, Knippers R. Human minichromosome maintenance proteins and human origin recognition complex 2 protein on chromatin. J Biol Chem 1998;273:24543-24549.
34. Gilbert DM. Making sense of eukaryotic DNA replication origins. Science 2001;294:96-100.
35. Newlon CS, Theis JF. The structure and function of yeast ARS elements. Curr Opin Genet Dev 1993;3:752-758.
36. 1-phase and are required to establish, but not maintain, the S-phase checkpoint. Mol Biol Cell 2001;12:3658-3667.
37. Bielinsky AK, Gerbi SA. Chromosomal ARS1 has a single leading strand start site. Mol Cell 1999;3:477-486.
38. Krysan PJ, Haase SB, Calos MP. Isolation of human sequences that replicate autonomously in human cells. Mol Cell Biol 1989;9:1026-1033.
39. Krysan PJ, Calos MP. Replication initiates at multiple locations on an autonomously replicating plasmid in human cells. Mol Cell Biol 1991;11:1464-1472.
40. Abdurashidova G, Deganuto M, Klima R, Riva S, Biamonti G, Giacca M, Falaschi A. Start sites of bidirectional DNA synthesis at the human lamin B2 origin. Science 2000;287:2023-2026.
41. Aladjem MI, Rodewald LW, Kolman JL, Wahl GM. Genetic dissection of a mammalian replicator in the human beta-globin locus. Science 1998;281:1005-1009
42. Dijkwel PA, Wang S, Hamlin JL. Initiation sites are distributed at frequent intervals in the chinese hamster dihydrofolate reductase origin of replication but are used with very different efficiencies. Mol Cell Biol 2002;22:3053-3065.
43. Dijkwel PA, Mesner LD, Levenson VV, d'Anna J, Hamlin JL. Dispersive initiation of replication in the Chinese hamster rhodopsin locus. Exp Cell Res 2000;256:150-157.
44. Little RD, Platt TH, Schirdkraut CL. Initiation and termination of DNA replication in human rRNA genes. Mol Cell Biol 1993;13:6600-6613.
45. Hyrien O, Maric C, Méchali M. Transition in specification of embryonic metazoan DNA replication origins. Science 1995;270:994-997.
46. Sasaki T, Sawado T, Yamaguchi M, Shinomiya T. Specification of regions of DNA replication initiation during embryogenesis in the 65-kilobase DNApolalpha-dE2F locus of Drosophila melanogaster. Mol Cell Biol 1999;19:547-555.
47. Maric C, Levacher B, Hyrien O. Developmental regulation of replication fork pausing in Xenopus laevis is ribosomal RNA genes. J Mol Biol 1999; 291:775-788.
48. 1 step required to specify the Chinese hamster DHFR replication origin. Science 1996;271:1270-1272.
49. Dimitrova DS, Prokhorova TA, Blow JJ, Todorov IT, Gilbert DM. Mammalian nuclei become licensed for DNA replication during late telophase. J Cell Sci 2002;115:51-59.
50. Gilbert DM. Replication timing and transcriptional control: beyond cause and effect. Curr Op Cell Biol 2002;14:377-383
51. Raghuraman MK, Brewer BJ, Fangman WL. Cell cycle-dependent establishment of a late replication program. Science 1997;276:806-809.
52. 1 phase. Mol Cell 1999;4:983-993
53. 1 phase. J Cell Biol 2001;154:283-292.
54. Heun P, Laroche T, Raghuraman MK, Gasser SM. The positioning and dynamics of origins of replication in the budding yeast nucleus. J Cell Biol 2001;152:385-400.
55. Blumenthal AB, Kriegstein HJ, Hogness DS. The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol 1974;38:205-223.
56. Blow JJ, Watson JV. Nuclei act as independent and integrated units of replication in a Xenopus cell-free DNA replication system. EMBO J 1987;6:1997-2002.
57. Walter J, Newport JW. Regulation of replicon size in Xenopus egg extracts. Science 1997;275:993-995.
58. Lucas I, Chevrier-Miller M, Sogo JM, Hyrien O. Mechanisms ensuring rapid and complete DNA replication despite random initiation in Xenopus early embryos. J Mol Biol 2000;296:769-786.
59. Herrick J, Stanislawski P, Hyrien O, Bensimon A. Replication fork density increases during DNA synthesis in X. laevis egg extracts. J Mol Biol 2000;300:1133-1142.
60. Blow JJ, Gillespie PJ, Francis D, Jackson DA. Replication origins in Xenopus egg extract are 5-15 kilobases apart and are activated in clusters that fire at different times. J Cell Biol 2001;152:15-26.
61. Marheineke K, Hyrien O. Aphidicolin triggers a block to replication origin firing in Xenopus egg extracts. J Biol Chem 2001;276:17092-17100
62. Mills AD, Blow JJ, White JG, Amos WB, Wilcock D, Laskey RA. Replication occurs at discrete foci spaced throughout nuclei replicating in vitro. J Cell Sci 1989;94:471-477.
63. O'Keefe RT, Henderson SC, Spector DL. Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J Cell Biol 1992;116:1095-1110.
64. Wolffe AP. Replication timing and Xenopus 5S RNA gene transcription in vitro. Dev Biol 1993;157:224-231.
65. Mahbubani HM, Paull T, Elder JK, Blow JJ. DNA replication initiates at multiple sites on plasmid DNA in Xenopus egg extracts. Nucleic Acids Res 1992;20:1457-1462.
66. Laskey RA. Chromosome replication in early development of Xenopus laevis. J Embryol Exp Morphol 1985;89 Suppl:285-296.
67. Rowles A, Chong JP, Brown L, Howell M, Evan GL, Blow JJ. Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell 1996;87:287-296.
68. Mahbubani HM, Chong JP, Chevalier S, Thommes P, Blow JJ. Cell cycle regulation of the replication licensing system: involvement of a Cdk-dependent inhibitor. J Cell Biol 1997;136:125-135.
69. Edwards MC, Tutter AV, Cvetic C, Gilbert CH, Prokhorova TA, Walter JC. MCM2-7 complexes bind chromatin in a distributed pattern surrounding ORC in Xenopus egg extracts. J Biol Chem 2002;277:33049-33057.
70. Blow JJ, Laskey RA. Initiation of DNA replication in nuclei and purified DNA by a cell-free extract of Xenopus eggs. Cell 1986;47:577-587.
71. Blow JJ, Sleeman AM. Replication of purified DNA in Xenopus egg extract is dependent on nuclear assembly. J Cell Sci 1990;95:383-391.
72. Hyrien O, Méchali M. Plasmid replication in Xenopus eggs and egg extracts: a 2D gel electrophoretic analysis. Nucleic Acids Res 1992;20:1463-1469.
73. Michalet X, et al. Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science 1997;277:1518-1523.
74. Kolmogorov AN. On the statistical theory of crystallization in metals. Izv Akad Nauk SSSR, Ser Fiz 1937;1:355-359.
75. Herrick J, Jun S, Bechhoefer J, Bensimon A. Kinetic model of DNA replication in eukaryotic organisms. J Mol Biol 2002;320:741-750.
76. Parra I, Windle B. High resolution visual mapping of stretched DNA by fluorescent hybridization. Nat Genet 1993;5:17-21.
77. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, Lockhart DJ, Davis RW, Brewer BJ, Fangman WL. Replication dynamics of the yeast genome. Science 2001;294:115-121.
78. Wyrick JJ, Aparicio JG, Chen T, Barnett JD, Jennings EG, Young RA, Bell SP, Aparicio OM. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 2001;294:2357-2360.
79. Bielinsky AK, Blitzblau H, Beall EL, Ezrokhi M, Smith HS, Botchan MR, Gerbi SA. Origin recognition complex binding to a metazoan replication origin. Curr Biol 2001;11:1427-1431.
80. Ladenburger EM, Keller C, Knippers R. Identification of a binding region for human origin recognition complex proteins 1 and 2 that coincides with an origin of DNA replication. Mol Cell Biol 2002;22:1036-1048.
81. Austin RJ, Orr-Weaver TL, Bell SP. Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev 1999;13:2639-2649.
82. Alexandrow MG, Ritzi M, Pemov A, Hamlin JL. A potential role for mini-chromosome maintenance (MCM) proteins in initiation at the dihydrofolate reductase replication origin. J Biol Chem 2002;277:2702-2708.
83. Pasero P, Duncker BP, Schwob E, Gasser SM. A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes Dev 1999;13:2159-2176.
84. Jares P, Blow JJ. Xenopus cdc7 function is dependent on licensing but not on XORC, XCdc6, or CDK activity and is required for XCdc45 loading. Genes Dev 2000;14:1528-1540.