Where and when to start: Regulating DNA replication origin activity in eukaryotic genomes

References

• Bell SP, Labib K. Chromosome duplication in Saccharomyces cerevisiae. Genetics. 2016; 203(3):1027–26. doi: 10.1534/genetics.115.186452
   PubMed Web of Science ®Google Scholar
• Costa A, Diffley JFX. The initiation of eukaryotic DNA replication. Annu Rev Biochem. 2022;91(1):107–131. doi: 10.1146/annurev-biochem-072321-110228
   PubMedGoogle Scholar
• Czajkowsky DM, Liu J, Hamlin JL, et al. DNA combing reveals intrinsic temporal disorder in the replication of yeast chromosome VI. J Mol Biol. 2008;375(1):12–19. doi: 10.1016/j.jmb.2007.10.046
   PubMed Web of Science ®Google Scholar
• Hawkins M, Retkute R, Muller CA, et al. High-resolution replication profiles define the stochastic nature of genome replication initiation and termination. Cell Rep. 2013;5(4):1132–1141. doi: 10.1016/j.celrep.2013.10.014
   PubMed Web of Science ®Google Scholar
• Saner N, Karschau J, Natsume T, et al. Stochastic association of neighboring replicons creates replication factories in budding yeast. J Cell Bio. 2013;202(7):1001–1012. doi: 10.1083/jcb.201306143
   PubMed Web of Science ®Google Scholar
• Fragkos M, Ganier O, Coulombe P, et al. DNA replication origin activation in space and time. Nat Rev Mol Cell Biol. 2015;16(6):360–374. doi: 10.1038/nrm4002
   PubMed Web of Science ®Google Scholar
• Ferguson BM, Brewer BJ, Reynolds AE, et al. A yeast origin of replication is activated late in S phase. Cell. 1991;65(3):507–515. doi: 10.1016/0092-8674(91)90468-e
   PubMed Web of Science ®Google Scholar
• Raghuraman MK, Winzeler EA, Collingwood D, et al. Replication dynamics of the yeast genome. Science. 2001;294(5540):115–121. doi: 10.1126/science.294.5540.115
   PubMed Web of Science ®Google Scholar
• Creager RL, Li Y, MacAlpine DM. SnapShot: origins of DNA replication. Cell. 2015;161(2):418–418 e411. doi: 10.1016/j.cell.2015.03.043
   PubMed Web of Science ®Google Scholar
• Leonard AC, Mechali M. DNA replication origins. Cold Spring Harb Perspect Biol. 2013; 5(10):a010116. doi: 10.1101/cshperspect.a010116
   PubMed Web of Science ®Google Scholar
• Azvolinsky A, Giresi PG, Lieb JD, et al. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol Cell. 2009;34(6):722–734. doi: 10.1016/j.molcel.2009.05.022
   PubMed Web of Science ®Google Scholar
• Barlow JH, Nussenzweig A. Replication initiation and genome instability: a crossroads for DNA and RNA synthesis. Cell Mol Life Sci. 2014; 71(23):4545–4559. doi: 10.1007/s00018-014-1721-1
   PubMed Web of Science ®Google Scholar
• Garcia-Muse T, Aguilera A. Transcription-replication conflicts: how they occur and how they are resolved. Nat Rev Mol Cell Biol. 2016;17(9):553–563. doi: 10.1038/nrm.2016.88
   PubMed Web of Science ®Google Scholar
• Knott SR, Viggiani CJ, Aparicio OM. To promote and protect: coordinating DNA replication and transcription for genome stability. Epigenetics. 2009;4(6):362–365. doi: 10.4161/epi.4.6.9712
   PubMed Web of Science ®Google Scholar
• Liu B, Alberts BM. Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex. Science. 1995;267(5201):1131–1137. doi: 10.1126/science.7855590
   PubMed Web of Science ®Google Scholar
• Sankar TS, Wastuwidyaningtyas BD, Dong Y, et al. The nature of mutations induced by replication-transcription collisions. Nature. 2016;535(7610):178–181. doi: 10.1038/nature18316
   PubMed Web of Science ®Google Scholar
• Kermi C, Lo Furno E, Maiorano D. Regulation of DNA replication in early embryonic cleavages. Genes (Basel). 2017;8(1): 8 1 42. doi:10.3390/genes8010042.
   PubMed Web of Science ®Google Scholar
• Rivera-Mulia JC, Buckley Q, Sasaki T, et al. Dynamic changes in replication timing and gene expression during lineage specification of human pluripotent stem cells. Genome Res. 2015;25(8):1091–1103. doi: 10.1101/gr.187989.114
   PubMed Web of Science ®Google Scholar
• Rivera-Mulia JC, Sasaki T, Trevilla-Garcia C, et al. Replication timing alterations in leukemia affect clinically relevant chromosome domains. Blood Adv. 2019;3(21):3201–3213. doi: 10.1182/bloodadvances.2019000641
   PubMed Web of Science ®Google Scholar
• Dimitrova DS, Gilbert DM. The spatial position and replication timing of chromosomal domains are both established in early G1 phase. Mol Cell. 1999; 4(6):983–993. doi: 10.1016/s1097-2765(00)80227-0
   PubMed Web of Science ®Google Scholar
• Raghuraman MK, Brewer BJ, Fangman WL. Cell cycle-dependent establishment of a late replication program. Science. 1997; 276(5313):806–809. doi: 10.1126/science.276.5313.806
   PubMed Web of Science ®Google Scholar
• Ferguson BM, Fangman WL. A position effect on the time of replication origin activation in yeast. Cell. 1992; 68(2):333–339. doi: 10.1016/0092-8674(92)90474-q
   PubMed Web of Science ®Google Scholar
• Vogelauer M, Rubbi L, Lucas I, et al. Histone acetylation regulates the time of replication origin firing. Mol Cell. 2002;10(5):1223–1233. doi: 10.1016/s1097-2765(02)00702-5
   PubMed Web of Science ®Google Scholar
• Yoshida K, Bacal J, Desmarais D, et al. The histone deacetylases sir2 and rpd3 act on ribosomal DNA to control the replication program in budding yeast. Mol Cell. 2014;54(4):691–697. doi: 10.1016/j.molcel.2014.04.032
   PubMed Web of Science ®Google Scholar
• Collart C, Allen GE, Bradshaw CR, et al. Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science. 2013;341(6148):893–896. doi: 10.1126/science.1241530
   PubMed Web of Science ®Google Scholar
• Mantiero D, Mackenzie A, Donaldson A, et al. Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. Embo J. 2011;30(23):4805–4814. doi: 10.1038/emboj.2011.404
   PubMed Web of Science ®Google Scholar
• Tanaka S, Nakato R, Katou Y, et al. Origin association of Sld3, Sld7, and Cdc45 proteins is a key step for determination of origin-firing timing. Curr Biol. 2011;21(24):2055–2063. doi: 10.1016/j.cub.2011.11.038
   PubMed Web of Science ®Google Scholar
• Ausiannikava D, Allers T. Diversity of DNA replication in the archaea. Genes (Basel). 2017;8(2): Genes 8 2 56. doi:10.3390/genes8020056.
   PubMed Web of Science ®Google Scholar
• Bleichert F, Botchan MR, Berger JM. Mechanisms for initiating cellular DNA replication. Science. 2017;355(6327). doi: 10.1126/science.aah6317
   PubMed Web of Science ®Google Scholar
• Ekundayo B, Bleichert F. Origins of DNA replication. PLoS Genet. 2019; 15(9):e1008320. doi: 10.1371/journal.pgen.1008320
   PubMed Web of Science ®Google Scholar
• Wolanski M, Donczew R, Zawilak-Pawlik A, et al. oriC-encoded instructions for the initiation of bacterial chromosome replication. Front Microbiol. 2014;5:735. doi: 10.3389/fmicb.2014.00735
   PubMed Web of Science ®Google Scholar
• Jacob F, Brenner S, Cuzin F. On the regulation of DNA replication in bacteria. Cold Spring Harb Symp Quant Biol. 1963;28:329–348. doi: 10.1101/SQB.1963.028.01.048
   Google Scholar
• Bell SP, Dutta A. DNA replication in eukaryotic cells. Annu Rev Biochem. 2002;71(1):333–374. doi: 10.1146/annurev.biochem.71.110601.135425
   PubMedGoogle Scholar
• Brewer BJ, Fangman WL. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell. 1987;51(3):463–471. doi: 10.1016/0092-8674(87)90642-8
   PubMed Web of Science ®Google Scholar
• Huberman JA, Spotila LD, Nawotka KA, et al. The in vivo replication origin of the yeast 2μm plasmid. Cell. 1987;51(3):473–481. doi: 10.1016/0092-8674(87)90643-X
   PubMed Web of Science ®Google Scholar
• Stinchcomb D, Struhl K, Davis R. Isolation and characterisation of a yeast chromosomal replicator. Nature. 1979;282(5734):39–43. doi: 10.1038/282039a0
   PubMed Web of Science ®Google Scholar
• Marahrens Y, Stillman B. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science. 1992;255(5046):817–823. doi: 10.1126/science.1536007
   PubMed Web of Science ®Google Scholar
• Rao H, Stillman B. The origin recognition complex interacts with a bipartite DNA binding site within yeast replicators. Proc Natl Acad Sci U S A. 1995; 92(6):2224–2228. doi: 10.1073/pnas.92.6.2224
   PubMed Web of Science ®Google Scholar
• Broach J, Li Y-Y, Feldman J, et al. Localization and sequence analysis of yeast origins of DNA replication, 47 Pt 2. Cold Spring Harbor Laboratory Press: Cold Spring Harbor Symposia on Quantitative Biology; 1983. p. 1165–73.
   Google Scholar
• Celniker S, Sweder K, Srienc F, et al. Deletion mutations affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae. Mol Cell Biol. 1984;4(11):2455–2466. doi: 10.1128/mcb.4.11.2455-2466.1984
   PubMed Web of Science ®Google Scholar
• Bell SP, Stillman B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature. 1992;357(6374):128–134. doi: 10.1038/357128a0
   PubMed Web of Science ®Google Scholar
• Li N, Lam WH, Zhai Y, et al. Structure of the origin recognition complex bound to DNA replication origin. Nature. 2018;559(7713):217–222. doi: 10.1038/s41586-018-0293-x
   PubMed Web of Science ®Google Scholar
• Rowley A, Cocker JH, Harwood J, et al. Initiation complex assembly at budding yeast replication origins begins with the recognition of a bipartite sequence by limiting amounts of the initiator, ORC. Embo J. 1995;14(11):2631–2641. doi: 10.1002/j.1460-2075.1995.tb07261.x
   PubMed Web of Science ®Google Scholar
• Van Houten JV, Newlon CS. Mutational analysis of the consensus sequence of a replication origin from yeast chromosome III. Mol Cell Biol. 1990;10(8):3917–3925. doi: 10.1128/MCB.10.8.3917
   PubMed Web of Science ®Google Scholar
• Theis JF, Newlon CS. The ARS309 chromosomal replicator of Saccharomyces cerevisiae depends on an exceptional ARS consensus sequence. Proc Natl Acad Sci U S A. 1997; 94(20):10786–10791. doi: 10.1073/pnas.94.20.10786
   PubMed Web of Science ®Google Scholar
• Breier AM, Chatterji S, Cozzarelli NR. Prediction of Saccharomyces cerevisiae replication origins. Genome Biol. 2004; 5(4):R22. doi: 10.1186/gb-2004-5-4-r22
   PubMed Web of Science ®Google Scholar
• Dao FY, Lv H, Wang F, et al. Identify origin of replication in Saccharomyces cerevisiae using two-step feature selection technique. Bioinformatics. 2019;35(12):2075–2083. doi: 10.1093/bioinformatics/bty943
   PubMed Web of Science ®Google Scholar
• Singh VK, Kumar V, Krishnamachari A. Prediction of replication sites in Saccharomyces cerevisiae genome using DNA segment properties: multi-view ensemble learning (MEL) approach. Biosystems. 2018;163:59–69. doi: 10.1016/j.biosystems.2017.12.005
   PubMed Web of Science ®Google Scholar
• Huang Y, Kowalski D. WEB-THERMODYN: sequence analysis software for profiling DNA helical stability. Nucleic Acids Res. 2003;31(13):3819–3821. doi: 10.1093/nar/gkg562
   PubMed Web of Science ®Google Scholar
• Natale DA, Umek RM, Kowalski D. Ease of DNA unwinding is a conserved property of yeast replication origins. Nucleic Acids Res. 1993; 21(3):555–560. doi: 10.1093/nar/21.3.555
   PubMed Web of Science ®Google Scholar
• Umek RM, Kowalski D. The DNA unwinding element in a yeast replication origin functions independently of easily unwound sequences present elsewhere on a plasmid. Nucleic Acids Res. 1990; 18(22):6601–6605. doi: 10.1093/nar/18.22.6601
   PubMed Web of Science ®Google Scholar
• Chang F, Theis JF, Miller J, et al. Analysis of chromosome III replicators reveals an unusual structure for the ARS318 silencer origin and a conserved WTW sequence within the origin recognition complex binding site. Mol Cell Biol. 2008;28(16):5071–5081. doi: 10.1128/MCB.00206-08
   PubMed Web of Science ®Google Scholar
• Eaton ML, Galani K, Kang S, et al. Conserved nucleosome positioning defines replication origins. Genes Dev. 2010;24(8):748–753. doi: 10.1101/gad.1913210
   PubMed Web of Science ®Google Scholar
• Xu W, Aparicio JG, Aparicio OM, et al. Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae. BMC Genomics. 2006;7(1):276. doi: 10.1186/1471-2164-7-276
   PubMedGoogle Scholar
• Yuan Z, Riera A, Bai L, et al. Structural basis of Mcm2-7 replicative helicase loading by ORC-Cdc6 and Cdt1. Nat Struct Mol Biol. 2017;24(3):316–324. doi: 10.1038/nsmb.3372
   PubMed Web of Science ®Google Scholar
• Lee CSK, Cheung MF, Li J, et al. Humanizing the yeast origin recognition complex. Nat Commun. 2021;12(1):33. doi: 10.1038/s41467-020-20277-y
   PubMed Web of Science ®Google Scholar
• Coster G, Diffley JF. Bidirectional eukaryotic DNA replication is established by quasi-symmetrical helicase loading. Science. 2017;357(6348):314–318. doi: 10.1126/science.aan0063
   PubMed Web of Science ®Google Scholar
• Lipford JR, Bell SP. Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol Cell. 2001; 7(1):21–30. doi: 10.1016/s1097-2765(01)00151-4
   PubMed Web of Science ®Google Scholar
• Palzkill TG, Newlon CS. A yeast replication origin consists of multiple copies of a small conserved sequence. Cell. 1988;53(3):441–450. doi: 10.1016/0092-8674(88)90164-X
   PubMed Web of Science ®Google Scholar
• Wilmes GM, Bell SP. The B2 element of the Saccharomyces cerevisiae ARS1 origin of replication requires specific sequences to facilitate pre-RC formation. Proc Nat Acad Sci. 2002;99(1):101–106. doi: 10.1073/pnas.012578499
   PubMed Web of Science ®Google Scholar
• Zou L, Stillman B. Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol Cell Biol. 2000;20(9):3086–3096. doi: 10.1128/MCB.20.9.3086-3096.2000
   PubMed Web of Science ®Google Scholar
• Diffley JF, Stillman B. Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer. Proc Natl Acad Sci U S A. 1988; 85(7):2120–2124. doi: 10.1073/pnas.85.7.2120
   PubMed Web of Science ®Google Scholar
• Ganapathi M, Palumbo MJ, Ansari SA, et al. Extensive role of the general regulatory factors, Abf1 and Rap1, in determining genome-wide chromatin structure in budding yeast. Nucleic Acids Res. 2011;39(6):2032–2044. doi: 10.1093/nar/gkq1161
   PubMed Web of Science ®Google Scholar
• Diffley JF, Cocker JH. Protein-DNA interactions at a yeast replication origin. Nature. 1992;357(6374):169–172. doi: 10.1038/357169a0
   PubMed Web of Science ®Google Scholar
• Chang VK, Donato JJ, Chan CS, et al. Mcm1 promotes replication initiation by binding specific elements at replication origins. Mol Cell Biol. 2004;24(14):6514–6524. doi: 10.1128/MCB.24.14.6514-6524.2004
   PubMed Web of Science ®Google Scholar
• Irlbacher H, Franke J, Manke T, et al. Control of replication initiation and heterochromatin formation in Saccharomyces cerevisiae by a regulator of meiotic gene expression. Genes Dev. 2005;19(15):1811–1822. doi: 10.1101/gad.334805
   PubMed Web of Science ®Google Scholar
• Walker SS, Francesconi SC, Eisenberg S. A DNA replication enhancer in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990; 87(12):4665–4669. doi: 10.1073/pnas.87.12.4665
   PubMed Web of Science ®Google Scholar
• Weiβ M, Chanou A, Schauer T, et al. Single-copy locus proteomics of early- and late-firing DNA replication origins identifies a role of Ask1/DASH complex in replication timing control. Cell Rep. 2023;42(2):112045. doi: 10.1016/j.celrep.2023.112045
   PubMed Web of Science ®Google Scholar
• Aladjem MI, Rodewald LW, Kolman JL, et al. Genetic dissection of a mammalian replicator in the human beta-globin locus. Science. 1998;281(5379):1005–1009. doi: 10.1126/science.281.5379.1005
   PubMed Web of Science ®Google Scholar
• Altman AL, Fanning E. Defined sequence modules and an architectural element cooperate to promote initiation at an ectopic mammalian chromosomal replication origin. Mol Cell Biol. 2004; 24(10):4138–4150. doi: 10.1128/MCB.24.10.4138-4150.2004
   PubMed Web of Science ®Google Scholar
• Liu G, Malott M, Leffak M. Multiple functional elements comprise a mammalian chromosomal replicator. Mol Cell Biol. 2003; 23(5):1832–1842. doi: 10.1128/MCB.23.5.1832-1842.2003
   PubMed Web of Science ®Google Scholar
• Malott M, Leffak M. Activity of the c-myc replicator at an ectopic chromosomal location. Mol Cell Biol. 1999; 19(8):5685–5695. doi: 10.1128/MCB.19.8.5685
   PubMed Web of Science ®Google Scholar
• Paixao S, Colaluca IN, Cubells M, et al. Modular structure of the human lamin B2 replicator. Mol Cell Biol. 2004;24(7):2958–2967. doi: 10.1128/MCB.24.7.2958-2967.2004
   PubMed Web of Science ®Google Scholar
• Wang L, Lin CM, Brooks S, et al. The human beta-globin replication initiation region consists of two modular independent replicators. Mol Cell Biol. 2004;24(8):3373–3386. doi: 10.1128/MCB.24.8.3373-3386.2004
   PubMed Web of Science ®Google Scholar
• Gilbert DM, Miyazawa H, DePamphilis ML. Site-specific initiation of DNA replication in Xenopus egg extract requires nuclear structure. Mol Cell Biol. 1995; 15(6):2942–2954. doi: 10.1128/MCB.15.6.2942
   PubMed Web of Science ®Google Scholar
• Besnard E, Babled A, Lapasset L, et al. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol. 2012;19(8):837–844. doi: 10.1038/nsmb.2339
   PubMed Web of Science ®Google Scholar
• Cayrou C, Ballester B, Peiffer I, et al. The chromatin environment shapes DNA replication origin organization and defines origin classes. Genome Res. 2015;25(12):1873–1885. doi: 10.1101/gr.192799.115
   PubMed Web of Science ®Google Scholar
• Cayrou C, Coulombe P, Vigneron A, et al. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 2011;21(9):1438–1449. doi: 10.1101/gr.121830.111
   PubMed Web of Science ®Google Scholar
• Dellino GI, Cittaro D, Piccioni R, et al. Genome-wide mapping of human DNA-replication origins: levels of transcription at ORC1 sites regulate origin selection and replication timing. Genome Res. 2013;23(1):1–11. doi: 10.1101/gr.142331.112
   PubMed Web of Science ®Google Scholar
• Eaton ML, Prinz JA, MacAlpine HK, et al. Chromatin signatures of the Drosophila replication program. Genome Res. 2011;21(2):164–174. doi: 10.1101/gr.116038.110
   PubMed Web of Science ®Google Scholar
• Hayashi M, Katou Y, Itoh T, et al. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. Embo J. 2007;26(5):1327–1339. doi: 10.1038/sj.emboj.7601585
   PubMed Web of Science ®Google Scholar
• Lubelsky Y, Sasaki T, Kuipers MA, et al. Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res. 2011;39(8):3141–3155. doi: 10.1093/nar/gkq1276
   PubMed Web of Science ®Google Scholar
• MacAlpine HK, Gordan R, Powell SK, et al. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 2010;20(2):201–211. doi: 10.1101/gr.097873.109
   PubMed Web of Science ®Google Scholar
• Martin MM, Ryan M, Kim R, et al. Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res. 2011;21(11):1822–1832. doi: 10.1101/gr.124644.111
   PubMed Web of Science ®Google Scholar
• Miotto B, Ji Z, Struhl K. Selectivity of ORC binding sites and the relation to replication timing, fragile sites, and deletions in cancers. Proc Natl Acad Sci U S A. 2016; 113(33):E4810–4819. doi: 10.1073/pnas.1609060113
   PubMed Web of Science ®Google Scholar
• Pourkarimi E, Bellush JM, Whitehouse I. Spatiotemporal coupling and decoupling of gene transcription with DNA replication origins during embryogenesis in C. elegans. Elife. 2016;5. doi: 10.7554/eLife.21728
   PubMed Web of Science ®Google Scholar
• Rodriguez-Martinez M, Pinzon N, Ghommidh C, et al. The gastrula transition reorganizes replication-origin selection in Caenorhabditis elegans. Nat Struct Mol Biol. 2017;24(3):290–299. doi: 10.1038/nsmb.3363
   PubMed Web of Science ®Google Scholar
• Akerman I, Kasaai B, Bazarova A, et al. A predictable conserved DNA base composition signature defines human core DNA replication origins. Nat Commun. 2020;11(1):4826. doi: 10.1038/s41467-020-18527-0
   PubMed Web of Science ®Google Scholar
• Comoglio F, Schlumpf T, Schmid V, et al. High-resolution profiling of Drosophila replication start sites reveals a DNA shape and chromatin signature of metazoan origins. Cell Rep. 2015;11(5):821–834. doi: 10.1016/j.celrep.2015.03.070
   PubMed Web of Science ®Google Scholar
• Guilbaud G, Murat P, Wilkes HS, et al. Determination of human DNA replication origin position and efficiency reveals principles of initiation zone organisation. Nucleic Acids Res. 2022;50(13):7436–7450. doi: 10.1093/nar/gkac555
   PubMed Web of Science ®Google Scholar
• Edenberg HJ, Huberman JA. Eukaryotic chromosome replication. Annu Rev Genet. 1975;9(1):245–284. doi: 10.1146/annurev.ge.09.120175.001333
   PubMed Web of Science ®Google Scholar
• Landt SG, Marinov GK, Kundaje A, et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 2012;22(9):1813–1831. doi: 10.1101/gr.136184.111
   PubMed Web of Science ®Google Scholar
• Wyrick JJ, Aparicio JG, Chen T, et al. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science. 2001;294(5550):2357–2360. doi: 10.1126/science.1066101
   PubMed Web of Science ®Google Scholar
• Chesnokov IN. Multiple functions of the origin recognition complex. Int Rev Cytol. 2007;256:69–109. doi: 10.1016/S0074-7696(07)56003-1
   PubMedGoogle Scholar
• Hemerly AS, Prasanth SG, Siddiqui K, et al. Orc1 controls centriole and centrosome copy number in human cells. Science. 2009;323(5915):789–793. doi: 10.1126/science.1166745
   PubMed Web of Science ®Google Scholar
• Kirstein N, Buschle A, Wu X, et al. Human ORC/MCM density is low in active genes and correlates with replication time but does not delimit initiation zones. Elife. 2021;10. doi: 10.7554/eLife.62161
   PubMed Web of Science ®Google Scholar
• Smith DJ, Whitehouse I. Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature. 2012;483(7390):434–438. doi: 10.1038/nature10895
   PubMed Web of Science ®Google Scholar
• Cadoret JC, Meisch F, Hassan-Zadeh V, et al. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U S A. 2008;105(41):15837–15842. doi: 10.1073/pnas.0805208105
   PubMed Web of Science ®Google Scholar
• Sequeira-Mendes J, Díaz-Uriarte R, Apedaile A, et al. Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet. 2009;5(4):e1000446. doi: 10.1371/journal.pgen.1000446
   PubMed Web of Science ®Google Scholar
• Mesner LD, Crawford EL, Hamlin JL. Isolating apparently pure libraries of replication origins from complex genomes. Molecular Cell. 2006;21(5):719–726. doi: 10.1016/j.molcel.2006.01.015
   PubMed Web of Science ®Google Scholar
• Muller CA, Boemo MA, Spingardi P, et al. Capturing the dynamics of genome replication on individual ultra-long nanopore sequence reads. Nat Methods. 2019;16(5):429–436. doi: 10.1038/s41592-019-0394-y
   PubMed Web of Science ®Google Scholar
• Lam ET, Hastie A, Lin C, et al. Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nature Biotechnol. 2012;30(8):771–776. doi: 10.1038/nbt.2303
   PubMed Web of Science ®Google Scholar
• Panning MM, Gilbert DM. Spatio‐temporal organization of DNA replication in murine embryonic stem, primary, and immortalized cells. J Cell Biochem. 2005;95(1):74–82. doi: 10.1002/jcb.20395
   PubMed Web of Science ®Google Scholar
• Wilson KA, Elefanty AG, Stanley EG, et al. Spatio-temporal re-organization of replication foci accompanies replication domain consolidation during human pluripotent stem cell lineage specification. Cell Cycle. 2016;15(18):2464–2475. doi: 10.1080/15384101.2016.1203492
   PubMed Web of Science ®Google Scholar
• Wang W, Klein KN, Proesmans K, et al. Genome-wide mapping of human DNA replication by optical replication mapping supports a stochastic model of eukaryotic replication. Molecular Cell. 2021;81(14):2975–2988. doi: 10.1016/j.molcel.2021.05.024 e2976.
   PubMed Web of Science ®Google Scholar
• 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(9):3053–3065. doi: 10.1128/MCB.22.9.3053-3065.2002
   PubMed Web of Science ®Google Scholar
• 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(2):134–146. doi: 10.1101/gad.822101
   PubMed Web of Science ®Google Scholar
• Zhang H, Tower J. Sequence requirements for function of the Drosophila chorion gene locus ACE3 replicator and ori-beta origin elements. Development. 2004;131(9):2089–2099. doi: 10.1242/dev.01064
   PubMed Web of Science ®Google Scholar
• Demczuk A, Gauthier MG, Veras I, et al. Regulation of DNA replication within the immunoglobulin heavy-chain locus during B cell commitment. PLoS Biol. 2012;10(7):e1001360. doi: 10.1371/journal.pbio.1001360
   PubMed Web of Science ®Google Scholar
• Prioleau MN, MacAlpine DM. DNA replication origins-where do we begin? Genes Dev. 2016;30(15):1683–1697. doi: 10.1101/gad.285114.116
   PubMed Web of Science ®Google Scholar
• Cayrou C, Coulombe P, Puy A, et al. New insights into replication origin characteristics in metazoans. Cell Cycle. 2012;11(4):658–667. doi: 10.4161/cc.11.4.19097
   PubMed Web of Science ®Google Scholar
• Langley AR, Graf S, Smith JC, et al. Genome-wide identification and characterisation of human DNA replication origins by initiation site sequencing (ini-seq). Nucleic Acids Res. 2016;44(21):10230–10247. doi: 10.1093/nar/gkw760
   PubMed Web of Science ®Google Scholar
• Valton AL, Hassan-Zadeh V, Lema I, et al. G4 motifs affect origin positioning and efficiency in two vertebrate replicators. Embo J. 2014;33(7):732–746. doi: 10.1002/embj.201387506
   PubMed Web of Science ®Google Scholar
• Halder K, Halder R, Chowdhury S. Genome-wide analysis predicts DNA structural motifs as nucleosome exclusion signals. Mol Biosyst. 2009; 5(12):1703–1712. doi: 10.1039/b905132e
   PubMedGoogle Scholar
• Halder R, Halder K, Sharma P, et al. Guanine quadruplex DNA structure restricts methylation of CpG dinucleotides genome-wide. Mol Biosyst. 2010;6(12):2439–2447. doi: 10.1039/c0mb00009d
   PubMedGoogle Scholar
• Valton AL, Prioleau MN. G-Quadruplexes in DNA replication: a problem or a necessity? Trends Genet. 2016; 32(11):697–706. doi: 10.1016/j.tig.2016.09.004
   PubMed Web of Science ®Google Scholar
• Tubbs A, Sridharan S, van Wietmarschen N, et al. Dual roles of poly(dA:dT) tracts in replication initiation and fork collapse. Cell. 2018;174(5):1127–1142 e1119. doi: 10.1016/j.cell.2018.07.011
   PubMed Web of Science ®Google Scholar
• De Carli F, Menezes N, Berrabah W, et al. High-throughput optical mapping of replicating DNA. Small Methods. 2018;2(9):1800146. doi: 10.1002/smtd.201800146
   Web of Science ®Google Scholar
• Vashee S, Cvetic C, Lu W, et al. Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 2003;17(15):1894–1908. doi: 10.1101/gad.1084203
   PubMed Web of Science ®Google Scholar
• Remus D, Beall EL, Botchan MR. DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. Embo J. 2004;23(4):897–907. doi: 10.1038/sj.emboj.7600077
   PubMed Web of Science ®Google Scholar
• Hoshina S, Yura K, Teranishi H, et al. Human origin recognition complex binds preferentially to G-quadruplex-preferable RNA and single-stranded DNA. J Biol Chem. 2013;288(42):30161–30171. doi: 10.1074/jbc.M113.492504
   PubMed Web of Science ®Google Scholar
• Prorok P, Artufel M, Aze A, et al. Involvement of G-quadruplex regions in mammalian replication origin activity. Nat Commun. 2019;10(1):3274. doi: 10.1038/s41467-019-11104-0
   PubMedGoogle Scholar
• Cadoret J-C, Meisch F, Hassan-Zadeh V, et al. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Nat Acad Sci. 2008;105(41):15837–15842. doi: 10.1073/pnas.0805208105
   PubMed Web of Science ®Google Scholar
• Harvey KJ, Newport J. CpG methylation of DNA restricts prereplication complex assembly in Xenopus egg extracts. Mol Cell Biol. 2003; 23(19):6769–6779. doi: 10.1128/Mcb.23.19.6769-6779.2003
   PubMed Web of Science ®Google Scholar
• Gros J, Kumar C, Lynch G, et al. Post-licensing specification of eukaryotic replication origins by facilitated Mcm2-7 sliding along DNA. Molecular Cell. 2015;60(5):797–807. doi: 10.1016/j.molcel.2015.10.022
   PubMed Web of Science ®Google Scholar
• Macheret M, Halazonetis TD. Intragenic origins due to short G1 phases underlie oncogene-induced DNA replication stress. Nature. 2018; 555(7694):112–116. doi: 10.1038/nature25507
   PubMed Web of Science ®Google Scholar
• Powell SK, MacAlpine HK, Prinz JA, et al. Dynamic loading and redistribution of the Mcm2-7 helicase complex through the cell cycle. Embo J. 2015;34(4):531–543. doi: 10.15252/embj.201488307
   PubMed Web of Science ®Google Scholar
• Scherr MJ, Abd Wahab S, Remus D, et al. Mobile origin-licensing factors confer resistance to conflicts with RNA polymerase. Cell Rep. 2022;38(12):110531. doi: 10.1016/j.celrep.2022.110531
   PubMed Web of Science ®Google Scholar
• Albert I, Mavrich TN, Tomsho LP, et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature. 2007;446(7135):572–576. doi: 10.1038/nature05632
   PubMed Web of Science ®Google Scholar
• Lee W, Tillo D, Bray N, et al. A high-resolution atlas of nucleosome occupancy in yeast. Nature Genet. 2007;39(10):1235–1244. doi: 10.1038/ng2117
   PubMed Web of Science ®Google Scholar
• Mavrich TN, Jiang C, Ioshikhes IP, et al. Nucleosome organization in the Drosophila genome. Nature. 2008;453(7193):358–362. doi: 10.1038/nature06929
   PubMed Web of Science ®Google Scholar
• Yuan G-C, Liu Y-J, Dion MF, et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science. 2005;309(5734):626–630. doi: 10.1126/science.1112178
   PubMed Web of Science ®Google Scholar
• Field Y, Kaplan N, Fondufe-Mittendorf Y, et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol. 2008;4(11):e1000216. doi: 10.1371/journal.pcbi.1000216
   PubMed Web of Science ®Google Scholar
• Berbenetz NM, Nislow C, Brown GW, et al. Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet. 2010;6(9):e1001092. doi: 10.1371/journal.pgen.1001092
   PubMed Web of Science ®Google Scholar
• Anderson JD, Widom J. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol Cell Biol. 2001; 21(11):3830–3839. doi: 10.1128/MCB.21.11.3830-3839.2001
   PubMed Web of Science ®Google Scholar
• Barnes T, Korber P. The active mechanism of nucleosome depletion by poly(dA:dT) tracts in vivo. Int J Mol Sci. 2021;22(15):8233. doi: 10.3390/ijms22158233
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Liu CL, Humphrey EL, et al. Global nucleosome occupancy in yeast. Genome Biol. 2004; 5(9):R62. doi: 10.1186/gb-2004-5-9-r62
   PubMed Web of Science ®Google Scholar
• Chacin E, Reusswig KU, Furtmeier J, et al. Establishment and function of chromatin organization at replication origins. Nature. 2023;616(7958):836–842. doi: 10.1038/s41586-023-05926-8
   PubMed Web of Science ®Google Scholar
• Li S, Wasserman MR, Yurieva O, et al. Nucleosome-directed replication origin licensing independent of a consensus DNA sequence. Nat Commun. 2022;13(1):4947. doi: 10.1038/s41467-022-32657-7
   PubMed Web of Science ®Google Scholar
• Azmi IF, Watanabe S, Maloney MF, et al. Nucleosomes influence multiple steps during replication initiation. Elife. 2017;6:e22512. doi: 10.7554/eLife.22512
   PubMed Web of Science ®Google Scholar
• Liu J, Zimmer K, Rusch DB, et al. DNA sequence templates adjacent nucleosome and ORC sites at gene amplification origins in Drosophila. Nucleic Acids Res. 2015;43(18):8746–8761. doi: 10.1093/nar/gkv766
   PubMed Web of Science ®Google Scholar
• Miotto B, Struhl K. HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol Cell. 2010; 37(1):57–66. doi: 10.1016/j.molcel.2009.12.012
   PubMed Web of Science ®Google Scholar
• Venditti P, Costanzo G, Negri R, et al. ABFI contributes to the chromatin organization of Saccharomyces cerevisiae ARS1 B-domain. Biochim Biophys Acta. 1994; 1219(3):677–689. doi: 10.1016/0167-4781(94)90227-5
   PubMedGoogle Scholar
• Soriano I, Morafraile EC, Vázquez E, et al. Different nucleosomal architectures at early and late replicating origins in Saccharomyces cerevisiae. BMC Genomics. 2014;15(1):1–15. doi: 10.1186/1471-2164-15-791
   PubMedGoogle Scholar
• Rodriguez J, Lee L, Lynch B, et al. Nucleosome occupancy as a novel chromatin parameter for replication origin functions. Genome Res. 2017;27(2):269–277. doi: 10.1101/gr.209940.116
   PubMed Web of Science ®Google Scholar
• Yin S, Deng W, Hu L, et al. The impact of nucleosome positioning on the organization of replication origins in eukaryotes. Biochem Biophys Res Commun. 2009;385(3):363–368. doi: 10.1016/j.bbrc.2009.05.072
   PubMed Web of Science ®Google Scholar
• Lombraña R, Almeida R, Revuelta I, et al. High‐resolution analysis of DNA synthesis start sites and nucleosome architecture at efficient mammalian replication origins. Embo J. 2013;32(19):2631–2644. doi: 10.1038/emboj.2013.195
   PubMed Web of Science ®Google Scholar
• Millan-Zambrano G, Burton A, Bannister AJ, et al. Histone post-translational modifications - cause and consequence of genome function. Nat Rev Genet. 2022;23(9):563–580. doi: 10.1038/s41576-022-00468-7
   PubMed Web of Science ®Google Scholar
• Unnikrishnan A, Gafken PR, Tsukiyama T. Dynamic changes in histone acetylation regulate origins of DNA replication. Nat Struct Mol Biol. 2010; 17(4):430–437. doi: 10.1038/nsmb.1780
   PubMed Web of Science ®Google Scholar
• Hoggard T, Muller CA, Nieduszynski CA, et al. Sir2 mitigates an intrinsic imbalance in origin licensing efficiency between early- and late-replicating euchromatin. Proc Natl Acad Sci U S A. 2020;117(25):14314–14321. doi: 10.1073/pnas.2004664117
   PubMed Web of Science ®Google Scholar
• Hoggard TA, Chang F, Perry KR, et al. Yeast heterochromatin regulators Sir2 and Sir3 act directly at euchromatic DNA replication origins. PLoS Genet. 2018;14(5):e1007418. doi: 10.1371/journal.pgen.1007418
   PubMed Web of Science ®Google Scholar
• Santos-Rosa H, Millan-Zambrano G, Han N, et al. Methylation of histone H3 at lysine 37 by Set1 and Set2 prevents spurious DNA replication. Mol Cell. 2021;81(13):2793–2807 e2798. doi: 10.1016/j.molcel.2021.04.021
   PubMed Web of Science ®Google Scholar
• Brewer BJ, Fangman WL. A replication fork barrier at the 3’ end of yeast ribosomal RNA genes. Cell. 1988;55(4):637–643. doi: 10.1016/0092-8674(88)90222-x
   PubMed Web of Science ®Google Scholar
• Pasero P, Bensimon A, Schwob E. Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev. 2002; 16(19):2479–2484. doi: 10.1101/gad.232902
   PubMed Web of Science ®Google Scholar
• Foss EJ, Lao U, Dalrymple E, et al. SIR2 suppresses replication gaps and genome instability by balancing replication between repetitive and unique sequences. Proc Natl Acad Sci U S A. 2017;114(3):552–557. doi: 10.1073/pnas.1614781114
   PubMed Web of Science ®Google Scholar
• Rine J, Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987; 116(1):9–22. doi: 10.1093/genetics/116.1.9
   PubMed Web of Science ®Google Scholar
• Aparicio OM, Billington BL, Gottschling DE. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell. 1991; 66(6):1279–1287. doi: 10.1016/0092-8674(91)90049-5
   PubMed Web of Science ®Google Scholar
• Stevenson JB, Gottschling DE. Telomeric chromatin modulates replication timing near chromosome ends. Genes Dev. 1999; 13(2):146–151. doi: 10.1101/gad.13.2.146
   PubMed Web of Science ®Google Scholar
• Zappulla DC, Sternglanz R, Leatherwood J. Control of replication timing by a transcriptional silencer. Curr Biol. 2002; 12(11):869–875. doi: 10.1016/s0960-9822(02)00871-0
   PubMed Web of Science ®Google Scholar
• Aparicio JG, Viggiani CJ, Gibson DG, et al. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol Cell Biol. 2004;24(11):4769–4780. doi: 10.1128/MCB.24.11.4769-4780.2004
   PubMed Web of Science ®Google Scholar
• Knott SR, Viggiani CJ, Tavare S, et al. Genome-wide replication profiles indicate an expansive role for Rpd3L in regulating replication initiation timing or efficiency, and reveal genomic loci of Rpd3 function in Saccharomyces cerevisiae. Genes Dev. 2009;23(9):1077–1090. doi: 10.1101/gad.1784309
   PubMed Web of Science ®Google Scholar
• Rizzardi LF, Dorn ES, Strahl BD, et al. DNA replication origin function is promoted by H3K4 di-methylation in Saccharomyces cerevisiae. Genetics. 2012;192(2):371–384. doi: 10.1534/genetics.112.142349
   PubMed Web of Science ®Google Scholar
• Pryde F, Jain D, Kerr A, et al. H3 k36 methylation helps determine the timing of cdc45 association with replication origins. PLoS One. 2009;4(6):e5882. doi: 10.1371/journal.pone.0005882
   PubMed Web of Science ®Google Scholar
• Feng YQ, Desprat R, Fu H, et al. DNA methylation supports intrinsic epigenetic memory in mammalian cells. PLoS Genet. 2006;2(4):e65. doi: 10.1371/journal.pgen.0020065
   PubMed Web of Science ®Google Scholar
• Mechali M, Yoshida K, Coulombe P, et al. Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr Opin Genet Dev. 2013;23(2):124–131. doi: 10.1016/j.gde.2013.02.010
   PubMed Web of Science ®Google Scholar
• Rhind N, Gilbert DM. DNA replication timing. Cold Spring Harb Perspect Biol. 2013; 5(8):a010132. doi: 10.1101/cshperspect.a010132
   PubMed Web of Science ®Google Scholar
• Smith OK, Aladjem MI. Chromatin structure and replication origins: determinants of chromosome replication and nuclear organization. J Mol Biol. 2014; 426(20):3330–3341. doi: 10.1016/j.jmb.2014.05.027
   PubMed Web of Science ®Google Scholar
• Smith OK, Kim R, Fu H, et al. Distinct epigenetic features of differentiation-regulated replication origins. Epigenet Chromatin. 2016;9:18. doi: 10.1186/s13072-016-0067-31
   PubMed Web of Science ®Google Scholar
• Marks AB, Fu H, Aladjem MI. Regulation of replication origins. DNA Replication. 2017;1042:43–59.
   Google Scholar
• Tardat M, Brustel J, Kirsh O, et al. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Biol. 2010;12(11):1086–1093. doi: 10.1038/ncb2113
   PubMed Web of Science ®Google Scholar
• Kuo AJ, Song J, Cheung P, et al. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature. 2012;484(7392):115–119. doi: 10.1038/nature10956
   PubMed Web of Science ®Google Scholar
• Long H, Zhang L, Lv M, et al. H2A.Z facilitates licensing and activation of early replication origins. Nature. 2020;577(7791):576–581. doi: 10.1038/s41586-019-1877-9
   PubMed Web of Science ®Google Scholar
• Kitsberg D, Selig S, Keshet I, et al. Replication structure of the human beta-globin gene domain. Nature. 1993;366(6455):588–590. doi: 10.1038/366588a0
   PubMed Web of Science ®Google Scholar
• Goren A, Tabib A, Hecht M, et al. DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. Genes Dev. 2008;22(10):1319–1324. doi: 10.1101/gad.468308
   PubMed Web of Science ®Google Scholar
• Lalonde ME, Avvakumov N, Glass KC, et al. Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev. 2013;27(18):2009–2024. doi: 10.1101/gad.223396.113
   PubMed Web of Science ®Google Scholar
• Feng Y, Vlassis A, Roques C, et al. BRPF3-HBO1 regulates replication origin activation and histone H3K14 acetylation. Embo J. 2016;35(2):176–192. doi: 10.15252/embj.201591293
   PubMed Web of Science ®Google Scholar
• Rondinelli B, Schwerer H, Antonini E, et al. H3k4me3 demethylation by the histone demethylase KDM5C/JARID1C promotes DNA replication origin firing. Nucleic Acids Res. 2015;43(5):2560–2574. doi: 10.1093/nar/gkv090
   PubMed Web of Science ®Google Scholar
• Wu R, Wang Z, Zhang H, et al. H3k9me3 demethylase Kdm4d facilitates the formation of pre-initiative complex and regulates DNA replication. Nucleic Acids Res. 2017;45(1):169–180. doi: 10.1093/nar/gkw848
   PubMed Web of Science ®Google Scholar
• Fu HQ, Maunakea AK, Martin MM, et al. Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet. 2013;9(6). ARTNe1003542.
   Web of Science ®Google Scholar
• Koren A, Handsaker RE, Kamitaki N, et al. Genetic variation in human DNA replication timing. Cell. 2014;159(5):1015–1026. doi: 10.1016/j.cell.2014.10.025
   PubMed Web of Science ®Google Scholar
• Ding Q, Edwards MM, Wang N, et al. The genetic architecture of DNA replication timing in human pluripotent stem cells. Nat Commun. 2021;12(1):6746. doi: 10.1038/s41467-021-27115-9
   PubMed Web of Science ®Google Scholar
• Das SP, Borrman T, Liu VW, et al. Replication timing is regulated by the number of MCMs loaded at origins. Genome Res. 2015;25(12):1886–1892. doi: 10.1101/gr.195305.115
   PubMed Web of Science ®Google Scholar
• Dukaj L, Rhind N, Copenhaver GP. The capacity of origins to load MCM establishes replication timing patterns. PLoS Genet. 2021;17(3):e1009467. doi: 10.1371/journal.pgen.1009467
   PubMed Web of Science ®Google Scholar
• Belsky JA, MacAlpine HK, Lubelsky Y, et al. Genome-wide chromatin footprinting reveals changes in replication origin architecture induced by pre-RC assembly. Genes Dev. 2015;29(2):212–224. doi: 10.1101/gad.247924.114
   PubMed Web of Science ®Google Scholar
• Foss EJ, Sripathy S, Gatbonton-Schwager T, et al. Chromosomal Mcm2-7 distribution and the genome replication program in species from yeast to humans. PLoS Genet. 2021;17(9):e1009714. doi: 10.1371/journal.pgen.1009714
   PubMed Web of Science ®Google Scholar
• Cremona CA, Sarangi P, Yang Y, et al. Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. Mol Cell. 2012;45(3):422–432. doi: 10.1016/j.molcel.2011.11.028
   PubMed Web of Science ®Google Scholar
• Golebiowski F, Matic I, Tatham MH, et al. System-wide changes to SUMO modifications in response to heat shock. Sci Signal. 2009;2(72):ra24. doi: 10.1126/scisignal.2000282
   PubMed Web of Science ®Google Scholar
• Regan-Mochrie G, Hoggard T, Bhagwat N, et al. Yeast ORC sumoylation status fine-tunes origin licensing. Genes Dev. 2022;36(13–14):807–821. doi: 10.1101/gad.349610.122
   PubMed Web of Science ®Google Scholar
• Santos MM, Johnson MC, Fiedler L, et al. Global early replication disrupts gene expression and chromatin conformation in a single cell cycle. Genome Biol. 2022; 23(1):217. doi: 10.1186/s13059-022-02788-7
   PubMed Web of Science ®Google Scholar
• Knott SR, Peace JM, Ostrow AZ, et al. Forkhead transcription factors establish origin timing and long-range clustering in S. cerevisiae. Cell. 2012;148(1–2):99–111. doi: 10.1016/j.cell.2011.12.012
   PubMed Web of Science ®Google Scholar
• Ostrow AZ, Nellimoottil T, Knott SR, et al. Fkh1 and Fkh2 bind multiple chromosomal elements in the S. cerevisiae genome with distinct specificities and cell cycle dynamics. PLoS One. 2014;9(2):e87647. doi: 10.1371/journal.pone.0087647
   PubMed Web of Science ®Google Scholar
• Peace JM, Villwock SK, Zeytounian JL, et al. Quantitative BrdU immunoprecipitation method demonstrates that Fkh1 and Fkh2 are rate-limiting activators of replication origins that reprogram replication timing in G1 phase. Genome Res. 2016;26(3):365–375. doi: 10.1101/gr.196857.115
   PubMed Web of Science ®Google Scholar
• Fang D, Lengronne A, Shi D, et al. Dbf4 recruitment by forkhead transcription factors defines an upstream rate-limiting step in determining origin firing timing. Genes Dev. 2017;31(23–24):2405–2415. doi: 10.1101/gad.306571.117
   PubMed Web of Science ®Google Scholar
• Zhang H, Petrie MV, He Y, et al. Dynamic relocalization of replication origins by Fkh1 requires execution of DDK function and Cdc45 loading at origins. Elife. 2019;8. doi: 10.7554/eLife.45512
   Web of Science ®Google Scholar
• He Y, Petrie MV, Zhang H, et al. Rpd3 regulates single-copy origins independently of the rDNA array by opposing Fkh1-mediated origin stimulation. Proc Natl Acad Sci U S A. 2022;119(40):e2212134119. doi: 10.1073/pnas.2212134119
   PubMed Web of Science ®Google Scholar
• Natsume T, Muller CA, Katou Y, et al. Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. Mol Cell. 2013;50(5):661–674. doi: 10.1016/j.molcel.2013.05.011
   PubMed Web of Science ®Google Scholar
• Lian HY, Robertson ED, Hiraga S, et al. The effect of Ku on telomere replication time is mediated by telomere length but is independent of histone tail acetylation. Mol Biol Cell. 2011;22(10):1753–1765. doi: 10.1091/mbc.E10-06-0549
   PubMed Web of Science ®Google Scholar
• Peace JM, Ter-Zakarian A, Aparicio OM, et al. Rif1 regulates initiation timing of late replication origins throughout the S. cerevisiae genome. PLoS One. 2014;9(5):e98501. doi: 10.1371/journal.pone.0098501
   PubMed Web of Science ®Google Scholar
• Dave A, Cooley C, Garg M, et al. Protein phosphatase 1 recruitment by Rif1 regulates DNA replication origin firing by counteracting DDK activity. Cell Rep. 2014;7(1):53–61. doi: 10.1016/j.celrep.2014.02.019
   PubMed Web of Science ®Google Scholar
• Hiraga S, Alvino GM, Chang F, et al. Rif1 controls DNA replication by directing protein phosphatase 1 to reverse Cdc7-mediated phosphorylation of the MCM complex. Genes Dev. 2014;28(4):372–383. doi: 10.1101/gad.231258.113
   PubMed Web of Science ®Google Scholar
• Mattarocci S, Shyian M, Lemmens L, et al. Rif1 controls DNA replication timing in yeast through the PP1 phosphatase Glc7. Cell Rep. 2014;7(1):62–69. doi: 10.1016/j.celrep.2014.03.010
   PubMed Web of Science ®Google Scholar
• Hafner L, Lezaja A, Zhang X, et al. Rif1 binding and control of chromosome-internal DNA replication origins is limited by telomere sequestration. Cell Rep. 2018;23(4):983–992. doi: 10.1016/j.celrep.2018.03.113
   PubMed Web of Science ®Google Scholar
• Shyian M, Mattarocci S, Albert B, et al. Budding yeast Rif1 controls genome integrity by inhibiting rDNA replication. PLoS Genet. 2016;12(11):e1006414. doi: 10.1371/journal.pgen.1006414
   PubMed Web of Science ®Google Scholar
• Alavi S, Ghadiri H, Dabirmanesh B, et al. G-quadruplex binding protein Rif1, a key regulator of replication timing. J Biochem. 2021;169(1):1–14. doi: 10.1093/jb/mvaa128
   PubMed Web of Science ®Google Scholar
• Kobayashi S, Fukatsu R, Kanoh Y, et al. Both a unique motif at the C terminus and an N-terminal HEAT repeat contribute to G-quadruplex binding and origin regulation by the Rif1 protein. Mol Cell Biol. 2019;39(4). doi: 10.1128/MCB.00364-18
   Web of Science ®Google Scholar
• Moriyama K, Yoshizawa-Sugata N, Masai H. Oligomer formation and G-quadruplex binding by purified murine Rif1 protein, a key organizer of higher-order chromatin architecture. J Biol Chem. 2018; 293(10):3607–3624. doi: 10.1074/jbc.RA117.000446
   PubMed Web of Science ®Google Scholar
• Cornacchia D, Dileep V, Quivy JP, et al. Mouse Rif1 is a key regulator of the replication‐timing programme in mammalian cells. Embo J. 2012;31(18):3678–3690. doi: 10.1038/emboj.2012.214
   PubMed Web of Science ®Google Scholar
• Hayano M, Kanoh Y, Matsumoto S, et al. Rif1 is a global regulator of timing of replication origin firing in fission yeast. Genes Dev. 2012;26(2):137–150. doi: 10.1101/gad.178491.111
   PubMed Web of Science ®Google Scholar
• Yamazaki S, Ishii A, Kanoh Y, et al. Rif1 regulates the replication timing domains on the human genome. Embo J. 2012;31(18):3667–3677. doi: 10.1038/emboj.2012.180
   PubMed Web of Science ®Google Scholar
• Hiraga SI, Ly T, Garzon J, et al. Human RIF1 and protein phosphatase 1 stimulate DNA replication origin licensing but suppress origin activation. EMBO Rep. 2017;18(3):403–419. doi: 10.15252/embr.201641983
   PubMed Web of Science ®Google Scholar
• Zhang Y, Huang L, Fu H, et al. A replicator-specific binding protein essential for site-specific initiation of DNA replication in mammalian cells. Nat Commun. 2016;7(1):11748. doi: 10.1038/ncomms11748
   PubMedGoogle Scholar
• Jang SM, Zhang Y, Utani K, et al. The replication initiation determinant protein (RepID) modulates replication by recruiting CUL4 to chromatin. Nat Commun. 2018;9(1):2782. doi: 10.1038/s41467-018-05177-6
   PubMedGoogle Scholar
• Taddei A, Hediger F, Neumann FR, et al. The function of nuclear architecture: a genetic approach. Ann Rev Genet. 2004;38(1):305–345. doi: 10.1146/annurev.genet.37.110801.142705
   PubMedGoogle Scholar
• Hiraga S, Robertson ED, Donaldson AD. The Ctf18 RFC-like complex positions yeast telomeres but does not specify their replication time. Embo J. 2006; 25(7):1505–1514. doi: 10.1038/sj.emboj.7601038
   PubMed Web of Science ®Google Scholar
• Ebrahimi H, Robertson ED, Taddei A, et al. Early initiation of a replication origin tethered at the nuclear periphery. J Cell Sci. 2010;123(Pt 7):1015–1019. doi: 10.1242/jcs.060392
   PubMed Web of Science ®Google Scholar
• Pasero P, Braguglia D, Gasser SM. ORC-dependent and origin-specific initiation of DNA replication at defined foci in isolated yeast nuclei. Genes Dev. 1997; 11(12):1504–1518. doi: 10.1101/gad.11.12.1504
   PubMed Web of Science ®Google Scholar
• Kitamura E, Blow JJ, Tanaka TU. Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell. 2006; 125(7):1297–1308. doi: 10.1016/j.cell.2006.04.041
   PubMed Web of Science ®Google Scholar
• Duan Z, Andronescu M, Schutz K, et al. A three-dimensional model of the yeast genome. Nature. 2010;465(7296):363–367. doi: 10.1038/nature08973
   PubMed Web of Science ®Google Scholar
• Ostrow AZ, Kalhor R, Gan Y, et al. Conserved forkhead dimerization motif controls DNA replication timing and spatial organization of chromosomes in S. cerevisiae. Proc Natl Acad Sci U S A. 2017;114(12):E2411–E2419. doi: 10.1073/pnas.1612422114
   PubMed Web of Science ®Google Scholar
• Natsume T, Tanaka TU. Spatial regulation and organization of DNA replication within the nucleus. Chromosome Res. 2010; 18(1):7–17. doi: 10.1007/s10577-009-9088-0
   PubMed Web of Science ®Google Scholar
• Nakamura H, Morita T, Sato C. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp Cell Res. 1986; 165(2):291–297. doi: 10.1016/0014-4827(86)90583-5
   PubMed Web of Science ®Google Scholar
• Hozak P, Cook PR. Replication factories. Trends Cell Biol. 1994; 4(2):48–52. doi: 10.1016/0962-8924(94)90009-4
   PubMedGoogle Scholar
• Hozak P, Hassan AB, Jackson DA, et al. Visualization of replication factories attached to a nucleoskeleton. Cell. 1993;73(2):361–373. doi: 10.1016/0092-8674(93)90235-i
   PubMed Web of Science ®Google Scholar
• Berezney R, Dubey DD, Huberman JA. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma. 2000; 108(8):471–484. doi: 10.1007/s004120050399
   PubMed Web of Science ®Google Scholar
• Xiang W, Roberti MJ, Heriche JK, et al. Correlative live and super-resolution imaging reveals the dynamic structure of replication domains. J Cell Bio. 2018;217(6):1973–1984. doi: 10.1083/jcb.201709074
   PubMed Web of Science ®Google Scholar
• Chagin VO, Casas-Delucchi CS, Reinhart M, et al. 4D visualization of replication foci in mammalian cells corresponding to individual replicons. Nat Commun. 2016;7(1):11231. doi: 10.1038/ncomms11231
   PubMed Web of Science ®Google Scholar
• Woodfine K, Fiegler H, Beare DM, et al. Replication timing of the human genome. Hum Mol Genet. 2004;13(2):191–202. doi: 10.1093/hmg/ddh016
   PubMed Web of Science ®Google Scholar
• Hiratani I, Ryba T, Itoh M, et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008;6(10):e245. doi: 10.1371/journal.pbio.0060245
   PubMed Web of Science ®Google Scholar
• Hansen RS, Thomas S, Sandstrom R, et al. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc Nat Acad Sci. 2010;107(1):139–144. doi: 10.1073/pnas.0912402107
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay R, Lajugie J, Fourel N, et al. Allele-specific genome-wide profiling in human primary erythroblasts reveal replication program organization. PLoS Genet. 2014;10(5):e1004319. doi: 10.1371/journal.pgen.1004319
   PubMed Web of Science ®Google Scholar
• Rivera-Mulia JC, Gilbert DM. Replicating large genomes: divide and conquer. Mol Cell. 2016; 62(5):756–765. doi: 10.1016/j.molcel.2016.05.007
   PubMed Web of Science ®Google Scholar
• Li F, Chen J, Izumi M, et al. The replication timing program of the Chinese hamster β-globin locus is established coincident with its repositioning near peripheral heterochromatin in early G1 phase. J Cell Bio. 2001;154(2):283–292. doi: 10.1083/jcb.200104043
   PubMed Web of Science ®Google Scholar
• Zhou J, Ermakova OV, Riblet R, et al. Replication and subnuclear location dynamics of the immunoglobulin heavy-chain locus in B-lineage cells. Mol Cell Biol. 2002;22(13):4876–4889. doi: 10.1128/MCB.22.13.4876-4889.2002
   PubMed Web of Science ®Google Scholar
• Lieberman-Aiden E, Van Berkum NL, Williams L, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326(5950):289–293. doi: 10.1126/science.1181369
   PubMed Web of Science ®Google Scholar
• Ryba T, Hiratani I, Lu J, et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 2010;20(6):761–770. doi: 10.1101/gr.099655.109
   PubMed Web of Science ®Google Scholar
• Dixon JR, Selvaraj S, Yue F, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485(7398):376–380. doi: 10.1038/nature11082
   PubMed Web of Science ®Google Scholar
• Pope BD, Ryba T, Dileep V, et al. Topologically associating domains are stable units of replication-timing regulation. Nature. 2014;515(7527):402–405. doi: 10.1038/nature13986
   PubMed Web of Science ®Google Scholar
• Narendra V, Rocha PP, An D, et al. CTCF establishes discrete functional chromatin domains at the hox clusters during differentiation. Science. 2015;347(6225):1017–1021. doi: 10.1126/science.1262088
   PubMed Web of Science ®Google Scholar
• Koren A, Polak P, Nemesh J, et al. Differential relationship of DNA replication timing to different forms of human mutation and variation. Am J Hum Genet. 2012;91(6):1033–1040. doi: 10.1016/j.ajhg.2012.10.018
   PubMed Web of Science ®Google Scholar
• Stamatoyannopoulos JA, Adzhubei I, Thurman RE, et al. Human mutation rate associated with DNA replication timing. Nature Genet. 2009;41(4):393–395. doi: 10.1038/ng.363
   PubMed Web of Science ®Google Scholar
• Peric-Hupkes D, Meuleman W, Pagie L, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Molecular Cell. 2010;38(4):603–613. doi: 10.1016/j.molcel.2010.03.016
   PubMed Web of Science ®Google Scholar
• Solovei I, Thanisch K, Feodorova Y. How to rule the nucleus: divide et impera. Curr Opin Cell Biol. 2016;40:47–59. doi: 10.1016/j.ceb.2016.02.014
   PubMed Web of Science ®Google Scholar
• Sima J, Chakraborty A, Dileep V, et al. Identifying cis elements for spatiotemporal control of mammalian DNA replication. Cell. 2019;176(4):816–830 e818. doi: 10.1016/j.cell.2018.11.036
   PubMed Web of Science ®Google Scholar
• Gillespie PJ, Li A, Blow JJ. Reconstitution of licensed replication origins on Xenopus sperm nuclei using purified proteins. BMC Biochem. 2001;2(1):15. doi: 10.1186/1471-2091-2-15
   PubMedGoogle Scholar
• Yeeles JT, Deegan TD, Janska A, et al. Regulated eukaryotic DNA replication origin firing with purified proteins. Nature. 2015;519(7544):431–435. doi: 10.1038/nature14285
   PubMed Web of Science ®Google Scholar
• Devbhandari S, Jiang J, Kumar C, et al. Chromatin constrains the initiation and elongation of DNA replication. Mol Cell. 2017;65(1):131–141. doi: 10.1016/j.molcel.2016.10.035
   PubMed Web of Science ®Google Scholar
• Kurat CF, Yeeles JTP, Patel H, et al. Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol Cell. 2017;65(1):117–130. doi: 10.1016/j.molcel.2016.11.016
   PubMed Web of Science ®Google Scholar
• Yeeles JTP, Janska A, Early A, et al. How the eukaryotic replisome achieves rapid and efficient DNA replication. Mol Cell. 2017;65(1):105–116. doi: 10.1016/j.molcel.2016.11.017
   PubMed Web of Science ®Google Scholar