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Evolutionary conservation of the CDK targets in eukaryotic DNA replication initiation

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Abstract

A fundamental requirement for all organisms is the faithful duplication and transmission of the genetic material. Failure to accurately copy and segregate the genome during cell division leads to loss of genetic information and chromosomal abnormalities. Such genome instability is the hallmark of the earliest stages of tumour formation. Cyclin-dependent kinase (CDK) plays a vital role in regulating the duplication of the genome within the eukaryotic cell cycle. Importantly, this kinase is deregulated in many cancer types and is an emerging target of chemotherapeutics. In this review, I will consider recent advances concerning the role of CDK in replication initiation across eukaryotes. The implications for strict CDK-dependent regulation of genome duplication in the context of the cell cycle will be discussed.

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References

  • Abe T, Yoshimura A, Hosono Y, Tada S, Seki M, Enomoto T (2011) The N-terminal region of RECQL4 lacking the helicase domain is both essential and sufficient for the viability of vertebrate cells. Role of the N-terminal region of RECQL4 in cells. Biochim Biophys Acta 1813(3):473–479

    CAS  PubMed  Google Scholar 

  • Aparicio OM (2013) Location, location, location: it’s all in the timing for replication origins. Genes Dev 27(2):117–128

    PubMed Central  CAS  PubMed  Google Scholar 

  • Araki H (2010) Cyclin-dependent kinase-dependent initiation of chromosomal DNA replication. Curr Opin Cell Biol 22(6):766–771

    CAS  PubMed  Google Scholar 

  • Araki H (2011) Initiation of chromosomal DNA replication in eukaryotic cells; contribution of yeast genetics to the elucidation. Genes Genet Syst 86(3):141–149

    CAS  PubMed  Google Scholar 

  • Arias EE, Walter JC (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 21(5):497–518

    CAS  PubMed  Google Scholar 

  • Aves SJ, Liu Y, Richards TA (2012) Evolutionary diversification of eukaryotic DNA replication machinery. Subcell Biochem 62:19–35

    CAS  PubMed  Google Scholar 

  • Balestrini A, Cosentino C, Errico A, Garner E, Costanzo V (2010) GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nat Cell Biol 12(5):484–491

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bell SD (2012) Archaeal orc1/cdc6 proteins. Subcell Biochem 62:59–69

    CAS  PubMed  Google Scholar 

  • Bell SD, Botchan MR (2013) The minichromosome maintenance replicative helicase. Cold Spring Harb Perspect Biol 5(11):a012807

    PubMed  Google Scholar 

  • Bell SP, Kaguni JM (2013) Helicase loading at chromosomal origins of replication. Cold Spring Harb Perspect Biol 5(6)

  • Blow JJ, Dutta A (2005) Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6(6):476–486

    PubMed Central  CAS  PubMed  Google Scholar 

  • Blow JJ, Laskey RA (1988) A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature 332(6164):546–548

    CAS  PubMed  Google Scholar 

  • Blow JJ, Ge XQ, Jackson DA (2011) How dormant origins promote complete genome replication. Trends Biochem Sci 36(8):405–414

    PubMed Central  CAS  PubMed  Google Scholar 

  • Boos D, Sanchez-Pulido L, Rappas M, Pearl LH, Oliver AW, Ponting CP, Diffley JF (2011) Regulation of DNA replication through Sld3-Dpb11 interaction is conserved from yeast to humans. Curr Biol 21(13):1152–1157

    CAS  PubMed  Google Scholar 

  • Boos D, Frigola J, Diffley JF (2012) Activation of the replicative DNA helicase: breaking up is hard to do. Curr Opin Cell Biol 24(3):423–430

    CAS  PubMed  Google Scholar 

  • Boos D, Yekezare M, Diffley JF (2013) Identification of a heteromeric complex that promotes DNA replication origin firing in human cells. Science 340(6135):981–984

    CAS  PubMed  Google Scholar 

  • Boye E, Lobner-Olesen A, Skarstad K (2000) Limiting DNA replication to once and only once. EMBO Rep 1(6):479–483

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brummer A, Salazar C, Zinzalla V, Alberghina L, Hofer T (2010) Mathematical modelling of DNA replication reveals a trade-off between coherence of origin activation and robustness against rereplication. PLoS Comput Biol 6(5):e1000783

    PubMed Central  PubMed  Google Scholar 

  • Capp C, Wu J, Hsieh TS (2009) Drosophila RecQ4 has a 3′-5′ DNA helicase activity that is essential for viability. J Biol Chem 284(45):30845–30852

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chowdhury A, Liu G, Kemp M, Chen X, Katrangi N, Myers S, Ghosh M, Yao J, Gao Y, Bubulya P, Leffak M (2010) The DNA unwinding element binding protein DUE-B interacts with Cdc45 in preinitiation complex formation. Mol Cell Biol 30(6):1495–1507

    PubMed Central  CAS  PubMed  Google Scholar 

  • Collart C, Allen GE, Bradshaw CR, Smith JC, Zegerman P (2013) Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341(6148):893–896

    PubMed Central  CAS  PubMed  Google Scholar 

  • Coudreuse D, Nurse P (2010) Driving the cell cycle with a minimal CDK control network. Nature 468(7327):1074–1079

    CAS  PubMed  Google Scholar 

  • Crevel G, Vo N, Crevel I, Hamid S, Hoa L, Miyata S, Cotterill S (2012) Drosophila RecQ4 is directly involved in both DNA replication and the response to UV damage in S2 cells. PLoS One 7(11):e49505

    CAS  PubMed  Google Scholar 

  • Croteau DL, Singh DK, Hoh Ferrarelli L, Lu H, Bohr VA (2012) RECQL4 in genomic instability and aging. Trends Genet 28(12):624–631

    PubMed Central  CAS  PubMed  Google Scholar 

  • Diffley JF (2004) Regulation of early events in chromosome replication. Curr Biol 14(18):R778–R786

    CAS  PubMed  Google Scholar 

  • Drury LS, Diffley JF (2009) Factors affecting the diversity of DNA replication licensing control in eukaryotes. Curr Biol 19(6):530–535

    CAS  PubMed  Google Scholar 

  • Drury LS, Perkins G, Diffley JF (2000) The cyclin-dependent kinase Cdc28p regulates distinct modes of Cdc6p proteolysis during the budding yeast cell cycle. Curr Biol 10(5):231–240

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandez-Cid A, Riera A, Tognetti S, Herrera MC, Samel S, Evrin C, Winkler C, Gardenal E, Uhle S, Speck C (2013) An ORC/Cdc6/MCM2-7 complex is formed in a multistep reaction to serve as a platform for MCM double-hexamer assembly. Mol Cell 50(4):577–588

    CAS  PubMed  Google Scholar 

  • Ferreira MF, Santocanale C, Drury LS, Diffley JF (2000) Dbf4p, an essential S phase-promoting factor, is targeted for degradation by the anaphase-promoting complex. Mol Cell Biol 20(1):242–248

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fukuura M, Nagao K, Obuse C, Takahashi TS, Nakagawa T, Masukata H (2011) CDK promotes interactions of Sld3 and Drc1 with Cut5 for initiation of DNA replication in fission yeast. Mol Biol Cell 22(14):2620–2633

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gaggioli V, Zeiser E, Rivers D, Bradshaw CR, Ahringer J, Zegerman P (2014) CDK phosphorylation of SLD-2 is required for replication initiation and germline development in C. elegans. J Cell Biol 204(4):507–522

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ge XQ, Jackson DA, Blow JJ (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 21(24):3331–3341

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425(6959):737–741

    CAS  PubMed  Google Scholar 

  • Going JJ, Nixon C, Dornan ES, Boner W, Donaldson MM, Morgan IM (2007) Aberrant expression of TopBP1 in breast cancer. Histopathology 50(4):418–424

    CAS  PubMed  Google Scholar 

  • Grieb BC, Chen X, Eischen CM (2014a) MTBP is overexpressed in triple-negative breast cancer and contributes to its growth and survival. Mol Cancer Res 12(9):1216–1224

    CAS  PubMed  Google Scholar 

  • Grieb BC, Gramling MW, Arrate MP, Chen X, Beauparlant SL, Haines DS, Xiao H, Eischen CM (2014b) Oncogenic protein MTBP interacts with MYC to promote tumorigenesis. Cancer Res 74(13):3591–3602

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674

    CAS  PubMed  Google Scholar 

  • Hashimoto Y, Puddu F, Costanzo V (2012) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat Struct Mol Biol 19(1):17–24

    PubMed Central  CAS  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hills SA, Diffley JF (2014) DNA replication and oncogene-induced replicative stress. Curr Biol 24(10):R435–R444

    CAS  PubMed  Google Scholar 

  • Ibarra A, Schwob E, Mendez J (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 105(26):8956–8961

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Im JS, Ki SH, Farina A, Jung DS, Hurwitz J, Lee JK (2009) Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc Natl Acad Sci U S A 106(37):15628–15632

    PubMed Central  CAS  PubMed  Google Scholar 

  • Itou H, Muramatsu S, Shirakihara Y, Araki H (2014) Crystal structure of the homology domain of the eukaryotic DNA replication proteins sld3/treslin. Structure 22(9):1341–1347

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Karppinen SM, Erkko H, Reini K, Pospiech H, Heikkinen K, Rapakko K, Syvaoja JE, Winqvist R (2006) Identification of a common polymorphism in the TopBP1 gene associated with hereditary susceptibility to breast and ovarian cancer. Eur J Cancer 42(15):2647–2652

    CAS  PubMed  Google Scholar 

  • Kawabata T, Luebben SW, Yamaguchi S, Ilves I, Matise I, Buske T, Botchan MR, Shima N (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol Cell 41(5):543–553

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kumagai A, Shevchenko A, Dunphy WG (2010) Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 140(3):349–359

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kumagai A, Shevchenko A, Dunphy WG (2011) Direct regulation of Treslin by cyclin-dependent kinase is essential for the onset of DNA replication. J Cell Biol 193(6):995–1007

    CAS  PubMed  Google Scholar 

  • Labib K (2010) How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells? Genes Dev 24(12):1208–1219

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lecona E, Fernandez-Capetillo O (2014) Replication stress and cancer: it takes two to tango. Exp Cell Res

  • Li Y, Araki H (2013) Loading and activation of DNA replicative helicases: the key step of initiation of DNA replication. Genes Cells 18(4):266–277

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y (2010) Rothmund-Thomson syndrome helicase, RECQ4: on the crossroad between DNA replication and repair. DNA Repair (Amst) 9(3):325–330

    CAS  Google Scholar 

  • Lobner-Olesen A, Skarstad K, Hansen FG, von Meyenburg K, Boye E (1989) The DNAA protein determines the initiation mass of Escherichia coli K-12. Cell 57(5):881–889

    CAS  PubMed  Google Scholar 

  • Loog M, Morgan DO (2005) Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434(7029):104–108

    CAS  PubMed  Google Scholar 

  • Makarova KS, Koonin EV (2013) Archaeology of eukaryotic DNA replication. Cold Spring Harb Perspect Med 3(10):a012963

    PubMed  Google Scholar 

  • Malumbres M, Barbacid M (2009) Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 9(3):153–166

    CAS  PubMed  Google Scholar 

  • Mann MB, Hodges CA, Barnes E, Vogel H, Hassold TJ, Luo G (2005) Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum Mol Genet 14(6):813–825

    CAS  PubMed  Google Scholar 

  • Mantiero D, Mackenzie A, Donaldson A, Zegerman P (2011) Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30(23):4805–4814

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Matsuno K, Kumano M, Kubota Y, Hashimoto Y, Takisawa H (2006) The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase alpha in the initiation of DNA replication. Mol Cell Biol 26(13):4843–4852

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mechali M (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11(10):728–738

    CAS  PubMed  Google Scholar 

  • Mimura S, Seki T, Tanaka S, Diffley JF (2004) Phosphorylation-dependent binding of mitotic cyclins to Cdc6 contributes to DNA replication control. Nature 431(7012):1118–1123

    CAS  PubMed  Google Scholar 

  • Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317(5846):1921–1926

    CAS  PubMed  Google Scholar 

  • Moses AM, Liku ME, Li JJ, Durbin R (2007) Regulatory evolution in proteins by turnover and lineage-specific changes of cyclin-dependent kinase consensus sites. Proc Natl Acad Sci U S A 104(45):17713–17718

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nakajima R, Masukata H (2002) SpSld3 is required for loading and maintenance of SpCdc45 on chromatin in DNA replication in fission yeast. Mol Biol Cell 13(5):1462–1472

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen VQ, Co C, Li JJ (2001) Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411(6841):1068–1073

    CAS  PubMed  Google Scholar 

  • Ohlenschlager O, Kuhnert A, Schneider A, Haumann S, Bellstedt P, Keller H, Saluz HP, Hortschansky P, Hanel F, Grosse F, Gorlach M, Pospiech H (2012) The N-terminus of the human RecQL4 helicase is a homeodomain-like DNA interaction motif. Nucleic Acids Res 40(17):8309–8324

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, Pines J (2011) Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 43(3):406–417

    CAS  PubMed  Google Scholar 

  • Patel PK, Kommajosyula N, Rosebrock A, Bensimon A, Leatherwood J, Bechhoefer J, Rhind N (2008) The Hsk1(Cdc7) replication kinase regulates origin efficiency. Mol Biol Cell 19(12):5550–5558

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pir P, Gutteridge A, Wu J, Rash B, Kell DB, Zhang N, Oliver SG (2012) The genetic control of growth rate: a systems biology study in yeast. BMC Syst Biol 6:4

    PubMed Central  PubMed  Google Scholar 

  • Randell JC, Bowers JL, Rodriguez HK, Bell SP (2006) Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol Cell 21(1):29–39

    CAS  PubMed  Google Scholar 

  • Remus D, Diffley JF (2009) Eukaryotic DNA replication control: lock and load, then fire. Curr Opin Cell Biol 21(6):771–777

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rhind N, Gilbert DM (2013) DNA replication timing. Cold Spring Harb Perspect Biol 5(8):a010132

    PubMed Central  PubMed  Google Scholar 

  • Sanchez-Pulido L, Diffley JF, Ponting CP (2010) Homology explains the functional similarities of Treslin/Ticrr and Sld3. Curr Biol 20(12):R509–R510

    CAS  PubMed  Google Scholar 

  • Sangrithi MN, Bernal JA, Madine M, Philpott A, Lee J, Dunphy WG, Venkitaraman AR (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121(6):887–898

    CAS  PubMed  Google Scholar 

  • Sansam CL, Cruz NM, Danielian PS, Amsterdam A, Lau ML, Hopkins N, Lees JA (2010) A vertebrate gene, ticrr, is an essential checkpoint and replication regulator. Genes Dev 24(2):183–194

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sheu YJ, Stillman B (2006) Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol Cell 24(1):101–113

    CAS  PubMed  Google Scholar 

  • Sheu YJ, Stillman B (2010) The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463(7277):113–117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Siddiqui K, On KF, Diffley JF (2013) Regulating DNA replication in eukarya. Cold Spring Harb Perspect Biol 5(9)

  • Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5(4):a012922

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka S, Araki H (2011) Multiple regulatory mechanisms to inhibit untimely initiation of DNA replication are important for stable genome maintenance. PLoS Genet 7(6):e1002136

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tanaka S, Komeda Y, Umemori T, Kubota Y, Takisawa H, Araki H (2013) Efficient initiation of DNA replication in eukaryotes requires Dpb11/TopBP1-GINS interaction. Mol Cell Biol 33(13):2614–2622

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thangavel S, Mendoza-Maldonado R, Tissino E, Sidorova JM, Yin J, Wang W, Monnat RJ Jr, Falaschi A, Vindigni A (2010) Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol Cell Biol 30(6):1382–1396

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, Morgan DO (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425(6960):859–864

    CAS  PubMed  Google Scholar 

  • Wardlaw CP, Carr AM, Oliver AW (2014) TopBP1: a BRCT-scaffold protein functioning in multiple cellular pathways. DNA Repair (Amst) 22:165–174

    CAS  Google Scholar 

  • Weinreich M, Stillman B (1999) Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway. EMBO J 18(19):5334–5346

    PubMed Central  CAS  PubMed  Google Scholar 

  • Weinreich M, Palacios DeBeer MA, Fox CA (2004) The activities of eukaryotic replication origins in chromatin. Biochim Biophys Acta 1677(1–3):142–157

    CAS  PubMed  Google Scholar 

  • Wong PG, Winter SL, Zaika E, Cao TV, Oguz U, Koomen JM, Hamlin JL, Alexandrow MG (2011) Cdc45 limits replicon usage from a low density of preRCs in mammalian cells. PLoS One 6(3):e17533

    PubMed Central  CAS  PubMed  Google Scholar 

  • Woodward AM, Gohler T, Luciani MG, Oehlmann M, Ge X, Gartner A, Jackson DA, Blow JJ (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 173(5):673–683

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wu PY, Nurse P (2009) Establishing the program of origin firing during S phase in fission yeast. Cell 136(5):852–864. doi:10.1016/j.cell.2009.01.017

  • Wu J, Capp C, Feng L, Hsieh TS (2008) Drosophila homologue of the Rothmund-Thomson syndrome gene: essential function in DNA replication during development. Dev Biol 323(1):130–142

    CAS  PubMed  Google Scholar 

  • Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y (2009a) MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J 28(19):3005–3014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xu Y, Lei Z, Huang H, Dui W, Liang X, Ma J, Jiao R (2009b) dRecQ4 is required for DNA synthesis and essential for cell proliferation in Drosophila. PLoS One 4(7):e6107

    PubMed Central  PubMed  Google Scholar 

  • Yabuuchi H, Yamada Y, Uchida T, Sunathvanichkul T, Nakagawa T, Masukata H (2006) Ordered assembly of Sld3, GINS and Cdc45 is distinctly regulated by DDK and CDK for activation of replication origins. EMBO J 25(19):4663–4674

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshida K, Poveda A, Pasero P (2013) Time to be versatile: regulation of the replication timing program in budding yeast. J Mol Biol 425(23):4696–4705

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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Acknowledgements

I apologise for any omissions due to space limitations and I am grateful to anonymous referees for their comments. I thank Vincent Gaggioli for critical reading of the manuscript and Max Telford and the Genome Institute at Washington University for access to the Priapulus caudatus genome sequence. PZ is supported Worldwide Cancer Research (AICR) 10-0908.

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Correspondence to Philip Zegerman.

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Zegerman, P. Evolutionary conservation of the CDK targets in eukaryotic DNA replication initiation. Chromosoma 124, 309–321 (2015). https://doi.org/10.1007/s00412-014-0500-y

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