The chromatin environment shapes DNA replication origin organization and defines origin classes

Genome Research

Volumn 25, Issue 12, 2015, Pages 1873-1885

  Cayrou, Christelle ^a,f   Ballester, Benoit ^b   Peiffer, Isabelle ^a   Fenouil, Romain ^c,d   Coulombe, Philippe ^a   Andrau, Jean Christophe ^c,e   Van Helden, Jacques ^b   Méchali, Marcel ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b Aix Marseille university   (France)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d MOUNT SINAI HOSPITAL   (United States)

^e INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^f UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE QUADRUPLEX; POLYCOMB GROUP PROTEIN; CHROMATIN; HETEROCHROMATIN; HISTONE; NUCLEOSOME; ORIGIN RECOGNITION COMPLEX;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CHROMATIN; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA REPLICATION ORIGIN; DNA TRANSCRIPTION; EMBRYONIC STEM CELL; ENHANCER REGION; EPIGENETICS; HUMAN; HUMAN CELL; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEOSOME; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE; ANIMAL; BIOLOGY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL MAPPING; CLUSTER ANALYSIS; DNA BASE COMPOSITION; DNA REPLICATION; GENETICS; GENOME; GENOMICS; HETEROCHROMATIN; HIGH THROUGHPUT SEQUENCING; METABOLISM; NUCLEOTIDE MOTIF; PROCEDURES; TRANSCRIPTION INITIATION;

ANIMALS; BASE COMPOSITION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME MAPPING; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DNA REPLICATION; EMBRYONIC STEM CELLS; GENOME; GENOMICS; HETEROCHROMATIN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTONES; HUMANS; MICE; NUCLEOSOMES; NUCLEOTIDE MOTIFS; ORIGIN RECOGNITION COMPLEX; REPLICATION ORIGIN; TRANSCRIPTIONAL ACTIVATION;

EID: 84956625318     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.192799.115     Document Type: Article

References (75)

1. Abdurashidova G, Deganuto M, Klima R, Riva S, Biamonti G, Giacca M, Falaschi A. 2000. Start sites of bidirectional DNA synthesis at the human lamin B2 origin. Science 287: 2023-2026.
2. Adelman K, Lis JT. 2012. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet 13: 720-731.
3. Aladjem MI. 2007. Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8: 588-600.
4. Bailey TL, Johnson J, Grant CE, Noble WS. 2015. The MEME Suite. Nucleic Acids Res 43: W39-W49.
5. 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.
6. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
7. 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: 837-844.
8. Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, Peiffer I, Rivals E, Puy A, Laurent-Chabalier S, Desprat R, et al. 2011. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res 21: 1438-1449.
9. Cayrou C, Coulombe P, Puy A, Rialle S, Kaplan N, Segal E, Méchali M. 2012a. New insights into replication origin characteristics in metazoans. Cell Cycle 11: 658-667.
10. Cayrou C, Grégoire D, Coulombe P, Danis E, Méchali M. 2012b. Genomescale identification of active DNA replication origins. Methods 57: 158-164.
11. Costas C, de la Paz Sanchez M, Stroud H, Yu Y, Oliveros JC, Feng S, Benguria A, López-Vidriero I, Zhang X, Solano R, et al. 2011. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat Struct Mol Biol 18: 395-400.
12. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
13. Delgado S, Gómez M, Bird A, Antequera F. 1998. Initiation of DNA replication at CpG islands in mammalian chromosomes. EMBO J 17: 2426-2435.
14. DePamphilis ML. 1993. Origins of DNA replication that function in eukaryotic cells. Curr Opin Cell Biol 5: 434-441.
15. Di Cerbo V, Mohn F, Ryan DP, Montellier E, Kacem S, Tropberger P, Kallis E, Holzner M, Hoerner L, Feldmann A, et al. 2014. Acetylation of histone H3 at lysine 64 regulates nucleosome dynamics and facilitates transcription. eLife 3: e01632.
16. Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM. 2010. Conserved nucleosome positioning defines replication origins. Genes Dev 24: 748-753.
17. Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ, Innocenti C, Ferrier P, Spicuglia S, Gut M, Gut I, et al. 2012. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res 22: 2399-2408.
18. Foulk MS, Urban JM, Gerbi SA. 2015. Characterizing and controlling intrinsic biases of lambda exonuclease in nascent strand sequencing reveals phasing between nucleosomes and G-quadruplex motifs around a subset of human replication origins. Genome Res 25: 725-735.
19. Fragkos M, Ganier O, Coulombe P, Méchali M. 2015. DNA replication origin activation in space and time. Nat Rev Mol Cell Biol 16: 360-374.
20. Gindin Y, Valenzuela MS, AladjemMI, Meltzer PS, Bilke S. 2014. A chromatin structure-based model accurately predicts DNA replication timing in human cells. Mol Syst Biol 10: 722.
21. Givens RM, Lai WK, Rizzo JM, Bard JE, Mieczkowski PA, Leatherwood J, Huberman JA, Buck MJ. 2012. Chromatin architectures at fission yeast transcriptional promoters and replication origins. Nucleic Acids Res 40: 7176-7189.
22. Görisch SM, Wachsmuth M, Tóth KF, Lichter P, Rippe K. 2005. Histone acetylation increases chromatin accessibility. J Cell Sci 118: 5825-5834.
23. Halder K, Halder R, Chowdhury S. 2009. Genome-wide analysis predicts DNA structural motifs as nucleosome exclusion signals. Mol Biosyst 5: 1703-1712.
24. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang CW, Lyou Y, Townes TM, Schübeler D, Gilbert DM. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6: e245.
25. Hoggard T, Shor E, Müller CA, Nieduszynski CA, Fox CA. 2013. A link between ORC-origin binding mechanisms and origin activation time revealed in budding yeast. PLoS Genet 9: e1003798.
26. Hoshina S, Yura K, Teranishi H, Kiyasu N, Tominaga A, Kadoma H, Nakatsuka A, Kunichika T, Obuse C, Waga S. 2013. Human origin recognition complex binds preferentially to G-quadruplex-preferable RNA and single-stranded DNA. J Biol Chem 288: 30161-30171.
27. Huppert JL, Balasubramanian S. 2007. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 35: 406-413.
28. Iyer V, Struhl K. 1995. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J 14: 2570-2579.
29. Jia J, Zheng X, Hu G, Cui K, Zhang J, Zhang A, Jiang H, Lu B, Yates J III, Liu C, et al. 2012. Regulation of pluripotency and self-renewal of ESCs through epigenetic-threshold modulation and mRNA pruning. Cell 151: 576-589.
30. Jin C, Felsenfeld G. 2007. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21: 1519-1529.
31. Kanoh Y, Matsumoto S, Fukatsu R, Kakusho N, Kono N, Renard-Guillet C, Masuda K, Iida K, Nagasawa K, Shirahige K, et al. 2015. Rif1 binds to G quadruplexes and suppresses replication over long distances. Nat Struct Mol Biol doi: 10.1038/nsmb.3102.
32. Kobayashi T, Rein T, DePamphilis ML. 1998. Identification of primary initiation sites for DNA replication in the hamster dihydrofolate reductase gene initiation zone. Mol Cell Biol 18: 3266-3277.
33. Koch F, Fenouil R, Gut M, Cauchy P, Albert TK, Zacarias-Cabeza J, Spicuglia S, de la Chapelle AL, Heidemann M, Hintermair C, et al. 2011. Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat Struct Mol Biol 18: 956-963.
34. König SL, Huppert JL, Sigel RK, Evans AC. 2013. Distance-dependent duplex DNA destabilization proximal to G-quadruplex/i-motif sequences. Nucleic Acids Res 41: 7453-7461.
35. Koren A, Handsaker RE, Kamitaki N, Karlic R, Ghosh S, Polak P, Eggan K, McCarroll SA. 2014. Genetic variation in human DNA replication timing. Cell 159: 1015-1026.
36. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
37. Lantermann AB, Straub T, Stralfors A, Yuan GC, Ekwall K, Korber P. 2010. Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiæ. Nat Struct Mol Biol 17: 251-257.
38. Li B, Su T, Ferrari R, Li JY, Kurdistani SK. 2014. A unique epigenetic signature is associated with active DNA replication loci in human embryonic stem cells. Epigenetics 9: 257-267.
39. Liu H, Mulholland N, Fu H, Zhao K. 2006. Cooperative activity of BRG1 and Z-DNA formation in chromatin remodeling. Mol Cell Biol 26: 2550-2559.
40. Liu X, Kraus WL, Bai X. 2015. Ready, pause, go: regulation of RNA polymerase II pausing and release by cellular signaling pathways. Trends Biochem Sci 40: 516-525.
41. Lombraña R, Almeida R, Revuelta I, Madeira S, Herranz G, Saiz N, Bastolla U, Gómez M. 2013. High-resolution analysis of DNA synthesis start sites and nucleosome architecture at efficient mammalian replication origins. EMBO J 32: 2631-2644.
42. 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: 3141-3155.
43. 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: 201-211.
44. Majewski J, Ott J. 2000. GT repeats are associated with recombination on human chromosome 22. Genome Res 10: 1108-1114.
45. Marahrens Y, Stillman B. 1992. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255: 817-823.
46. Maruyama A, Mimura J, Harada N, Itoh K. 2013. Nrf2 activation is associated with Z-DNA formation in the human HO-1 promoter. Nucleic Acids Res 41: 5223-5234.
47. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF. 2008. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073-1083.
48. Nordman J, Orr-Weaver TL. 2012. Regulation of DNA replication during development. Development 139: 455-464.
49. Pæschke K, Capra JA, Zakian VA. 2011. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiæ Pif1 DNA helicase. Cell 145: 678-691.
50. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K. 2004. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061-4071.
51. Picard F, Cadoret JC, Audit B, Arneodo A, Alberti A, Battail C, Duret L, Prioleau MN. 2014. The spatiotemporal program of DNA replication is associated with specific combinations of chromatin marks in human cells. PLoS Genet 10: e1004282.
52. Piunti A, Rossi A, Cerutti A, Albert M, Jammula S, Scelfo A, Cedrone L, Fragola G, Olsson L, Koseki H, et al. 2014. Polycomb proteins control proliferation and transformation independently of cell cycle checkpoints by regulating DNA replication. Nat Commun 5: 3649.
53. Prioleau MN. 2009. CpG islands: starting blocks for replication and transcription. PLoS Genet 5: e1000454.
54. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
55. R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org/.
56. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
57. Rhind N, Gilbert DM. 2013. DNA replication timing. Cold Spring Harb Perspect Med 3: 1-26.
58. Rhodes D. 1979. Nucleosome cores reconstituted from poly (dA-dT) and the octamer of histones. Nucleic Acids Res 6: 1805-1816.
59. Romero J, Lee H. 2008. Asymmetric bidirectional replication at the human DBF4 origin. Nat Struct Mol Biol 15: 722-729.
60. Sarkies P, Reams C, Simpson LJ, Sale JE. 2010. Epigenetic instability due to defective replication of structured DNA. Mol Cell 40: 703-713.
61. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. 2011. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
62. Tan BC, Chien CT, Hirose S, Lee SC. 2006. Functional cooperation between FACT andMCMhelicase facilitates initiation of chromatin DNA replication. EMBO J 25: 3975-3985.
63. Teif VB, Vainshtein Y, Caudron-Herger M, Mallm JP, Marth C, Höfer T, Rippe K. 2012. Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol 19: 1185-1192.
64. Valton AL, Hassan-Zadeh V, Lema I, Boggetto N, Alberti P, Saintomé C, Riou JF, Prioleau MN. 2014. G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBO J 33: 732-746.
65. van Helden J, del Olmo M, Pérez-Ortín JE. 2000. Statistical analysis of yeast genomic downstream sequences reveals putative polyadenylation signals. Nucleic Acids Res 28: 1000-1010.
66. Vorobyeva NE, Mazina MU, Golovnin AK, Kopytova DV, Gurskiy DY, Nabirochkina EN, Georgieva SG, Georgiev PG, Krasnov AN. 2013 Insulator protein Su(Hw) recruits SAGA and Brahma complexes and constitutes part of Origin Recognition Complex-binding sites in the Drosophila genome. Nucleic Acids Res 41: 5717-5730.
67. Wachter E, Quante T, Merusi C, Arczewska A, Stewart F, Webb S, Bird A. 2014. Synthetic CpG islands reveal DNA sequence determinants of chromatin structure. eLife 3: e03397.
68. Wahls WP, Wallace LJ, Moore PD. 1990. The Z-DNA motif d(TG)30 promotes reception of information during gene conversion events while stimulating homologous recombination in human cells in culture. Mol Cell Biol 10: 785-793.
69. Wahls WP, Swenson G, Moore PD. 1991. Two hypervariable minisatellite DNA binding proteins. Nucleic Acids Res 19: 3269-3274.
70. Wang S, Dijkwel PA, Hamlin JL. 1998. Lagging-strand, early-labelling, and two-dimensional gel assays suggest multiple potential initiation sites in the Chinese hamster dihydrofolate reductase origin. Mol Cell Biol 18: 39-50.
71. Widlund HR, Cao H, Simonsson S, Magnusson E, Simonsson T, Nielsen PE, Kahn JD, Crothers DM, Kubista M. 1997. Identification and characterization of genomic nucleosome-positioning sequences. J Mol Biol 267: 807-817.
72. Wong HM, Huppert JL. 2009. Stable G-quadruplexes are found outside nucleosome-bound regions. Mol Biosyst 5: 1713-1719.
73. Xu J, Yanagisawa Y, Tsankov AM, Hart C, Aoki K, Kommajosyula N, Steinmann KE, Bochicchio J, Russ C, Regev A, et al. 2012. Genomewide identification and characterization of replication origins by deep sequencing. Genome Biol 13: R27.
74. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histonemodification ChIP-Seq data. Bioinformatics 25: 1952-1958.
75. Zellner E, Herrmann T, Schulz C, Grummt F. 2007. Site-specific interaction of the murine pre-replicative complex with origin DNA: assembly and disassembly during cell cycle transit and differentiation. Nucleic Acids Res 35: 6701-6713.