Abstract
The replication of the genome of a eukaryotic cell is a complex process requiring the ordered assembly of multiprotein replisomes at many chromosomal sites. The process is strictly controlled during the cell cycle to ensure the complete and faithful transmission of genetic information to progeny cells. Our current understanding of the mechanisms of eukaryotic DNA replication has evolved over a period of more than 30 years through the efforts of many investigators. The aim of this perspective is to provide a brief history of the major advances during this period.
References
Abid Ali F, Renault L, Gannon J, Gahlon HL, Kotecha A, Zhou JC, Rueda D, Costa A (2016) Cryo-EM structures of the eukaryotic replicative helicase bound to a translocation substrate. Nat Commun 7:10708
Aparicio OM, Weinstein DM, Bell SP (1997) Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 91(1):59–69
Aparicio OM, Stout AM, Bell SP (1999) Differential assembly of cdc45p and DNA polymerases at early and late origins of DNA replication [in process citation]. Proc Natl Acad Sci U S A 96(16):9130–9135
Araki H, Ropp PA, Johnson AL, Johnston LH, Morrison A, Sugino A (1992) DNA polymerase II, the probable homolog of mammalian DNA polymerase epsilon, replicates chromosomal DNA in the yeast Saccharomyces cerevisiae. EMBO J 11:733
Araki H, Leem SH, Phongdara A, Sugino A (1995) Dpb11, which interacts with DNA polymerase II (epsilon) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc Natl Acad Sci U S A 92(25):11791–11795
Arias EE, Walter JC (2005) Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes Dev 19(1):114–126
Arias EE, Walter JC (2006) PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat Cell Biol 8(1):84–90
Arias EE, Walter JC (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 21(5):497–518
Balakrishnan L, Bambara RA (2013) Okazaki fragment metabolism. Cold Spring Harb Perspect Biol 5(2), a010173
Baxter J, Diffley JF (2008) Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast. Mol Cell 30(6):790–802
Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR (2002) Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420(6917):833–837
Bechhoefer J, Rhind N (2012) Replication timing and its emergence from stochastic processes. Trends Genet 28(8):374–381
Bell SP (1995) Eukaryotic replicators and associated protein complexes. Curr Opin Genet Dev 5(2):162–167
Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71:333–374
Bell SP, Kaguni JM (2013) Helicase loading at chromosomal origins of replication. Cold Spring Harb Perspect Biol 5(6), a010124
Bell SP, Stillman B (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357(6374):128–134
Bell SP, Kobayashi R, Stillman B (1993) Yeast origin recognition complex functions in transcription silencing and DNA replication. Science 262(5141):1844–1849
Bell SP, Mitchell J, Leber J, Kobayashi R, Stillman B (1995) The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83(4):563–568
Berbenetz NM, Nislow C, Brown GW (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet 6(9), e1001092
Bessman MJ, Kornberg A, Lehman IR, Simms ES (1956) Enzymic synthesis of deoxyribonucleic acid. Biochim Biophys Acta 21(1):197–198
Blow JJ (1993) Preventing re-replication of DNA in a single cell cycle: evidence for a replication licensing factor. J Cell Biol 122(5):993–1002
Blow JJ, Laskey RA (1988) A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature 332:546–548
Bochman ML, Schwacha A (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31(2):287–293
Borowiec JA, Hurwitz J (1988) Localized melting and structural changes in the SV40 origin of replication induced by T-antigen. EMBO J 7(10):3149–3158
Bowman GD, Goedken ER, Kazmirski SL, O’Donnell M, Kuriyan J (2005) DNA polymerase clamp loaders and DNA recognition. FEBS Lett 579(4):863–867
Breier AM, Chatterji S, Cozzarelli NR (2004) Prediction of Saccharomyces cerevisiae replication origins. Genome Biol 5(4):R22
Brewer BJ, Fangman WL (1987) The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51(3):463–471
Broach JR, Li YY, Feldman J, Jayaram M, Abraham J, Nasmyth KA, Hicks JB (1983) Localization and sequence analysis of yeast origins of DNA replication. Cold Spring Harb Symp Quant Biol 47(Pt 2):1165–1173
Broek D, Bartlett R, Crawford K, Nurse P (1991) Involvement of p34cdc2 in establishing the dependency of S phase on mitosis. Nature 349(6308):388–393
Brush GS, Kelly TJ, Stillman B (1995) Identification of eukaryotic DNA replication proteins using simian virus 40 in vitro replication system. Methods Enzymol 262:522–548
Budd ME, Sitney KC, Campbell JL (1989) Purification of DNA polymerase II, a distinct DNA polymerase, from Saccharomyces cerevisiae. J Biol Chem 264(11):6557–6565
Burgers PM, Gordenin D, Kunkel TA (2016) Who is leading the replication fork, Pol epsilon or Pol delta? Mol Cell 61(4):492–493
Byrnes JJ, Downey KM, Black VL, So AG (1976) A new mammalian DNA polymerase with 3′ to 5′ exonuclease activity: DNA polymerase delta. Biochemistry 15(13):2817–2823
Cai J, Uhlmann F, Gibbs E, Flores-Rozas H, Lee CG, Phillips B, Finkelstein J, Yao N, O’Donnell M, Hurwitz J (1996) Reconstitution of human replication factor C from its five subunits in baculovirus-infected insect cells. Proc Natl Acad Sci U S A 93(23):12896–12901
Cairns J (1963) The bacterial chromosome and its manner of replication as seen by autoradiography. J Mol Biol 6:208–213
Campbell JL (1986) Eukaryotic DNA replication. Annu Rev Biochem 55:733–771
Campbell JL, Newlon CS (1991) Chromosomal DNA replication. In: Broach JR, Pringle JR, Jones EW (eds) The molecular and cellular biology of the yeast saccharomyces, vol 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 41–146
Cegielska A, Virshup DM (1993) Control of simian virus 40 DNA replication by the HeLa cell nuclear kinase casein kinase I. Mol Cell Biol 13(2):1202–1211
Cegielska A, Moarefi I, Fanning E, Virshup DM (1994) T-antigen kinase inhibits simian virus 40 DNA replication by phosphorylation of intact T antigen on serines 120 and 123. J Virol 68(1):269–275
Celniker SE, Sweder K, Srienc F, Bailey JE, Campbell JL (1984) Deletion mutations affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae. Mol Cell Biol 4(11):2455–2466
Challberg MD, Kelly TJ (1979) Adenovirus DNA replication in vitro. Proc Natl Acad Sci U S A 76(2):655–659
Challberg MD, Kelly TJ (1982) Eukaryotic DNA replication: viral and plasmid model systems. Annu Rev Biochem 51:901–934
Challberg MD, Kelly TJ (1989) Animal virus DNA replication. Annu Rev Biochem 58(671):671–717
Challberg MD, Desiderio SV, Kelly TJ (1980) Adenovirus DNA replication in vitro: characterization of a protein covalently linked to nascent DNA strands. Proc Natl Acad Sci U S A 77(9):5105–5109
Challberg MD, Ostrove JM, Kelly TJ Jr (1982) Initiation of adenovirus DNA replication: detection of covalent complexes between nucleotide and the 80-kilodalton terminal protein. J Virol 41(1):265–270
Chen R, Wold MS (2014) Replication protein a: single-stranded DNA’s first responder: dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. BioEssays 36(12):1156–1161
Chong JP, Mahbubani HM, Khoo CY, Blow JJ (1995) Purification of an MCM-containing complex as a component of the DNA replication licensing system [see comments]. Nature 375(6530):418–421
Chong JP, Thommes P, Blow JJ (1996) The role of MCM/P1 proteins in the licensing of DNA replication. Trends Biochem Sci 21(3):102–106
Chong JP, Hayashi MK, Simon MN, Xu RM, Stillman B (2000) A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci U S A 97(4):1530–1535
Chuang R, Kelly TJ (1999) The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc Natl Acad Sci U S A 96:2656–2661
Clarey MG, Erzberger JP, Grob P, Leschziner AE, Berger JM, Nogales E, Botchan M (2006) Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex. Nat Struct Mol Biol 13(8):684–690
Clyne RK, Kelly TJ (1995) Genetic analysis of an ARS element from the fission yeast Schizosaccharomyces pombe. EMBO J 14(24):6348–6357
Cocker JH, Piatti S, Santocanale C, Nasmyth K, Diffley JF (1996) An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature 379(6561):180–182
Coleman TR, Carpenter PB, Dunphy WG (1996) The Xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell 87(1):53–63
Collins KL, Kelly TJ (1991) Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase. Mol Cell Biol 11(4):2108–2115
Collins KL, Russo AA, Tseng BY, Kelly TJ (1993) The role of the 70 kDa subunit of human DNA polymerase alpha in DNA replication. EMBO J 12(12):4555–4566
Cook JG, Chasse DA, Nevins JR (2004) The regulated association of Cdt1 with minichromosome maintenance proteins and Cdc6 in mammalian cells. J Biol Chem 279(10):9625–9633
Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, Botchan MR, Berger JM (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18(4):471–477
Costa A, Renault L, Swuec P, Petojevic T, Pesavento JJ, Ilves I, MacLellan-Gibson K, Fleck RA, Botchan MR, Berger JM (2014) DNA binding polarity, dimerization, and ATPase ring remodeling in the CMG helicase of the eukaryotic replisome. Elife 3, e03273
D’Urso G, Marraccino RL, Marshak DR, Roberts JM (1990) Cell cycle control of DNA replication by a homologue from human cells of the p34cdc2 protein kinase. Science 250(4982):786–791
Dahmann C, Diffley JF, Nasmyth KA (1995) S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of replication origins to a pre-replicative state. Curr Biol 5(11):1257–1269
Dai J, Chuang RY, Kelly TJ (2005) DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci U S A 102(2):337–342
Danna KJ, Nathans D (1972) Bidirectional replication of Simian Virus 40 DNA. Proc Natl Acad Sci U S A 69(11):3097–3100
Dave A, Cooley C, Garg M, Bianchi A (2014) Protein phosphatase 1 recruitment by Rif1 regulates DNA replication origin firing by counteracting DDK activity. Cell Rep 7(1):53–61
Dean FB, Bullock P, Murakami Y, Wobbe CR, Weissbach L, Hurwitz J (1987) Simian virus 40 (SV40) DNA replication: SV40 large T antigen unwinds DNA containing the SV40 origin of replication. Proc Natl Acad Sci U S A 84:16–20
Dean FB, Borowiec JA, Eki T, Hurwitz J (1992) The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J Biol Chem 267(20):14129–14137
Deegan TD, Yeeles JT, Diffley JF (2016) Phosphopeptide binding by Sld3 links Dbf4-dependent kinase to MCM replicative helicase activation. EMBO J 35(9):961–973
Delucia A, Lewton B, Tjian R, Tegtmeyer P (1983) Topography of simian virus 40 A protein-DNA complexes: arrangement of pentanucleotide interaction sites at the origin of replication. J Virol 46:143–150
Dershowitz A, Snyder M, Sbia M, Skurnick JH, Ong LY, Newlon CS (2007) Linear derivatives of Saccharomyces cerevisiae chromosome III can be maintained in the absence of autonomously replicating sequence elements. Mol Cell Biol 27(13):4652–4663
Desiderio SV, Kelly TJ (1981) Structure of the linkage between adenovirus DNA and the 55,000 molecular weight terminal protein. J Mol Biol 145(2):319–337
van Deursen F, Sengupta S, De Piccoli G, Sanchez-Diaz A, Labib K (2012) Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J 31(9):2195–2206
Devault A, Vallen EA, Yuan T, Green S, Bensimon A, Schwob E (2002) Identification of Tah11/Sid2 as the ortholog of the replication licensing factor Cdt1 in Saccharomyces cerevisiae. Curr Biol 12(8):689–694
Devbhandari S, Jiang J, Kumar C, Whitehouse I, Remus D (2017) Chromatin constrains the initiation and elongation of DNA replication. Mol Cell 65(1):131–141
Dewar JM, Budzowska M, Walter JC (2015) The mechanism of DNA replication termination in vertebrates. Nature 525(7569):345–350
Diffley JF (1996) Once and only once upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev 10(22):2819–2830
Diffley JF, Cocker JH (1992) Protein-DNA interactions at a yeast replication origin. Nature 357(6374):169–172
Diffley JF, Cocker JH, Dowell SJ, Rowley A (1994) Two steps in the assembly of complexes at yeast replication origins in vivo. Cell 78(2):303–316
DiNardo S, Voelkel K, Sternglanz R (1984) DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc Natl Acad Sci U S A 81(9):2616–2620
Donovan S, Harwood J, Drury LS, Diffley JF (1997) Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc Natl Acad Sci U S A 94(11):5611–5616
Dornreiter I, Erdile LF, Gilbert IU, von Winkler D, Kelly TJ, Fanning E (1992) Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. EMBO J 11(2):769–776
Drury LS, Perkins G, Diffley JF (1997) The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J 16(19):5966–5976
Dua R, Levy DL, Campbell JL (1999) Analysis of the essential functions of the C-terminal protein/protein interaction domain of saccharomyces cerevisiae pol epsilon and its unexpected ability to support growth in the absence of the DNA polymerase domain [in process citation]. J Biol Chem 274(32):22283–22288
Dubey DD, Zhu J, Carlson DL, Sharma K, Huberman JA (1994) Three ARS elements contribute to the ura4 replication origin region in the fission yeast, Schizosaccharomyces pombe. EMBO J 13(15):3638–3647
Dubey DD, Kim SM, Todorov IT, Huberman JA (1996) Large, complex modular structure of a fission yeast DNA replication origin. Curr Biol 6(4):467–473
Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, MacAlpine DM (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21(2):164–174
Edgell DR, Doolittle FW (1997) Archaea and the origin(s) of DNA replication proteins. Cell 89:995–998
Enemark EJ, Joshua-Tor L (2008) On helicases and other motor proteins. Curr Opin Struct Biol 18(2):243–257
Enomoto T, Lichy JH, Ikeda JE, Hurwitz J (1981) Adenovirus DNA replication in vitro: purification of the terminal protein in a functional form. Proc Natl Acad Sci U S A 78(11):6779–6783
Evrin C, Clarke P, Zech J, Lurz R, Sun J, Uhle S, Li H, Stillman B, Speck C (2009) A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc Natl Acad Sci U S A 106(48):20240–20245
Fachinetti D, Bermejo R, Cocito A, Minardi S, Katou Y, Kanoh Y, Shirahige K, Azvolinsky A, Zakian VA, Foiani M (2010) Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol Cell 39(4):595–605
Fairman MP, Stillman B (1988) Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J 7(4):1211–1218
Fangman WL, Brewer BJ (1991) Activation of replication origins within yeast chromosomes. Annu Rev Cell Biol 7(375):375–402
Feng W, D’Urso G (2001) Schizosaccharomyces pombe cells lacking the amino-terminal catalytic domains of DNA polymerase epsilon are viable but require the DNA damage checkpoint control. Mol Cell Biol 21(14):4495–4504
Friedman KL, Brewer BJ, Fangman WL (1997) Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2(11):667–678
Fu YV, Yardimci H, Long DT, Ho TV, Guainazzi A, Bermudez VP, Hurwitz J, van Oijen A, Scharer OD, Walter JC (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146(6):931–941
Gai D, Zhao R, Li D, Finkielstein CV, Chen XS (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119(1):47–60
Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, Labib K (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8(4):358–366
Gambus A, van Deursen F, Polychronopoulos D, Foltman M, Jones RC, Edmondson RD, Calzada A, Labib K (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 28(19):2992–3004
Georgescu R, Langston L, O’Donnell M (2015a) A proposal: evolution of PCNA’s role as a marker of newly replicated DNA. DNA Repair (Amst) 29:4–15
Georgescu RE, Schauer GD, Yao NY, Langston LD, Yurieva O, Zhang D, Finkelstein J, O’Donnell ME (2015b) Reconstitution of a eukaryotic replisome reveals suppression mechanisms that define leading/lagging strand operation. Elife 4, e04988
Gopalakrishnan V, Simancek P, Houchens C, Snaith HA, Frattini MG, Sazer S, Kelly TJ (2001) Redundant control of rereplication in fission yeast. Proc Natl Acad Sci U S A 98(23):13114–13119
Gros J, Devbhandari S, Remus D (2014) Origin plasticity during budding yeast DNA replication in vitro. EMBO J 33(6):621–636
Gros J, Kumar C, Lynch G, Yadav T, Whitehouse I, Remus D (2015) Post-licensing specification of eukaryotic replication origins by facilitated Mcm2-7 sliding along DNA. Mol Cell 60(5):797–807
Guarino E, Shepherd ME, Salguero I, Hua H, Deegan RS, Kearsey SE (2011) Cdt1 proteolysis is promoted by dual PIP degrons and is modulated by PCNA ubiquitylation. Nucleic Acids Res 39(14):5978–5990
Hardy CF, Dryga O, Seematter S, Pahl PM, Sclafani RA (1997) mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p. Proc Natl Acad Sci U S A 94(7):3151–3155
Hauk G, Berger JM (2016) The role of ATP-dependent machines in regulating genome topology. Curr Opin Struct Biol 36:85–96
Hayano M, Kanoh Y, Matsumoto S, Renard-Guillet C, Shirahige K, Masai H (2012) Rif1 is a global regulator of timing of replication origin firing in fission yeast. Genes Dev 26(2):137–150
Hayashi MT, Takahashi TS, Nakagawa T, Nakayama J, Masukata H (2009) The heterochromatin protein Swi6/HP1 activates replication origins at the pericentromeric region and silent mating-type locus. Nat Cell Biol 11(3):357–362
Hayles J, Fisher D, Woollard A, Nurse P (1994) Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 78(5):813–822
Heichinger C, Penkett CJ, Bahler J, Nurse P (2006) Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25(21):5171–5179
Heller RC, Kang S, Lam WM, Chen S, Chan CS, Bell SP (2011) Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 146(1):80–91
Hennessy KM, Clark CD, Botstein D (1990) Subcellular localization of yeast CDC46 varies with the cell cycle. Genes Dev 4(12B):2252–2263
Herrmann R, Huf J, Bonhoeffer F (1972) Cross hybridization and rate of chain elongation of the two classes of DNA intermediates. Nat New Biol 240(103):235–237
Hiraga S, Alvino GM, Chang F, Lian HY, Sridhar A, Kubota T, Brewer BJ, Weinreich M, Raghuraman MK, Donaldson AD (2014) Rif1 controls DNA replication by directing Protein Phosphatase 1 to reverse Cdc7-mediated phosphorylation of the MCM complex. Genes Dev 28(4):372–383
Hopwood B, Dalton S (1996) Cdc45p assembles into a complex with Cdc46p/Mcm5p, is required for minichromosome maintenance, and is essential for chromosomal DNA replication. Proc Natl Acad Sci U S A 93(22):12309–12314
Hsiao CL, Carbon J (1979) High-frequency transformation of yeast by plasmids containing the cloned yeast ARG4 gene. Proc Natl Acad Sci U S A 76(8):3829–3833
Hua XH, Newport J (1998) Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J Cell Biol 140:271–281
Hua XH, Yan H, Newport J (1997) A role for Cdk2 kinase in negatively regulating DNA replication during S phase of the cell cycle. J Cell Biol 137(1):183–192
Huberman JA, Riggs AD (1968) On the mechanism of DNA replication in mammalian chromosomes. J Mol Biol 32(2):327–341
Huberman JA, Spotila LD, Nawotka KA, el Assouli S, Davis LR (1987) The in vivo replication origin of the yeast 2 microns plasmid. Cell 51(3):473–481
Hurwitz J, Dean FB, Kwong AD, Lee SH (1990) The in vitro replication of DNA containing the SV40 origin. J Biol Chem 265(30):18043–18046
Ilves I, Petojevic T, Pesavento JJ, Botchan MR (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 37(2):247–258
Ishimi Y (1997) A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex [published erratum appears in J Biol Chem 1998 Sep 4;273(36):23616]. J Biol Chem 272(39):24508–24513
Ishimi Y, Sugasawa K, Hanaoka F, Eki T, Hurwitz J (1992) Topoisomerase II plays an essential role as a swivelase in the late stage of SV40 chromosome replication in vitro. J Biol Chem 267(1):462–466
Jacob F, Brenner S, Cuzin F (1964) On the regulation of DNA replication in bacteria. Cold Spring Harb Symp Quant Biol 28:329–348
Jallepalli PV, Kelly TJ (1996) Rum1 and Cdc18 link inhibition of cyclin-dependent kinase to the initiation of DNA replication in Schizosaccharomyces pombe. Genes Dev 10(5):541–552
Jallepalli PV, Brown GW, Muzi-Falconi M, Tien D, Kelly TJ (1997) Regulation of the replication initiator protein p65cdc18 by CDK phosphorylation. Genes Dev 11(21):2767–2779
Jeruzalmi D, O’Donnell M, Kuriyan J (2002) Clamp loaders and sliding clamps. Curr Opin Struct Biol 12(2):217–224
Johnson A, O’Donnell M (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem 74:283–315
de Jong RN, van der Vliet PC, Brenkman AB (2003) Adenovirus DNA replication: protein priming, jumping back and the role of the DNA binding protein DBP. Curr Top Microbiol Immunol 272:187–211
Kaguni LS, Rossignol JM, Conaway RC, Lehman IR (1983) Isolation of an intact DNA polymerase-primase from embryos of Drosophila melanogaster. Proc Natl Acad Sci U S A 80(8):2221–2225
Kamimura Y, Masumoto H, Sugino A, Araki H (1998) Sld2, which interacts with Dpb11 in Saccharomyces cerevisiae, is required for chromosomal DNA replication. Mol Cell Biol 18(10):6102–6109
Kamimura Y, Tak YS, Sugino A, Araki H (2001) Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae. EMBO J 20(8):2097–2107
Kanemaki M, Labib K (2006) Distinct roles for Sld3 and GINS during establishment and progression of eukaryotic DNA replication forks. EMBO J 25(8):1753–1763
Kanke M, Kodama Y, Takahashi TS, Nakagawa T, Masukata H (2012) Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J 31(9):2182–2194
Kaplan DL, Davey MJ, O’Donnell M (2003) Mcm4,6,7 uses a “pump in ring” mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J Biol Chem 278(49):49171–49182
Kawasaki Y, Kim HD, Kojima A, Seki T, Sugino A (2006) Reconstitution of Saccharomyces cerevisiae prereplicative complex assembly in vitro. Genes Cells 11(7):745–756
Kaykov A, Nurse P (2015) The spatial and temporal organization of origin firing during the S-phase of fission yeast. Genome Res 25(3):391–401
Kelly TJ (1988) SV40 DNA replication. J Biol Chem 263:17889–17892
Kelman Z, Lee JK, Hurwitz J (1999) The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc Natl Acad Sci U S A 96(26):14783–14788
Kesti T, Flick K, Keranen S, Syvaoja JE, Wittenberg C (1999) DNA polymerase epsilon catalytic domains are dispensable for DNA replication, DNA repair, and cell viability. Mol Cell 3(5):679–685
Kim SM, Huberman JA (2001) Regulation of replication timing in fission yeast. EMBO J 20(21):6115–6126
King AJ, van der Vliet PC (1994) A precursor terminal protein-trinucleotide intermediate during initiation of adenovirus DNA replication: regeneration of molecular ends in vitro by a jumping back mechanism. EMBO J 13(23):5786–5792
Kong D, DePamphilis ML (2001) Site-specific DNA binding of the Schizosaccharomyces pombe origin recognition complex is determined by the Orc4 subunit. Mol Cell Biol 21(23):8095–8103
Kornberg A (1981) DNA replication, 1st edn. W.H. Freeman and Co, New York
Kornberg A, Baker TA (1992) DNA replication, 2nd edn. Freeman and Co., New York
Kurat CF, Yeeles JT, Patel H, Early A, Diffley JF (2017) Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol Cell 65(1):117–130
Labib K, Diffley JF, Kearsey SE (1999) G1-phase and B-type cyclins exclude the DNA-replication factor Mcm4 from the nucleus. Nat Cell Biol 1(7):415–422
Labib K, Tercero JA, Diffley JF (2000) Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288(5471):1643–1647
Labib K, Kearsey SE, Diffley JF (2001) MCM2-7 proteins are essential components of prereplicative complexes that accumulate cooperatively in the nucleus during G1-phase and are required to establish, but not maintain, the S-phase checkpoint. Mol Biol Cell 12(11):3658–3667
Lang GI, Murray AW (2011) Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biol Evol 3:799–811
Langston LD, Zhang D, Yurieva O, Georgescu RE, Finkelstein J, Yao NY, Indiani C, O’Donnell ME (2014) CMG helicase and DNA polymerase epsilon form a functional 15-subunit holoenzyme for eukaryotic leading-strand DNA replication. Proc Natl Acad Sci U S A 111(43):15390–15395
Lee S-H, Eki T, Hurwitz J (1989) Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases alpha and delta. Proc Natl Acad Sci U S A 86(19):7361–7365
Lee SH, Kwong AD, Pan ZQ, Hurwitz J (1991) Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase delta. J Biol Chem 266(1):594–602
Lee C, Hong B, Choi JM, Kim Y, Watanabe S, Ishimi Y, Enomoto T, Tada S, Kim Y, Cho Y (2004) Structural basis for inhibition of the replication licensing factor Cdt1 by geminin. Nature 430(7002):913–917
Lehman IR, Kaguni LS (1989) DNA polymerase alpha. J Biol Chem 264:4265–4268
Leipe DD, Aravind L, Koonin EV (1999) Did DNA replication evolve twice independently? Nucleic Acids Res 27(17):3389–3401
Leonard AC, Mechali M (2013) DNA replication origins. Cold Spring Harb Perspect Biol 5(10):a010116
Levine AJ, Kang HS, Billheimer FE (1970) DNA replication in SV40 infected cells. I. Analysis of replicating SV40 DNA. J Mol Biol 50(2):549–568
Lewis JS, Jergic S, Dixon NE (2016) The E. coli DNA replication fork. Enzyme 39:31–88
Li JJ, Kelly TJ (1984) Simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A 81:6973–6977
Li D, Zhao R, Lilyestrom W, Gai D, Zhang R, DeCaprio JA, Fanning E, Jochimiak A, Szakonyi G, Chen XS (2003a) Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423(6939):512–518
Li X, Zhao Q, Liao R, Sun P, Wu X (2003b) The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J Biol Chem 278(33):30854–30858
Liu E, Li X, Yan F, Zhao Q, Wu X (2004) Cyclin-dependent kinases phosphorylate human Cdt1 and induce its degradation. J Biol Chem 279(17):17283–17288
Lopez-Mosqueda J, Maas NL, Jonsson ZO, Defazio-Eli LG, Wohlschlegel J, Toczyski DP (2010) Damage-induced phosphorylation of Sld3 is important to block late origin firing. Nature 467(7314):479–483
Lucas I, Germe T, Chevrier-Miller M, Hyrien O (2001) Topoisomerase II can unlink replicating DNA by precatenane removal. EMBO J 20(22):6509–6519
Lutzmann M, Maiorano D, Mechali M (2006) A Cdt1-geminin complex licenses chromatin for DNA replication and prevents rereplication during S phase in Xenopus. EMBO J 25(24):5764–5774
Madine MA, Khoo CY, Mills AD, Laskey RA (1995) MCM3 complex required for cell cycle regulation of DNA replication in vertebrate cells [see comments]. Nature 375(6530):421–424
Maine GT, Sinha P, Tye B-K (1984) Mutants of S. cerevisiae defective in the maintenance of minichromosomes. Genetics 106:365–385
Maiorano D, Moreau J, Mechali M (2000) XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis [see comments]. Nature 404(6778):622–625
Makarova KS, Koonin EV (2013) Archaeology of eukaryotic DNA replication. Cold Spring Harb Perspect Biol 5(11):a012963
Marahrens Y, Stillman B (1992) A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255(5046):817–823
Maric M, Maculins T, De Piccoli G, Labib K (2014) Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science 346(6208):1253596
Masumoto H, Muramatsu S, Kamimura Y, Araki H (2002) S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast. Nature 415(6872):651–655
Mattarocci S, Shyian M, Lemmens L, Damay P, Altintas DM, Shi T, Bartholomew CR, Thoma NH, Hardy CF, Shore D (2014) Rif1 controls DNA replication timing in yeast through the PP1 phosphatase Glc7. Cell Rep 7(1):62–69
McGarry TJ, Kirschner MW (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93(6):1043–1053
McVey D, Brizuela L, Mohr I, Marshak DR, Gluzman Y, Beach D (1989) Phosphorylation of large tumour antigen by cdc2 stimulates SV40 DNA replication. Nature 341:503–507
McVey D, Ray S, Gluzman Y, Berger L, Wildeman AG, Marshak DR, Tegtmeyer P (1993) cdc2 phosphorylation of threonine 124 activates the origin-unwinding functions of simian virus 40 T antigen. J Virol 67(9):5206–5215
Melendy T, Stillman B (1993) An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J Biol Chem 268(5):3389–3395
Meselson M, Stahl F (1958) The replication of DNA in Escherichia coli. Proc Natl Acad Sci U S A 44(7):671–682
Moarefi IF, Small D, Gilbert I, Hopfner M, Randall SK, Schneider C, Russo AA, Ramsperger U, Arthur AK, Stahl H, Kelly TJ, Fanning E (1993) Mutation of the cyclin-dependent kinase phosphorylation site in simian virus 40 (SV40) large T antigen specifically blocks SV40 origin DNA unwinding. J Virol 67(8):4992–5002
Moir D, Stewart SE, Osmond BC, Botstein D (1982) Cold-sensitive cell-division-cycle mutants of yeast: isolation, properties, and pseudoreversion studies. Genetics 100(4):547–563
Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129(4):665–679
Moreno S, Nurse P (1994) Regulation of progression through the G1 phase of the cell cycle by the rum1+ gene. Nature 367(6460):236–242
Morrison A, Araki H, Clark AB, Hamatake RK, Sugino A (1990) A third essential DNA polymerase in S. cerevisiae. Cell 62(6):1143–1151
Moyer SE, Lewis PW, Botchan MR (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci U S A 103(27):10236–10241
Murakami Y, Wobbe CR, Weissbach L, Dean FB, Hurwitz J (1986) Role of DNA polymerase a and DNA primase in simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A 83:2869–2873
Murakami Y, Eki T, Hurwitz J (1992) Studies on the initiation of simian virus 40 replication in vitro: RNA primer synthesis and its elongation. Proc Natl Acad Sci U S A 89(3):952–956
Muramatsu S, Hirai K, Tak YS, Kamimura Y, Araki H (2010) CDK-dependent complex formation between replication proteins Dpb11, Sld2, Pol (epsilon), and GINS in budding yeast. Genes Dev 24(6):602–612
Nagata K, Guggenheimer RA, Enomoto T, Lichy JH, Hurwitz J (1982) Adenovirus DNA replication in vitro: identification of a host factor that stimulates synthesis of the preterminal protein-dCMP complex. Proc Natl Acad Sci U S A 79(21):6438–6442
Nagata K, Guggenheimer RA, Hurwitz J (1983) Adenovirus DNA replication in vitro: synthesis of full-length DNA with purified proteins. Proc Natl Acad Sci U S A 80(14):4266–4270
Newlon CS (1988) Yeast chromosome replication and segregation. Microbiol Rev 52(4):568–601
Nguyen VQ, Co C, Irie K, Li JJ (2000) Clb/Cdc28 kinases promote nuclear export of the replication initiator proteins Mcm2-7. Curr Biol 10(4):195–205
Nguyen VQ, Co C, Li JJ (2001) Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411(6841):1068–1073
Nishitani H, Nurse P (1995) p65cdc18 plays a major role controlling the initiation of DNA replication in fission yeast. Cell 83(3):397–405
Nishitani H, Lygerou Z, Nishimoto T, Nurse P (2000) The Cdt1 protein is required to license DNA for replication in fission yeast [see comments]. Nature 404(6778):625–628
O’Donnell M, Li H (2016) The eukaryotic replisome goes under the microscope. Curr Biol 26(6):R247–R256
O’Neill EA, Fletcher C, Burrow CR, Heintz N, Roeder RG, Kelly TJ (1988) Transcription factor OTF-1 is functionally identical to the DNA replication factor NF-III. Science 241:1210–1213
Okazaki R, Okazaki T, Sakabe K, Sugimoto K, Sugino A (1968) Mechanism of DNA chain growth. I. Possible discontinuity and unusual secondary structure of newly synthesized chains. Proc Natl Acad Sci U S A 59(2):598–605
Olivera BM, Bonhoeffer F (1972) Discontinuous DNA replication in vitro. I. Two distinct size classes of intermediates. Nat New Biol 240(103):233–235
On KF, Beuron F, Frith D, Snijders AP, Morris EP, Diffley JF (2014) Prereplicative complexes assembled in vitro support origin-dependent and independent DNA replication. EMBO J 33(6):605–620
Pacek M, Walter JC (2004) A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J 23(18):3667–3676
Pacek M, Tutter AV, Kubota Y, Takisawa H, Walter JC (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21(4):581–587
Patel PK, Arcangioli B, Baker SP, Bensimon A, Rhind N (2006) DNA replication origins fire stochastically in fission yeast. Mol Biol Cell 17(1):308–316
Plevani P, Foiani M, Valsasnini P, Badaracco G, Cheriathundam E, Chang LM (1985) Polypeptide structure of DNA primase from a yeast DNA polymerase-primase complex. J Biol Chem 260(11):7102–7107
Pospiech H, Kursula I, Abdel-Aziz W, Malkas L, Uitto L, Kastelli M, Vihinen-Ranta M, Eskelinen S, Syvaoja JE (1999) A neutralizing antibody against human DNA polymerase epsilon inhibits cellular but not SV40 DNA replication. Nucleic Acids Res 27(19):3799–3804
Prelich G, Tan CK, Kostura M, Mathews MB, So AG, Downey KM, Stillman B (1987) Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 326(6112):517–520
Pruijn GJ, van Driel W, van der Vliet PC (1986) Nuclear factor III, a novel sequence-specific DNA-binding protein from HeLa cells stimulating adenovirus DNA replication. Nature 322(6080):656–659
Ralph E, Boye E, Kearsey SE (2006) DNA damage induces Cdt1 proteolysis in fission yeast through a pathway dependent on Cdt2 and Ddb1. EMBO Rep 7(11):1134–1139
Randell JC, Fan A, Chan C, Francis LI, Heller RC, Galani K, Bell SP (2010) Mec1 is one of multiple kinases that prime the Mcm2-7 helicase for phosphorylation by Cdc7. Mol Cell 40(3):353–363
Rao PN, Johnson RT (1970) Mammalian cell fusion: studies on the regulation of DNA synthesis and mitosis. Nature 225(228):159–164
Rekosh DM, Russell WC, Bellet AJ, Robinson AJ (1977) Identification of a protein linked to the ends of adenovirus DNA. Cell 11(2):283–295
Remus D, Beall EL, Botchan MR (2004) DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J 23(4):897–907
Remus D, Beuron F, Tolun G, Griffith JD, Morris EP, Diffley JF (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139(4):719–730
Romanowski P, Madine MA, Laskey RA (1996a) XMCM7, a novel member of the Xenopus MCM family, interacts with XMCM3 and colocalizes with it throughout replication [see comments]. Proc Natl Acad Sci U S A 93(19):10189–10194
Romanowski P, Madine MA, Rowles A, Blow JJ, Laskey RA (1996b) The Xenopus origin recognition complex is essential for DNA replication and MCM binding to chromatin. Curr Biol 6(11):1416–1425
Rosenfeld PJ, Kelly TJ (1986) Purification of nuclear factor I by DNA recognition site affinity chromatography. J Biol Chem 261(3):1398–1408
Rowles A, Chong JP, Brown L, Howell M, Evan GI, Blow JJ (1996) Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell 87(2):287–296
Rowles A, Tada S, Blow JJ (1999) Changes in association of the Xenopus origin recognition complex with chromatin on licensing of replication origins. J Cell Sci 112(Pt 12):2011–2018
Samora CP, Saksouk J, Goswami P, Wade BO, Singleton MR, Bates PA, Lengronne A, Costa A, Uhlmann F (2016) Ctf4 links DNA replication with sister chromatid cohesion establishment by recruiting the Chl1 helicase to the replisome. Mol Cell 63(3):371–384
Santocanale C, Diffley JF (1998) A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395(6702):615–618
Santocanale C, Sharma K, Diffley JF (1999) Activation of dormant origins of DNA replication in budding yeast. Genes Dev 13(18):2360–2364
Scheidtmann KH, Virshup DM, Kelly TJ (1991) Protein phosphatase 2A dephosphorylates SV40 large T antigen specifically at residues involved in regulation of the DNA binding activity. J Virol 65:2098–2101
Segurado M, de Luis A, Antequera F (2003) Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4(11):1048–1053
Senga T, Sivaprasad U, Zhu W, Park JH, Arias EE, Walter JC, Dutta A (2006) PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J Biol Chem 281(10):6246–6252
Sengupta S, van Deursen F, de Piccoli G, Labib K (2013) Dpb2 integrates the leading-strand DNA polymerase into the eukaryotic replisome. Curr Biol 23(7):543–552
Sheu YJ, Stillman B (2010) The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463(7277):113–117
Shirahige K, Hori Y, Shiraishi K, Yamashita M, Takahashi K, Obuse C, Tsurimoto T, Yoshikawa H (1998) Regulation of DNA-replication origins during cell-cycle progression. Nature 395(6702):618–621
Siddiqui K, On KF, Diffley JF (2013) Regulating DNA replication in eukarya. Cold Spring Harb Perspect Biol 5(9), a012922
Simmons DT, Melendy T, Usher D, Stillman B (1996) Simian virus 40 large T antigen binds to topoisomerase I. Virology 222(2):365–374
Simon AC, Zhou JC, Perera RL, van Deursen F, Evrin C, Ivanova ME, Kilkenny ML, Renault L, Kjaer S, Matak-Vinkovic D, Labib K, Costa A, Pellegrini L (2014) A Ctf4 trimer couples the CMG helicase to DNA polymerase alpha in the eukaryotic replisome. Nature 510(7504):293–297
Singleton MR, Dillingham MS, Wigley DB (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 76:23–50
Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5(4), a012922
Speck C, Stillman B (2007) Cdc6 ATPase activity regulates ORC x Cdc6 stability and the selection of specific DNA sequences as origins of DNA replication. J Biol Chem 282(16):11705–11714
Speck C, Chen Z, Li H, Stillman B (2005) ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat Struct Mol Biol 12(11):965–971
Stahl H, Droge P, Knippers R (1986) DNA helicase activity of SV40 large tumor antigen. EMBO J 5:1939–1944
Stamatoyannopoulos JA, Adzhubei I, Thurman RE, Kryukov GV, Mirkin SM, Sunyaev SR (2009) Human mutation rate associated with DNA replication timing. Nat Genet 41(4):393–395
Stillman BW (1983) The replication of adenovirus DNA with purified proteins. Cell 35(1):7–9
Stillman B (1989) Initiation of eukaryotic DNA replication in vitro. Annu Rev Cell Biol 5(197):197–245
Stinchcomb DT, Struhl K, Davis RW (1979) Isolation and characterisation of a yeast chromosomal replicator. Nature 282(5734):39–43
Sugimoto N, Tatsumi Y, Tsurumi T, Matsukage A, Kiyono T, Nishitani H, Fujita M (2004) Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J Biol Chem 279(19):19691–19697
Sun J, Fernandez-Cid A, Riera A, Tognetti S, Yuan Z, Stillman B, Speck C, Li H (2014) Structural and mechanistic insights into Mcm2-7 double-hexamer assembly and function. Genes Dev 28(20):2291–2303
Sun J, Shi Y, Georgescu RE, Yuan Z, Chait BT, Li H, O’Donnell ME (2015) The architecture of a eukaryotic replisome. Nat Struct Mol Biol 22(12):976–982
Sundin O, Varshavsky A (1980) Terminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers. Cell 21(1):103–114
Sundin O, Varshavsky A (1981) Arrest of segregation leads to accumulation of highly intertwined catenated dimers: dissection of the final stages of SV40 DNA replication. Cell 25(3):659–669
Sussenbach JS, van der Vliet PC (1984) The mechanism of adenovirus DNA replication and the characterization of replication proteins. Curr Top Microbiol Immunol 109:53–73
Sutani T, Shirahige K (2016) Attaching accessory devices to the replisome. Mol Cell 63(3):347–348. https://doi.org/10.1016/j.molcel.2016.07.017
Tada S, Li A, Maiorano D, Mechali M, Blow JJ (2001) Repression of origin assembly in metaphase depends on inhibition of RLF- B/Cdt1 by geminin. Nat Cell Biol 3(2):107–113
Tak YS, Tanaka Y, Endo S, Kamimura Y, Araki H (2006) A CDK-catalysed regulatory phosphorylation for formation of the DNA replication complex Sld2-Dpb11. EMBO J 25(9):1987–1996
Takayama Y, Kamimura Y, Okawa M, Muramatsu S, Sugino A, Araki H (2003) GINS, a novel multiprotein complex required for chromosomal DNA replication in budding yeast. Genes Dev 17(9):1153–1165
Takeda DY, Parvin JD, Dutta A (2005) Degradation of Cdt1 during S phase is Skp2-independent and is required for efficient progression of mammalian cells through S phase. J Biol Chem 280(24):23416–23423
Tamanoi F, Stillman BW (1982) Function of adenovirus terminal protein in the initiation of DNA replication. Proc Natl Acad Sci U S A 79(7):2221–2225
Tamanoi F, Stillman BW (1983) Initiation of adenovirus DNA replication in vitro requires a specific DNA sequence. Proc Natl Acad Sci U S A 80(21):6446–6450
Tan CK, Castillo C, So AG, Downey KM (1986) An auxiliary protein for DNA polymerase-delta from fetal calf thymus. J Biol Chem 261(26):12310–12316
Tanaka S, Araki H (2013) Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb Perspect Biol 5(12), a010371
Tanaka S, Diffley JF (2002) Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat Cell Biol 4(3):198–207
Tanaka T, Knapp D, Nasmyth K (1997) Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 90(4):649–660
Tanaka S, Umemori T, Hirai K, Muramatsu S, Kamimura Y, Araki H (2007) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445(7125):328–332
Tanaka H, Katou Y, Yagura M, Saitoh K, Itoh T, Araki H, Bando M, Shirahige K (2009) Ctf4 coordinates the progression of helicase and DNA polymerase alpha. Genes Cells 14(7):807–820
Tanaka S, Nakato R, Katou Y, Shirahige K, Araki H (2011) Origin association of Sld3, Sld7, and Cdc45 proteins is a key step for determination of origin-firing timing. Curr Biol 21(24):2055–2063
Tapper DP, DePamphilis ML (1978) Discontinuous DNA replication: accumulation of Simian virus 40 DNA at specific stages in its replication. J Mol Biol 120(3):401–422
Tegtmeyer P (1972) Simian virus 40 deoxyribonucleic acid synthesis: the viral replicon. J Virol 10(4):591–598
Ticau S, Friedman LJ, Ivica NA, Gelles J, Bell SP (2015) Single-molecule studies of origin licensing reveal mechanisms ensuring bidirectional helicase loading. Cell 161(3):513–525
Tjian R (1978) The binding site on SV40 DNA for a T antigen-related protein. Cell 13:165–179
Tseng BY, Ahlem CN (1982) DNA primase activity from human lymphocytes. Synthesis of oligoribonucleotides that prime DNA synthesis. J Biol Chem 257(13):7280–7283
Tsurimoto T, Stillman B (1989) Purification of a cellular replication factor, RF-C, that is required for coordinated synthesis of leading and lagging strands during simian virus 40 DNA replication in vitro. Mol Cell Biol 9(2):609–619
Tsurimoto T, Stillman B (1990) Functions of replication factor C and proliferating-cell nuclear antigen: functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4. Proc Natl Acad Sci U S A 87:1023–1027
Tsurimoto T, Stillman B (1991a) Replication factors required for SV40 DNA replication in vitro. I. DNA structure-specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins. J Biol Chem 266(3):1950–1960
Tsurimoto T, Stillman B (1991b) Replication factors required for SV40 DNA replication in vitro. II. Switching of DNA polymerase alpha and delta during initiation of leading and lagging strand synthesis. J Biol Chem 266(3):1961–1968
Tsurimoto T, Melendy T, Stillman B (1990) Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature 346(6284):534–539
Valle M, Gruss C, Halmer L, Carazo JM, Donate LE (2000) Large T-antigen double hexamers imaged at the simian virus 40 origin of replication. Mol Cell Biol 20(1):34–41
Van Houten J, Newlon CS (1990) Mutational analysis of the consensus sequence of a replication origin from yeast chromosome III. Mol Cell Biol 10(8):3917–3925
Vashee S, Cvetic C, Lu W, Simancek P, Kelly TJ, Walter JC (2003) Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev 17(15):1894–1908
Villa F, Simon AC, Ortiz Bazan MA, Kilkenny ML, Wirthensohn D, Wightman M, Matak-Vinkovic D, Pellegrini L, Labib K (2016) Ctf4 is a hub in the eukaryotic replisome that links multiple CIP-box proteins to the CMG helicase. Mol Cell 63(3):385–396
Virshup DM, Kauffman MG, Kelly TJ (1989) Activation of SV40 DNA replication in vitro by cellular protein phosphatase 2A. EMBO J 8(12):3891–3898
Virshup DM, Russo AA, Kelly TJ (1992) Mechanism of activation of simian virus 40 DNA replication by protein phosphatase 2A. Mol Cell Biol 12(11):4883–4895
Vujcic M, Miller CA, Kowalski D (1999) Activation of silent replication origins at autonomously replicating sequence elements near the HML locus in budding yeast. Mol Cell Biol 19(9):6098–6109
Waga S, Stillman B (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369(6477):207–212
Waga S, Stillman B (1998) The DNA replication fork in eukaryotic cells. Annu Rev Biochem 67:721–751
Waga S, Bauer G, Stillman B (1994) Reconstitution of complete SV40 DNA replication with purified replication factors. J Biol Chem 269(14):10923–10934
Watase G, Takisawa H, Kanemaki MT (2012) Mcm10 plays a role in functioning of the eukaryotic replicative DNA helicase, Cdc45-Mcm-GINS. Curr Biol 22(4):343–349
Weinberg DH, Kelly TJ (1989) Requirement for two DNA polymerases in the replication of simian virus 40 DNA in vitro. Proc Natl Acad Sci U S A 86:9742–9746
Wobbe CR, Weissbach L, Borowiec JA, Dean FB, Murakami Y, Bullock P, Hurwitz J (1987) Replication of SV40 origin-containing DNA with purified proteins. Proc Natl Acad Sci U S A 84:1834–1838
Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A (2000) Inhibition of eukaryotic DNA replication by geminin binding to cdt1. Science 290(5500):2309–2312
Wold MS (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61–92
Wold MS, Kelly TJ (1988) Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc Natl Acad U S A 85:2523–2527
Wold MS, Li JJ, Kelly TJ (1987) Initiation of simian virus 40 DNA replication in vitro: large-tumor-antigen- and origin-dependent unwinding of the template. Proc Natl Acad Sci U S A 84:3643–3647
Wold MS, Li JJ, Weinberg DH, Virshup DM, Sherley JM, Verheyen E, Kelly T (1988) Cellular proteins required for SV40 DNA replication in vitro. In: Kelly T, Stillman B (eds) Eukaryotic DNA replication. Cancer Cells. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 133–142
Woo YH, Li WH (2012) DNA replication timing and selection shape the landscape of nucleotide variation in cancer genomes. Nat Commun 3:1004
Yan H, Gibson S, Tye BK (1991) Mcm2 and Mcm3, two proteins important for ARS activity, are related in structure and function. Genes Dev 5(6):944–957
Yang L, Wold MS, Li JJ, Kelly TJ, Liu LF (1987) Roles of DNA topoisomerases in simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A 84(4):950–954
Yao NY, O’Donnell M (2012) The RFC clamp loader: structure and function. Subcell Biochem 62:259–279
Yao NY, Johnson A, Bowman GD, Kuriyan J, O’Donnell M (2006) Mechanism of proliferating cell nuclear antigen clamp opening by replication factor C. J Biol Chem 281(25):17528–17539
Yeeles JT, Deegan TD, Janska A, Early A, Diffley JF (2015) Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519(7544):431–435
Yeeles JT, Janska A, Early A, Diffley JF (2017) How the eukaryotic replisome achieves rapid and efficient DNA replication. Mol Cell 65(1):105–116
Yuan Z, Bai L, Sun J, Georgescu R, Liu J, O’Donnell ME, Li H (2016) Structure of the eukaryotic replicative CMG helicase suggests a pumpjack motion for translocation. Nat Struct Mol Biol 23(3):217–224
Zegerman P, Diffley JF (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445(7125):281–285
Zegerman P, Diffley JF (2010) Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature 467(7314):474–478
Zhou B, Arnett DR, Yu X, Brewster A, Sowd GA, Xie CL, Vila S, Gai D, Fanning E, Chen XS (2012) Structural basis for the interaction of a hexameric replicative helicase with the regulatory subunit of human DNA polymerase alpha-primase. J Biol Chem 287(32):26854–26866
Zhu W, Ukomadu C, Jha S, Senga T, Dhar SK, Wohlschlegel JA, Nutt LK, Kornbluth S, Dutta A (2007) Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev 21(18):2288–2299
Zlotkin T, Kaufmann G, Jiang Y, Lee MY, Uitto L, Syvaoja J, Dornreiter I, Fanning E, Nethanel T (1996) DNA polymerase epsilon may be dispensable for SV40- but not cellular-DNA replication. EMBO J 15(9):2298–2305
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Kelly, T. (2017). Historical Perspective of Eukaryotic DNA Replication. In: Masai, H., Foiani, M. (eds) DNA Replication. Advances in Experimental Medicine and Biology, vol 1042. Springer, Singapore. https://doi.org/10.1007/978-981-10-6955-0_1
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