Origins of DNA replication

Autoři: Babatunde Ekundayo aff001;  Franziska Bleichert aff001
Působiště autorů: Quantitative Biology, Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland aff001
Vyšlo v časopise: Origins of DNA replication. PLoS Genet 15(9): e1008320. doi:10.1371/journal.pgen.1008320
Kategorie: Topic Page


In all kingdoms of life, DNA is used to encode hereditary information. Propagation of the genetic material between generations requires timely and accurate duplication of DNA by semiconservative replication prior to cell division to ensure each daughter cell receives the full complement of chromosomes. DNA synthesis of daughter strands starts at discrete sites, termed replication origins, and proceeds in a bidirectional manner until all genomic DNA is replicated. Despite the fundamental nature of these events, organisms have evolved surprisingly divergent strategies that control replication onset. Here, we discuss commonalities and differences in replication origin organization and recognition in the three domains of life.

Klíčová slova:

Biology and life sciences – Genetics – DNA – DNA replication – DNA structure – Biochemistry – Nucleic acids – Enzymology – Enzymes – Helicases – Proteins – DNA-binding proteins – Organisms – Eukaryota – Fungi – Yeast – Saccharomyces – Saccharomyces cerevisiae – Cell biology – Cell processes – Cell cycle and cell division – Molecular biology – Macromolecular structure analysis – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Yeast and fungal models


1. Mendel G (1865) Versuche ueber Pflanzenhybriden Verhandlungen des naturforschenden Vereines in Bruenn, Bd IV Abhandlungen:3–47

2. Avery OT, Macleod CM & McCarty M (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type iii J. Exp. Med. 79:137–58 [doi: 10.1084/jem.79.2.137 19871359]

3. Watson JD & Crick FH (1953) The structure of DNA Cold Spring Harb. Symp. Quant. Biol. 18:123–31 [doi: 10.1101/sqb.1953.018.01.020 13168976]

4. Meselson M & Stahl FW (1958) The replication of DNA in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 44:671–82 [doi: 10.1073/pnas.44.7.671 16590258]

5. Meselson M & Stahl FW (1958) The replication of DNA Cold Spring Harb. Symp. Quant. Biol. 23:9–12 [doi: 10.1101/sqb.1958.023.01.004 13635537]

6. IR Lehman, MJ Bessman, ES Simms & Kornberg A (1958) Enzymatic synthesis of deoxyribonucleic acid. I. Preparation of substrates and partial purification of an enzyme from Escherichia coli J. Biol. Chem. 233:163–70 [13563462]

7. O'Donnell M, Langston L & Stillman B (2013) Principles and concepts of DNA replication in bacteria, archaea, and eukarya Cold Spring Harb Perspect Biol 5:a010108 [doi: 10.1101/cshperspect.a010108 23818497]

8. Barlow JH & Nussenzweig A (2014) Replication initiation and genome instability: a crossroads for DNA and RNA synthesis Cell. Mol. Life Sci. 71:4545–59 [doi: 10.1007/s00018-014-1721-1 25238783]

9. Abbas T, Keaton MA & Dutta A (2013) Genomic instability in cancer Cold Spring Harb Perspect Biol 5:a012914 [doi: 10.1101/cshperspect.a012914 23335075]

10. Siddiqui K, On KF & Diffley JF (2013) Regulating DNA replication in eukarya Cold Spring Harb Perspect Biol 5:a012930 [doi: 10.1101/cshperspect.a012930 23838438]

11. Sclafani RA & Holzen TM (2007) Cell cycle regulation of DNA replication Annu. Rev. Genet. 41:237–80 [doi: 10.1146/annurev.genet.41.110306.130308 17630848]

12. García-Muse T & Aguilera A (2016) Transcription-replication conflicts: how they occur and how they are resolved Nat. Rev. Mol. Cell Biol. 17:553–63 [doi: 10.1038/nrm.2016.88 27435505]

13. Leonard AC & Méchali M (2013) DNA replication origins Cold Spring Harb Perspect Biol 5:a010116 [doi: 10.1101/cshperspect.a010116 23838439]

14. Creager RL, Li Y & MacAlpine DM (2015) SnapShot: Origins of DNA replication Cell 161:418–418.e1 [doi: 10.1016/j.cell.2015.03.043 25860614]

15. Knott SR, Viggiani CJ & Aparicio OM (2009) To promote and protect: coordinating DNA replication and transcription for genome stability Epigenetics 4:362–5 [doi: 10.4161/epi.4.6.9712 19736523]

16. Deshpande AM & Newlon CS (1996) DNA replication fork pause sites dependent on transcription Science 272:1030–3 [doi: 10.1126/science.272.5264.1030 8638128]

17. Sankar TS, Wastuwidyaningtyas BD, Dong Y, Lewis SA & Wang JD (2016) The nature of mutations induced by replication–transcription collisions Nature 535:178–81 [doi: 10.1038/nature18316 27362223]

18. Liu B & Alberts BM (1995) Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex Science 267:1131–7 [doi: 10.1126/science.7855590 7855590]

19. Azvolinsky A, Giresi PG, Lieb JD & Zakian VA (2009) Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae Mol. Cell 34:722–34 [doi: 10.1016/j.molcel.2009.05.022 19560424]

20. Jacob F, Brenner S & Cuzin F (1963) On the regulation of DNA replication in bacteria Cold Spring Harbor Symp Quant Biol 28:329–48

21. Novick RP (1987) Plasmid incompatibility Microbiol. Rev. 51:381–95 [3325793]

22. Skarstad K & Katayama T (2013) Regulating DNA replication in bacteria Cold Spring Harb Perspect Biol 5:a012922 [doi: 10.1101/cshperspect.a012922 23471435]

23. Marks AB, Fu H & Aladjem MI (2017) Regulation of Replication Origins Adv. Exp. Med. Biol. 1042:43–59 [doi: 10.1007/978-981-10-6955-0_2 29357052]

24. Parker MW, Botchan MR & Berger JM (2017) Mechanisms and regulation of DNA replication initiation in eukaryotes Crit. Rev. Biochem. Mol. Biol. 52:107–44 [doi: 10.1080/10409238.2016.1274717 28094588]

25. Gilbert DM (2004) In search of the holy replicator Nat. Rev. Mol. Cell Biol. 5:848–55 [doi: 10.1038/nrm1495 15459665]

26. Aladjem MI & Fanning E (2004) The replicon revisited: an old model learns new tricks in metazoan chromosomes EMBO Rep. 5:686–91 [doi: 10.1038/sj.embor.7400185 15229645]

27. Remus D, Beall EL & Botchan MR (2004) DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding EMBO J. 23:897–907 [doi: 10.1038/sj.emboj.7600077 14765124]

28. 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. 17:1894–908 [doi: 10.1101/gad.1084203 12897055]

29. Shen Z, Sathyan KM, Geng Y, Zheng R, Chakraborty A, Freeman B, Wang F, Prasanth KV & Prasanth SG (2010) A WD-repeat protein stabilizes ORC binding to chromatin Mol. Cell 40:99–111 [doi: 10.1016/j.molcel.2010.09.021 20932478]

30. Dorn ES & Cook JG (2011) Nucleosomes in the neighborhood: new roles for chromatin modifications in replication origin control Epigenetics 6:552–9 [doi: 10.4161/epi.6.5.15082 21364325]

31. Aladjem MI & Redon CE (2017) Order from clutter: selective interactions at mammalian replication origins Nat. Rev. Genet.18:101–16 [doi: 10.1038/nrg.2016.141 27867195]

32. Fragkos M, Ganier O, Coulombe P & Méchali M (2015) DNA replication origin activation in space and time Nat. Rev. Mol. Cell Biol.16:360–74 [doi: 10.1038/nrm4002 25999062]

33. Prioleau MN & MacAlpine DM (2016) DNA replication origins-where do we begin? Genes Dev. 30:1683–97 [doi: 10.1101/gad.285114.116 27542827]

34. Cayrou C, Coulombe P, Puy A, Rialle S, Kaplan N, Segal E & Méchali M (2012) New insights into replication origin characteristics in metazoans Cell Cycle 11:658–67 [doi: 10.4161/cc.11.4.19097 22373526]

35. Lombraña R, Almeida R, Álvarez A & Gómez M (2015) R-loops and initiation of DNA replication in human cells: a missing link? Front Genet 6:158 [doi: 10.3389/fgene.2015.00158 25972891]

36. Jang SM, Zhang Y, Utani K, Fu H, Redon CE, Marks AB, Smith OK, Redmond CJ, Baris AM, Tulchinsky DA & Aladjem MI (2018) The replication initiation determinant protein (RepID) modulates replication by recruiting CUL4 to chromatin Nat Commun 9:2782 [doi: 10.1038/s41467-018-05177-6 30018425]

37. Zakian VA & Scott JF (1982) Construction, replication, and chromatin structure of TRP1 RI circle, a multiple-copy synthetic plasmid derived from Saccharomyces cerevisiae chromosomal DNA Mol. Cell. Biol. 2:221–32 [doi: 10.1128/mcb.2.3.221 6287231]

38. Rhodes N, Company M & Errede B (1990) A yeast-Escherichia coli shuttle vector containing the M13 origin of replication Plasmid 23:159–62 [2194231]

39. Paululat A & Heinisch JJ (2012) New yeast/E. coli/Drosophila triple shuttle vectors for efficient generation of Drosophila P element transformation constructs Gene 511:300–5 [doi: 10.1016/j.gene.2012.09.058 23026211]

40. Ryan VT, Grimwade JE, Camara JE, Crooke E & Leonard AC (2004) Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA Mol. Microbiol. 51:1347–59 [doi: 10.1046/j.1365-2958.2003.03906.x 14982629]

41. Mackiewicz P, Zakrzewska-Czerwinska J, Zawilak A, Dudek MR & Cebrat S (2004) Where does bacterial replication start? Rules for predicting the oriC region Nucleic Acids Res. 32:3781–91 [doi: 10.1093/nar/gkh699 15258248]

42. Luo H & Gao F (2019) DoriC 10.0: an updated database of replication origins in prokaryotic genomes including chromosomes and plasmids Nucleic Acids Res. 47:D74–D77 [doi: 10.1093/nar/gky1014 30364951]

43. Fuller RS, Funnell BE & Kornberg A (1984) The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites Cell 38:889–900 [doi: 10.1016/0092-8674(84)90284-8 6091903]

44. Fuller RS & Kornberg A (1983) Purified dnaA protein in initiation of replication at the Escherichia coli chromosomal origin of replication Proc. Natl. Acad. Sci. U.S.A. 80:5817–21 [doi: 10.1073/pnas.80.19.5817 6310593]

45. Jakimowicz D, Majka J, Messer W, Speck C, Fernandez M, Martin MC, Sanchez J, Schauwecker F, Keller U, Schrempf H & Zakrzewska-Czerwińska J (1998) Structural elements of the Streptomyces oriC region and their interactions with the DnaA protein Microbiology 144:1281–90 [doi: 10.1099/00221287-144-5-1281 9611803]

46. Tsodikov OV & Biswas T (2011) Structural and thermodynamic signatures of DNA recognition by Mycobacterium tuberculosis DnaA J. Mol. Biol. 410:461–76 [doi: 10.1016/j.jmb.2011.05.007 21620858]

47. Costa A, Hood IV & Berger JM (2013) Mechanisms for initiating cellular DNA replication Annu. Rev. Biochem. 82:25–54 [doi: 10.1146/annurev-biochem-052610-094414 23746253]

48. Wolański M, Donczew R, Zawilak-Pawlik A & Zakrzewska-Czerwińska J (2014) oriC-encoded instructions for the initiation of bacterial chromosome replication Front Microbiol 5:735 [doi: 10.3389/fmicb.2014.00735 25610430]

49. Messer W, Blaesing F, Majka J, Nardmann J, Schaper S, Schmidt A, Seitz H, Speck C, Tüngler D, Wegrzyn G, Weigel C, Welzeck M & Zakrzewska-Czerwinska J (1999) Functional domains of DnaA proteins Biochimie 81:819–25 [doi: 10.1016/s0300-9084(99)00215-1 10572294]

50. Sutton MD & Kaguni JM (1997) The Escherichia coli dnaA gene: four functional domains J. Mol. Biol. 274:546–61 [doi: 10.1006/jmbi.1997.1425 9417934]

51. Speck C & Messer W (2001) Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA EMBO J. 20:1469–76 [doi: 10.1093/emboj/20.6.1469 11250912]

52. Fujikawa N, Kurumizaka H, Nureki O, Terada T, Shirouzu M, Katayama T & Yokoyama S (2003) Structural basis of replication origin recognition by the DnaA protein Nucleic Acids Res. 31:2077–86 [doi: 10.1093/nar/gkg309 12682358]

53. Duderstadt KE, Chuang K & Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening Nature478:209–13 [doi: 10.1038/nature10455 21964332]

54. Erzberger JP, Pirruccello MM & Berger JM (2002) The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation EMBO J. 21:4763–73 [doi: 10.1093/emboj/cdf496 12234917]

55. Iyer LM, Leipe DD, Koonin EV & Aravind L (2004) Evolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol.146:11–31 [doi: 10.1016/j.jsb.2003.10.010 15037234]

56. Sutton MD & Kaguni JM (1997) Threonine 435 of Escherichia coli DnaA protein confers sequence-specific DNA binding activity J. Biol. Chem. 272:23017–24 [doi: 10.1074/jbc.272.37.23017 9287298]

57. Bramhill D & Kornberg A (1988) A model for initiation at origins of DNA replication Cell 54:915–8 [doi: 10.1016/0092-8674(88)90102-x 2843291]

58. Rozgaja TA, Grimwade JE, Iqbal M, Czerwonka C, Vora M & Leonard AC (2011) Two oppositely oriented arrays of low-affinity recognition sites in oriC guide progressive binding of DnaA during Escherichia coli pre-RC assembly Mol. Microbiol. 82:475–88 [doi: 10.1111/j.1365-2958.2011.07827.x 21895796]

59. Zawilak-Pawlik A, Kois A, Majka J, Jakimowicz D, Smulczyk-Krawczyszyn A, Messer W & Zakrzewska-Czerwińska J (2005) Architecture of bacterial replication initiation complexes: orisomes from four unrelated bacteria Biochem. J. 389:471–81 [doi: 10.1042/BJ20050143 15790315]

60. Grimwade JE, Rozgaja TA, Gupta R, Dyson K, Rao P & Leonard AC (2018) Origin recognition is the predominant role for DnaA-ATP in initiation of chromosome replication Nucleic Acids Res. 46:6140–51 [doi: 10.1093/nar/gky457 29800247]

61. Sakiyama Y, Kasho K, Noguchi Y, Kawakami H & Katayama T (2017) Regulatory dynamics in the ternary DnaA complex for initiation of chromosomal replication in Escherichia coli Nucleic Acids Res.45:12354–73 [doi: 10.1093/nar/gkx914 29040689]

62. Matsui M, Oka A, Takanami M, Yasuda S & Hirota Y (1985) Sites of dnaA protein-binding in the replication origin of the Escherichia coli K-12 chromosome J. Mol. Biol. 184:529–33 [doi: 10.1016/0022-2836(85)90299-2 2995681]

63. Margulies C & Kaguni JM (1996) Ordered and sequential binding of DnaA protein to oriC, the chromosomal origin of Escherichia coli J. Biol. Chem. 271:17035–40 [doi: 10.1074/jbc.271.29.17035 8663334]

64. Schaper S & Messer W (1995) Interaction of the initiator protein DnaA of Escherichia coli with its DNA target J. Biol. Chem. 270:17622–6 [doi: 10.1074/jbc.270.29.17622 7615570]

65. Weigel C, Schmidt A, Rückert B, Lurz R & Messer W (1997) DnaA protein binding to individual DnaA boxes in the Escherichia coli replication origin, oriC EMBO J. 16:6574–83 [doi: 10.1093/emboj/16.21.6574 9351837]

66. Samitt CE, Hansen FG, Miller JF & Schaechter M (1989) In vivo studies of DnaA binding to the origin of replication of Escherichia coli EMBO J. 8:989–93 [2542031]

67. McGarry KC, Ryan VT, Grimwade JE & Leonard AC (2004) Two discriminatory binding sites in the Escherichia coli replication origin are required for DNA strand opening by initiator DnaA-ATP Proc. Natl. Acad. Sci. U.S.A. 101:2811–6 [doi: 10.1073/pnas.0400340101 14978287]

68. Kawakami H, Keyamura K & Katayama T (2005) Formation of an ATP-DnaA-specific initiation complex requires DnaA Arginine 285, a conserved motif in the AAA+ protein family J. Biol. Chem. 280:27420–30 [doi: 10.1074/jbc.M502764200 15901724]

69. Speck C, Weigel C & Messer W (1999) ATP- and ADP-dnaA protein, a molecular switch in gene regulation EMBO J. 18:6169–76 [doi: 10.1093/emboj/18.21.6169 10545126]

70. Miller DT, Grimwade JE, Betteridge T, Rozgaja T, Torgue JJ & Leonard AC (2009) Bacterial origin recognition complexes direct assembly of higher-order DnaA oligomeric structures Proc. Natl. Acad. Sci. U.S.A.106:18479–84 [doi: 10.1073/pnas.0909472106 19833870]

71. Erzberger JP, Mott ML & Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling Nat. Struct. Mol. Biol. 13:676–83 [doi: 10.1038/nsmb1115 16829961]

72. Zorman S, Seitz H, Sclavi B & Strick TR (2012) Topological characterization of the DnaA-oriC complex using single-molecule nanomanipuation Nucleic Acids Res. 40:7375–83 [doi: 10.1093/nar/gks371 22581769]

73. Richardson TT, Harran O & Murray H (2016) The bacterial DnaA-trio replication origin element specifies single-stranded DNA initiator binding Nature 534:412–6 [doi: 10.1038/nature17962 27281207]

74. Duderstadt KE, Mott ML, Crisona NJ, Chuang K, Yang H & Berger JM (2010) Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator J. Biol. Chem. 285:28229–39 [doi: 10.1074/jbc.M110.147975 20595381]

75. Ozaki S & Katayama T (2012) Highly organized DnaA-oriC complexes recruit the single-stranded DNA for replication initiation Nucleic Acids Res. 40:1648–65 [doi: 10.1093/nar/gkr832 22053082]

76. Myllykallio H, Lopez P, López-García P, Heilig R, Saurin W, Zivanovic Y, Philippe H & Forterre P (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon Science288:2212–5 [doi: 10.1126/science.288.5474.2212 10864870]

77. Norais C, Hawkins M, Hartman AL, Eisen JA, Myllykallio H & Allers T (2007) Genetic and physical mapping of DNA replication origins in Haloferax volcanii PLoS Genet. 3:e77 [doi: 10.1371/journal.pgen.0030077 17511521]

78. Hawkins M, Malla S, Blythe MJ, Nieduszynski CA & Allers T (2013) Accelerated growth in the absence of DNA replication origins Nature503 544–7 [doi: 10.1038/nature12650 24185008]

79. Wu Z, Liu J, Yang H, Liu H & Xiang H (2014) Multiple replication origins with diverse control mechanisms in Haloarcula hispanica Nucleic Acids Res. 42:2282–94 [doi: 10.1093/nar/gkt1214 24271389]

80. Pelve EA, Martens-Habbena W, Stahl DA & Bernander R (2013) Mapping of active replication origins in vivo in thaum- and euryarchaeal replicons Mol. Microbiol. 90:538–50 [doi: 10.1111/mmi.12382 23991938]

81. Pelve EA, Lindås AC, Knöppel A, Mira A & Bernander R (2012) Four chromosome replication origins in the archaeon Pyrobaculum calidifontis Mol. Microbiol. 85:986–95 [doi: 10.1111/j.1365-2958.2012.08155.x 22812406]

82. Robinson NP, Dionne I, Lundgren M, Marsh VL, Bernander R & Bell SD (2004) Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus Cell 116:25–38 [doi: 10.1016/s0092-8674(03)01034-1 14718164]

83. Lundgren M, Andersson A, Chen L, Nilsson P & Bernander R (2004) Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination Proc. Natl. Acad. Sci. U.S.A. 101:7046–51 [doi: 10.1073/pnas.0400656101 15107501]

84. Bell SD (2017) Initiation of DNA Replication in the Archaea Adv. Exp. Med. Biol. 1042:99–115 [doi: 10.1007/978-981-10-6955-0_5 29357055]

85. Ausiannikava D & Allers T (2017) Diversity of DNA Replication in the Archaea Genes (Basel) 8:E56 [doi: 10.3390/genes8020056 28146124]

86. Wu Z, Liu J, Yang H & Xiang H (2014) DNA replication origins in archaea Front Microbiol 5:179 [doi: 10.3389/fmicb.2014.00179 24808892]

87. Matsunaga F, Forterre P, Ishino Y & Myllykallio H (2001) In vivo interactions of archaeal Cdc6/Orc1 and minichromosome maintenance proteins with the replication origin Proc. Natl. Acad. Sci. U.S.A. 98:11152–7 [doi: 10.1073/pnas.191387498 11562464]

88. Wu Z, Liu H, Liu J, Liu X & Xiang H (2012) Diversity and evolution of multiple orc/cdc6-adjacent replication origins in haloarchaea BMC Genomics 13:478 [doi: 10.1186/1471-2164-13-478 22978470]

89. Bell SD (2012) Archaeal orc1/cdc6 proteins Subcell. Biochem. 62:59–69 [doi: 10.1007/978-94-007-4572-8_4 22918580]

90. Samson RY, Xu Y, Gadelha C, Stone TA, Faqiri JN, Li D, Qin N, Pu F, Liang YX, She Q & Bell SD (2013) Specificity and function of archaeal DNA replication initiator proteins Cell Rep 3:485–96 [doi: 10.1016/j.celrep.2013.01.002 23375370]

91. Grainge I, Gaudier M, Schuwirth BS, Westcott SL, Sandall J, Atanassova N & Wigley DB (2006) Biochemical analysis of a DNA replication origin in the archaeon Aeropyrum pernix J. Mol. Biol.363:355–69 [doi: 10.1016/j.jmb.2006.07.076 16978641]

92. Robinson NP & Bell SD (2007) Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes Proc. Natl. Acad. Sci. U.S.A. 104:5806–11 [doi: 10.1073/pnas.0700206104 17392430]

93. Robinson NP, Blood KA, McCallum SA, Edwards PA & Bell SD (2007) Sister chromatid junctions in the hyperthermophilic archaeon Sulfolobus solfataricus EMBO J. 26:816–24 [doi: 10.1038/sj.emboj.7601529 17255945]

94. Dueber EL, Corn JE, Bell SD & Berger JM (2007) Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex Science 317:1210–3 [doi: 10.1126/science.1143690 17761879]

95. Gaudier M, Schuwirth BS, Westcott SL & Wigley DB (2007) Structural basis of DNA replication origin recognition by an ORC protein Science 317:1213–6 [doi: 10.1126/science.1143664 17761880]

96. Capaldi SA & Berger JM (2004) Biochemical characterization of Cdc6/Orc1 binding to the replication origin of the euryarchaeon Methanothermobacter thermoautotrophicus Nucleic Acids Res.32:4821–32 [doi: 10.1093/nar/gkh819 15358831]

97. Liu J, Smith CL, DeRyckere D, DeAngelis K, Martin GS & Berger JM (2000) Structure and function of Cdc6/Cdc18: implications for origin recognition and checkpoint control Mol. Cell 6:637–48 [11030343]

98. Singleton MR, Morales R, Grainge I, Cook N, Isupov MN & Wigley DB (2004) Conformational changes induced by nucleotide binding in Cdc6/ORC from Aeropyrum pernix J. Mol. Biol. 343:547–57 [doi: 10.1016/j.jmb.2004.08.044 15465044]

99. Matsunaga F, Norais C, Forterre P & Myllykallio H (2003) Identification of short 'eukaryotic' Okazaki fragments synthesized from a prokaryotic replication origin EMBO Rep. 4:154–8 [doi: 10.1038/sj.embor.embor732 12612604]

100. Berquist BR & DasSarma S (2003) An archaeal chromosomal autonomously replicating sequence element from an extreme halophile, Halobacterium sp. strain NRC-1 J. Bacteriol. 185:5959–66 [doi: 10.1128/JB.185.20.5959-5966.2003 14526006]

101. Kasiviswanathan R, Shin JH & Kelman Z (2005) Interactions between the archaeal Cdc6 and MCM proteins modulate their biochemical properties Nucleic Acids Res. 33:4940–50 [doi: 10.1093/nar/gki807 16150924]

102. Samson RY, Abeyrathne PD & Bell SD (2016) Mechanism of Archaeal MCM Helicase Recruitment to DNA Replication Origins Mol. Cell61:287–96 [doi: 10.1016/j.molcel.2015.12.005 26725007]

103. Dueber EC, Costa A, Corn JE, Bell SD & Berger JM (2011) Molecular determinants of origin discrimination by Orc1 initiators in archaea Nucleic Acids Res. 39:3621–31 [doi: 10.1093/nar/gkq1308 21227921]

104. Matsunaga F, Takemura K, Akita M, Adachi A, Yamagami T & Ishino Y (2010) Localized melting of duplex DNA by Cdc6/Orc1 at the DNA replication origin in the hyperthermophilic archaeon Pyrococcus furiosus Extremophiles 14:21–31 [doi: 10.1007/s00792-009-0284-9 19787415]

105. Onishi M, Liou GG, Buchberger JR, Walz T & Moazed D (2007) Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly Mol. Cell 28:1015–28 [doi: 10.1016/j.molcel.2007.12.004 18158899]

106. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ & Gozani O (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome Nature 484:115–9 [doi: 10.1038/nature10956 22398447]

107. Bleichert F, Botchan MR & Berger JM (2017) Mechanisms for initiating cellular DNA replication Science 355:aah6317 [doi: 10.1126/science.aah6317 28209641]

108. Gambus A, Khoudoli GA, Jones RC & Blow JJ (2011) MCM2-7 form double hexamers at licensed origins in Xenopus egg extract J. Biol. Chem. 286:11855–64 [doi: 10.1074/jbc.M110.199521 21282109]

109. 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 139:719–30 [doi: 10.1016/j.cell.2009.10.015 19896182]

110. 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. 106:20240–5 [doi: 10.1073/pnas.0911500106 19910535]

111. 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. 21:3331–41 [doi: 10.1101/gad.457807 18079179]

112. Ibarra A, Schwob E & Méndez J (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication Proc. Natl. Acad. Sci. U.S.A. 105:8956–61 [doi: 10.1073/pnas.0803978105 18579778]

113. Stinchcomb DT, Struhl K & Davis RW (1979) Isolation and characterisation of a yeast chromosomal replicator Nature 282:39–43 [doi: 10.1038/282039a0 388229]

114. Huberman JA, Spotila LD, Nawotka KA, el-Assouli SM & Davis LR (1987) The in vivo replication origin of the yeast 2 microns plasmid Cell 51:473–81 [doi: 10.1016/0092-8674(87)90643-x 3311385]

115. Brewer BJ & Fangman WL (1987) The localization of replication origins on ARS plasmids in S. cerevisiae Cell 51:463–71 [doi: 10.1016/0092-8674(87)90642-8 2822257]

116. Marahrens Y & Stillman B (1992) A yeast chromosomal origin of DNA replication defined by multiple functional elements Science255:817–23 [doi: 10.1126/science.1536007 1536007]

117. Rao H, Marahrens Y & Stillman B (1994) Functional conservation of multiple elements in yeast chromosomal replicators Mol. Cell. Biol. 14:7643–51 [doi: 10.1128/mcb.14.11.7643 7935478]

118. 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 2:1165–73 [doi: 10.1101/sqb.1983.047.01.132 6345070]

119. Celniker SE, Sweder K, Srienc F, Bailey JE & Campbell JL (1984) Deletion mutations affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae Mol. Cell. Biol. 4:2455–66 [doi: 10.1128/mcb.4.11.2455 6392851]

120. Rao H & Stillman B (1995) The origin recognition complex interacts with a bipartite DNA binding site within yeast replicators Proc. Natl. Acad. Sci. U.S.A. 92:2224–8 [doi: 10.1073/pnas.92.6.2224 7892251]

121. Rowley A, Cocker JH, Harwood J & Diffley JF (1995) 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. 14:2631–41 [7781615]

122. Bell SP & Stillman B (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex Nature 357:128–34 [doi: 10.1038/357128a0 1579162]

123. Li N, Lam WH, Zhai Y, Cheng J, Cheng E, Zhao Y, Gao N & Tye BK (2018) Structure of the origin recognition complex bound to DNA replication origin Nature 559:217–222 [doi: 10.1038/s41586-018-0293-x 29973722]

124. Bleichert F, Botchan MR & Berger JM (2015) Crystal structure of the eukaryotic origin recognition complex Nature 519:321–6 [doi: 10.1038/nature14239 25762138]

125. Sun J, Evrin C, Samel SA, Fernández-Cid A, Riera A, Kawakami H, Stillman B, Speck C & Li H (2013) Cryo-EM structure of a helicase loading intermediate containing ORC-Cdc6-Cdt1-MCM2-7 bound to DNA Nat. Struct. Mol. Biol. 20:944–51 [doi: 10.1038/nsmb.2629 23851460]

126. Kawakami H, Ohashi E, Kanamoto S, Tsurimoto T & Katayama T (2015) Specific binding of eukaryotic ORC to DNA replication origins depends on highly conserved basic residues Sci Rep 5:14929 [doi: 10.1038/srep14929 26456755]

127. Palzkill TG & Newlon CS (1988) A yeast replication origin consists of multiple copies of a small conserved sequence Cell 53:441–50 [doi: 10.1016/0092-8674(88)90164-x 3284655]

128. Wilmes GM & Bell SP (2002) The B2 element of the Saccharomyces cerevisiae ARS1 origin of replication requires specific sequences to facilitate pre-RC formation Proc. Natl. Acad. Sci. U.S.A. 99:101–6 [doi: 10.1073/pnas.012578499 11756674]

129. Coster G & Diffley JFX (2017) Bidirectional eukaryotic DNA replication is established by quasi-symmetrical helicase loading Science 357:314–8 [doi: 10.1126/science.aan0063 28729513]

130. Zou L & Stillman B (2000) 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. 20:3086–96 [doi: 10.1128/mcb.20.9.3086-3096.2000 10757793]

131. Lipford JR & Bell SP (2001) Nucleosomes positioned by ORC facilitate the initiation of DNA replication Mol. Cell 7:21–30 [11172708]

132. Diffley JF & Cocker JH (1992) Protein-DNA interactions at a yeast replication origin Nature 357:169–72 [doi: 10.1038/357169a0 1579168]

133. Diffley JF & Stillman B (1988) Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer Proc. Natl. Acad. Sci. U.S.A. 85:2120–4 [doi: 10.1073/pnas.85.7.2120 3281162]

134. Miotto B, Ji Z & Struhl K (2016) Selectivity of ORC binding sites and the relation to replication timing, fragile sites, and deletions in cancers Proc. Natl. Acad. Sci. U.S.A. 113:E4810–9 [doi: 10.1073/pnas.1609060113 27436900]

135. MacAlpine HK, Gordân R, Powell SK, Hartemink AJ & MacAlpine DM (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading Genome Res. 20:201–11 [doi: 10.1101/gr.097873.109 19996087]

136. Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV & MacAlpine DM (2011) Chromatin signatures of the Drosophila replication program Genome Res. 21:164–74 [doi: 10.1101/gr.116038.110 21177973]

137. Dellino GI, Cittaro D, Piccioni R, Luzi L, Banfi S, Segalla S, Cesaroni M, Mendoza-Maldonado R, Giacca M & Pelicci PG (2013) Genome-wide mapping of human DNA-replication origins: levels of transcription at ORC1 sites regulate origin selection and replication timing Genome Res. 23:1–11 [doi: 10.1101/gr.142331.112 23187890]

138. Cayrou C, Ballester B, Peiffer I, Fenouil R, Coulombe P, Andrau JC, van Helden J & Méchali M (2015) The chromatin environment shapes DNA replication origin organization and defines origin classes Genome Res. 25:1873–85 [doi: 10.1101/gr.192799.115 26560631]

139. Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, Peiffer I, Rivals E, Puy A, Laurent-Chabalier S, Desprat R & Méchali M (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features Genome Res. 21:1438–49 [doi: 10.1101/gr.121830.111 21750104]

140. Lubelsky Y, Sasaki T, Kuipers MA, Lucas I, Le Beau MM, Carignon S, Debatisse M, Prinz JA, Dennis JH & Gilbert DM (2011) Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone Nucleic Acids Res. 39:3141–55 [doi: 10.1093/nar/gkq1276 21148149]

141. Hayashi M, Katou Y, Itoh T, Tazumi A, Tazumi M, Yamada Y, Takahashi T, Nakagawa T, Shirahige K & Masukata H (2007) Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast EMBO J. 26:1327–39 [doi: 10.1038/sj.emboj.7601585 17304213]

142. Martin MM, Ryan M, Kim R, Zakas AL, Fu H, Lin CM, Reinhold WC, Davis SR, Bilke S, Liu H, Doroshow JH, Reimers MA, Valenzuela MS, Pommier Y, Meltzer PS & Aladjem MI (2011) Genome-wide depletion of replication initiation events in highly transcribed regions Genome Res. 21:1822–32 [doi: 10.1101/gr.124644.111 21813623]

143. Pourkarimi E, Bellush JM & Whitehouse I (2016) Spatiotemporal coupling and decoupling of gene transcription with DNA replication origins during embryogenesis in C. elegans elife 5:e21728 [doi: 10.7554/eLife.21728 28009254]

144. Rodríguez-Martínez M, Pinzón N, Ghommidh C, Beyne E, Seitz H, Cayrou C & Méchali M (2017) The gastrula transition reorganizes replication-origin selection in Caenorhabditis elegans Nat. Struct. Mol. Biol. 24:290–9 [doi: 10.1038/nsmb.3363 28112731]

145. Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, Dantec C, Marin JM & Lemaitre JM (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs Nat. Struct. Mol. Biol. 19:837–44 [doi: 10.1038/nsmb.2339 22751019]

146. Delgado S, Gómez M, Bird A & Antequera F (1998) Initiation of DNA replication at CpG islands in mammalian chromosomes EMBO J.17:2426–35 [doi: 10.1093/emboj/17.8.2426 9545253]

147. Sequeira-Mendes J, Díaz-Uriarte R, Apedaile A, Huntley D, Brockdorff N & Gómez M (2009) Transcription initiation activity sets replication origin efficiency in mammalian cells PLoS Genet. 5:e1000446 [doi: 10.1371/journal.pgen.1000446 19360092]

148. Kelly T & Callegari AJ (2019) Dynamics of DNA replication in a eukaryotic cell Proc. Natl. Acad. Sci. U.S.A. 116:4973–82 [doi: 10.1073/pnas.1818680116 30718387]

149. Austin RJ, Orr-Weaver TL & Bell SP (1999) Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element Genes Dev. 13:2639–49 [doi: 10.1101/gad.13.20.2639 10541550]

150. 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 420:833–7 [doi: 10.1038/nature01228 12490953]

151. Beall EL, Bell M, Georlette D & Botchan MR (2004) Dm-myb mutant lethality in Drosophila is dependent upon mip130: positive and negative regulation of DNA replication Genes Dev. 18:1667–80 [doi: 10.1101/gad.1206604 15256498]

152. Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ & Botchan MR (2004) Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex Genes Dev. 18:2929–40 [doi: 10.1101/gad.1255204 15545624]

153. Bosco G, Du W & Orr-Weaver TL (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex Nat. Cell Biol. 3:289–95 [doi: 10.1038/35060086 11231579]

154. Chuang RY & 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. 96:2656–61 [doi: 10.1073/pnas.96.6.2656 10077566]

155. Balasov M, Huijbregts RP & Chesnokov I (2007) Role of the Orc6 protein in origin recognition complex-dependent DNA binding and replication in Drosophila melanogaster Mol. Cell. Biol. 27:3143–53 [doi: 10.1128/MCB.02382-06 17283052]

156. Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, Sardet C & Julien E (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells Nat. Cell Biol. 12:1086–93 [doi: 10.1038/ncb2113 20953199]

157. Beck DB, Burton A, Oda H, Ziegler-Birling C, Torres-Padilla ME & Reinberg D (2012) The role of PR-Set7 in replication licensing depends on Suv4-20h Genes Dev. 26:2580–9 [doi: 10.1101/gad.195636.112 23152447]

158. Brustel J, Kirstein N, Izard F, Grimaud C, Prorok P, Cayrou C, Schotta G, Abdelsamie AF, Déjardin J, Méchali M, Baldacci G, Sardet C, Cadoret JC, Schepers A & Julien E (2017) Histone H4K20 tri-methylation at late-firing origins ensures timely heterochromatin replication EMBO J.36:2726–41 [doi: 10.15252/embj.201796541 28778956]

159. Shoaib M, Walter D, Gillespie PJ, Izard F, Fahrenkrog B, Lleres D, Lerdrup M, Johansen JV, Hansen K, Julien E, Blow JJ & Sørensen CS (2018) Histone H4K20 methylation mediated chromatin compaction threshold ensures genome integrity by limiting DNA replication licensing Nat Commun 9:3704 [doi: 10.1038/s41467-018-06066-8 30209253]

160. Noguchi K, Vassilev A, Ghosh S, Yates JL & DePamphilis ML (2006) The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo EMBO J. 25:5372–82 [doi: 10.1038/sj.emboj.7601396 17066079]

161. Shen Z, Chakraborty A, Jain A, Giri S, Ha T, Prasanth KV & Prasanth SG (2012) Dynamic association of ORCA with prereplicative complex components regulates DNA replication initiation Mol. Cell. Biol.32:3107–20 [doi: 10.1128/MCB.00362-12 22645314]

162. Wang Y, Khan A, Marks AB, Smith OK, Giri S, Lin YC, Creager R, MacAlpine DM, Prasanth KV, Aladjem MI & Prasanth SG (2017) Temporal association of ORCA/LRWD1 to late-firing origins during G1 dictates heterochromatin replication and organization Nucleic Acids Res. 45:2490–502 [doi: 10.1093/nar/gkw1211 27924004]

163. Bartke T, Vermeulen M, Xhemalce B, Robson SC, Mann M & Kouzarides T (2010) Nucleosome-interacting proteins regulated by DNA and histone methylation Cell 143:470–84 [doi: 10.1016/j.cell.2010.10.012 21029866]

164. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG & Mann M (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers Cell 142:967–80 [doi: 10.1016/j.cell.2010.08.020 20850016]

165. Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N, Toyoda Y, Gak IA, Weisswange I, Mansfeld J, Buchholz F, Hyman AA & Mann M (2015) A human interactome in three quantitative dimensions organized by stoichiometries and abundances Cell 163:712–23 [doi: 10.1016/j.cell.2015.09.053 26496610]

166. Thomae AW, Pich D, Brocher J, Spindler MP, Berens C, Hock R, Hammerschmidt W & Schepers A (2008) Interaction between HMGA1a and the origin recognition complex creates site-specific replication origins Proc. Natl. Acad. Sci. U.S.A. 105:1692–7 [doi: 10.1073/pnas.0707260105 18234858]

167. Zhang Y, Huang L, Fu H, Smith OK, Lin CM, Utani K, Rao M, Reinhold WC, Redon CE, Ryan M, Kim R, You Y, Hanna H, Boisclair Y, Long Q & Aladjem MI (2016) A replicator-specific binding protein essential for site-specific initiation of DNA replication in mammalian cells Nat Commun 7:11748 [doi: 10.1038/ncomms11748 27272143]

168. Bleichert F, Leitner A, Aebersold R, Botchan MR & Berger JM (2018) Conformational control and DNA-binding mechanism of the metazoan origin recognition complex Proc. Natl. Acad. Sci. U.S.A.115:E5906–15 [doi: 10.1073/pnas.1806315115 29899147]

169. Clarey MG, Botchan M & Nogales E (2008) Single particle EM studies of the Drosophila melanogaster origin recognition complex and evidence for DNA wrapping J. Struct. Biol. 164:241–9 [doi: 10.1016/j.jsb.2008.08.006 18824234]

170. Lee DG & Bell SP (1997) Architecture of the yeast origin recognition complex bound to origins of DNA replication Mol. Cell. Biol. 17:7159–68 [doi: 10.1128/mcb.17.12.7159 9372948]

171. Riera A, Barbon M, Noguchi Y, Reuter LM, Schneider S & Speck C (2017) From structure to mechanism-understanding initiation of DNA replication Genes Dev. 31:1073–88 [doi: 10.1101/gad.298232.117 28717046]

172. Tognetti S, Riera A & Speck C (2015) Switch on the engine: how the eukaryotic replicative helicase MCM2-7 becomes activated Chromosoma 124:13–26 [doi: 10.1007/s00412-014-0489-2 25308420]

173. Berbenetz NM, Nislow C & Brown GW (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure PLoS Genet. 6:e1001092 [doi: 10.1371/journal.pgen.1001092 20824081]

174. Eaton ML, Galani K, Kang S, Bell SP & MacAlpine DM (2010) Conserved nucleosome positioning defines replication origins Genes Dev. 24:748–53 [doi: 10.1101/gad.1913210 20351051]

175. Azmi IF, Watanabe S, Maloney MF, Kang S, Belsky JA, MacAlpine DM, Peterson CL & Bell SP (2017) Nucleosomes influence multiple steps during replication initiation eLife 6:e22512 [doi: 10.7554/eLife.22512 28322723]

176. Miotto B & Struhl K (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin Mol. Cell 37:57–66 [doi: 10.1016/j.molcel.2009.12.012 20129055]

177. Liu J, Zimmer K, Rusch DB, Paranjape N, Podicheti R, Tang H & Calvi BR (2015) DNA sequence templates adjacent nucleosome and ORC sites at gene amplification origins in Drosophila Nucleic Acids Res.43:8746–61 [doi: 10.1093/nar/gkv766 26227968]

178. Zhao PA, Rivera-Mulia JC & Gilbert DM (2017) Replication Domains: Genome Compartmentalization into Functional Replication Units Adv. Exp. Med. Biol. 1042:229–57 [doi: 10.1007/978-981-10-6955-0_11 29357061]

179. Sugimoto N & Fujita M (2017) Molecular Mechanism for Chromatin Regulation During MCM Loading in Mammalian Cells Adv. Exp. Med. Biol. 1042:61–78 [doi: 10.1007/978-981-10-6955-0_3 29357053]

180. MacAlpine DM & Almouzni G (2013) Chromatin and DNA replication Cold Spring Harb Perspect Biol 5:a010207 [doi: 10.1101/cshperspect.a010207 23751185]

181. Sima J, Chakraborty A, Dileep V, Michalski M, Klein KN, Holcomb NP, Turner JL, Paulsen MT, Rivera-Mulia JC, Trevilla-Garcia C, Bartlett DA, Zhao PA, Washburn BK, Nora EP, Kraft K, Mundlos S, Bruneau BG, Ljungman M, Fraser P, Ay F & Gilbert DM (2019) Identifying cis Elements for Spatiotemporal Control of Mammalian DNA Replication Cell 176:816–30. [doi: 10.1016/j.cell.2018.11.036 30595451]

182. Cadoret JC, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C, Duret L, Quesneville H & Prioleau MN (2008) Genome-wide studies highlight indirect links between human replication origins and gene regulation Proc. Natl. Acad. Sci. U.S.A. 105:15837–42 [doi: 10.1073/pnas.0805208105 18838675]

183. 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 60:797–807 [doi: 10.1016/j.molcel.2015.10.022 26656162]

184. Letessier A, Millot GA, Koundrioukoff S, Lachagès AM, Vogt N, Hansen RS, Malfoy B, Brison O & Debatisse M (2011) Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site Nature 470:120–3 [doi: 10.1038/nature09745 21258320]

185. Smith OK, Kim R, Fu H, Martin MM, Lin CM, Utani K, Zhang Y, Marks AB, Lalande M, Chamberlain S, Libbrecht MW, Bouhassira EE, Ryan MC, Noble WS & Aladjem MI (2016) Distinct epigenetic features of differentiation-regulated replication origins Epigenetics Chromatin9:18 [doi: 10.1186/s13072-016-0067-3 27168766]

186. Sher N, Bell GW, Li S, Nordman J, Eng T, Eaton ML, Macalpine DM & Orr-Weaver TL (2012) Developmental control of gene copy number by repression of replication initiation and fork progression Genome Res.22:64–75 [doi: 10.1101/gr.126003.111 22090375]

187. Comoglio F, Schlumpf T, Schmid V, Rohs R, Beisel C & Paro R (2015) High-resolution profiling of Drosophila replication start sites reveals a DNA shape and chromatin signature of metazoan origins Cell Rep11:821–34 [doi: 10.1016/j.celrep.2015.03.070 25921534]

188. Calvi BR, Lilly MA & Spradling AC (1998) Cell cycle control of chorion gene amplification Genes Dev. 12:734–44 [doi: 10.1101/gad.12.5.734 9499407]

189. Mosig G (1998) Recombination and recombination-dependent DNA replication in bacteriophage T4 Annu. Rev. Genet. 32:379–413 [doi: 10.1146/annurev.genet.32.1.379 9928485]

190. Ravoitytė B & Wellinger RE (2017) Non-Canonical Replication Initiation: You're Fired! Genes (Basel) 8:E54 [doi: 10.3390/genes8020054 28134821]

191. Asai T, Sommer S, Bailone A & Kogoma T (1993) Homologous recombination-dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli EMBO J. 12:3287–95 [8344265]

192. Lydeard JR, Jain S, Yamaguchi M & Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32 Nature 448:820–3 [doi: 10.1038/nature06047 17671506]

193. Dasgupta S, Masukata H & Tomizawa J (1987) Multiple mechanisms for initiation of ColE1 DNA replication: DNA synthesis in the presence and absence of ribonuclease H Cell 51:1113–22 [doi: 10.1016/0092-8674(87)90597-6 2446774]

194. Stuckey R, García-Rodríguez N, Aguilera A & Wellinger RE (2015) Role for RNA:DNA hybrids in origin-independent replication priming in a eukaryotic system Proc. Natl. Acad. Sci. U.S.A. 112:5779–84 [doi: 10.1073/pnas.1501769112 25902524]

195. Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective Cold Spring Harb Perspect Biol 6:a016147 [doi: 10.1101/cshperspect.a016147 24789819]

196. Lee PH, Meng X & Kapler GM (2015) Developmental regulation of the Tetrahymena thermophila origin recognition complex PLoS Genet.11:e1004875 [doi: 10.1371/journal.pgen.1004875 25569357]

197. Mohammad MM, Donti TR, Sebastian Yakisich J, Smith AG & Kapler GM (2007) Tetrahymena ORC contains a ribosomal RNA fragment that participates in rDNA origin recognition EMBO J. 26:5048–60 [doi: 10.1038/sj.emboj.7601919 18007594]

198. Donti TR, Datta S, Sandoval PY & Kapler GM (2009) Differential targeting of Tetrahymena ORC to ribosomal DNA and non-rDNA replication origins EMBO J. 28:223–33 [doi: 10.1038/emboj.2008.282 19153611]

199. Marques CA & McCulloch R (2018) Conservation and Variation in Strategies for DNA Replication of Kinetoplastid Nuclear Genomes Curr. Genomics 19:98–109 [doi: 10.1186/s12864-018-4453-z 29491738]

200. Marques CA, Tiengwe C, Lemgruber L, Damasceno JD, Scott A, Paape D, Marcello L & McCulloch R (2016) Diverged composition and regulation of the Trypanosoma brucei origin recognition complex that mediates DNA replication initiation Nucleic Acids Res. 44:4763–84 [doi: 10.1093/nar/gkw147 26951375]

201. Tiengwe C, Marcello L, Farr H, Gadelha C, Burchmore R, Barry JD, Bell SD & McCulloch R (2012) Identification of ORC1/CDC6-interacting factors in Trypanosoma brucei reveals critical features of origin recognition complex architecture PLoS ONE 7:e32674 [doi: 10.1371/journal.pone.0032674 22412905]

202. Marques CA, Dickens NJ, Paape D, Campbell SJ & McCulloch R (2015) Genome-wide mapping reveals single-origin chromosome replication in Leishmania, a eukaryotic microbe Genome Biol. 16:230 [doi: 10.1186/s13059-015-0788-9 26481451]

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