Abstract
DNA replication ensures the accurate duplication of the genome at each cell cycle. During S phase, tens of thousands of replication origins throughout the vertebrate genome are activated according to a spatiotemporal program. The genome-wide mapping of origins in several model systems has identified G-quadruplexes—higher-order DNA structures formed from G-rich sequences—as potential key regulators of origin activity. Here, I describe genetic experiments demonstrating the role of G-quadruplexes in origin function. I discuss the different means by which G-quadruplexes might regulate origin function. Finally, comparisons of replicon organization in the three domains of life suggest that G-quadruplexes may have retained a conserved role in origin function during evolution.
This is a preview of subscription content, log in via an institution to check access.
References
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. https://doi.org/10.1371/journal.pgen.1001092
Berezney R, Dubey DD, Huberman JA (2000) Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108:471–484
Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, Dantec C, Marin J-M, Lemaitre J-M (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol 19:837–844. https://doi.org/10.1038/nsmb.2339
Bielinsky AK, Gerbi SA (1998) Discrete start sites for DNA synthesis in the yeast ARS1 origin. Science 279:95–98
Cadoret J-C, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C, Duret L, Quesneville H, Prioleau M-N (2008) Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U S A 105:15837–15842. https://doi.org/10.1073/pnas.0805208105
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 21:1438–1449. https://doi.org/10.1101/gr.121830.111
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 11:658–667. https://doi.org/10.4161/cc.11.4.19097
Cayrou C, Ballester B, Peiffer I, Fenouil R, Coulombe P, Andrau J-C, van Helden J, Méchali M (2015) The chromatin environment shapes DNA replication origin organization and defines origin classes. Genome Res 25:1873–1885. https://doi.org/10.1101/gr.192799.115
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 96:2656–2661
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 Rep 11:821–834. https://doi.org/10.1016/j.celrep.2015.03.070
Diffley JFX (2004) Regulation of early events in chromosome replication. Curr Biol 14:R778–R786. https://doi.org/10.1016/j.cub.2004.09.019
Dueber ELC, Corn JE, Bell SD, Berger JM (2007) Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science 317:1210–1213. https://doi.org/10.1126/science.1143690
Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM (2010) Conserved nucleosome positioning defines replication origins. Genes Dev 24:748–753. https://doi.org/10.1101/gad.1913210
Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ, Innocenti C, Ferrier P, Spicuglia S, Gut M, Gut I, Andrau J-C (2012) CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res 22:2399–2408. https://doi.org/10.1101/gr.138776.112
Foulk MS, Urban JM, Casella C, 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. https://doi.org/10.1101/gr.183848.114
Gaudier M, Schuwirth BS, Westcott SL, Wigley DB (2007) Structural basis of DNA replication origin recognition by an ORC protein. Science 317:1213–1216. https://doi.org/10.1126/science.1143664
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 21:3331–3341. https://doi.org/10.1101/gad.457807
Hänsel-Hertsch R, Beraldi D, Lensing SV, Marsico G, Zyner K, Parry A, Di Antonio M, Pike J, Kimura H, Narita M, Tannahill D, Balasubramanian S (2016) G-quadruplex structures mark human regulatory chromatin. Nat Genet 48:1267–1272. https://doi.org/10.1038/ng.3662
Hassan-Zadeh V, Chilaka S, Cadoret J-C, Ma MK-W, Boggetto N, West AG, Prioleau M-N (2012) USF binding sequences from the HS4 insulator element impose early replication timing on a vertebrate replicator. PLoS Biol 10:e1001277. https://doi.org/10.1371/journal.pbio.1001277
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 26:1327–1339. https://doi.org/10.1038/sj.emboj.7601585
Heichinger C, Penkett CJ, Bähler J, Nurse P (2006) Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25:5171–5179. https://doi.org/10.1038/sj.emboj.7601390
Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang C-W, Lyou Y, Townes TM, Schübeler D, Gilbert DM (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6:e245. https://doi.org/10.1371/journal.pbio.0060245
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. https://doi.org/10.1074/jbc.M113.492504
Huppert JL, Balasubramanian S (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res 33:2908–2916. https://doi.org/10.1093/nar/gki609
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 105:8956–8961. https://doi.org/10.1073/pnas.0803978105
Jacob F, Brenner S, Cuzin F (1963) On the regulation of DNA replication in bacteria. Cold Spring Harb Symp Quant Biol 28:329–348. https://doi.org/10.1101/SQB.1963.028.01.048
Keller H, Kiosze K, Sachsenweger J, Haumann S, Ohlenschläger O, Nuutinen T, Syväoja JE, Görlach M, Grosse F, Pospiech H (2014) The intrinsically disordered amino-terminal region of human RecQL4: multiple DNA-binding domains confer annealing, strand exchange and G4 DNA binding. Nucleic Acids Res 42:12614–12627. https://doi.org/10.1093/nar/gku993
Kelman LM, Kelman Z (2014) Archaeal DNA replication. Annu Rev Genet 48:71–97. https://doi.org/10.1146/annurev-genet-120213-092148
Langley AR, Gräf S, Smith JC, Krude T (2016) Genome-wide identification and characterisation of human DNA replication origins by initiation site sequencing (ini-seq). Nucleic Acids Res 44:10230–10247. https://doi.org/10.1093/nar/gkw760
Liachko I, Youngblood RA, Tsui K, Bubb KL, Queitsch C, Raghuraman MK, Nislow C, Brewer BJ, Dunham MJ (2014) GC-rich DNA elements enable replication origin activity in the methylotrophic yeast Pichia pastoris. PLoS Genet 10:e1004169. https://doi.org/10.1371/journal.pgen.1004169
Lombraña R, Álvarez A, Fernández-Justel JM, Almeida R, Poza-Carrión C, Gomes F, Calzada A, Requena JM, Gómez M (2016) Transcriptionally driven DNA replication program of the human parasite Leishmania major. Cell Rep 16:1774–1786. https://doi.org/10.1016/j.celrep.2016.07.007
Mantiero D, Mackenzie A, Donaldson A, Zegerman P (2011) Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30:4805–4814. https://doi.org/10.1038/emboj.2011.404
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. https://doi.org/10.1371/journal.pgen.0030077
Picard F, Cadoret J-C, Audit B, Arneodo A, Alberti A, Battail C, Duret L, Prioleau M-N (2014) The spatiotemporal program of DNA replication is associated with specific combinations of chromatin marks in human cells. PLoS Genet 10:e1004282. https://doi.org/10.1371/journal.pgen.1004282
Prioleau M-N, MacAlpine DM (2016) DNA replication origins-where do we begin? Genes Dev 30:1683–1697. https://doi.org/10.1101/gad.285114.116
Rhodes D, Lipps HJ (2015) G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res 43:8627–8637. https://doi.org/10.1093/nar/gkv862
Rodriguez R, Miller KM, Forment JV, Bradshaw CR, Nikan M, Britton S, Oelschlaegel T, Xhemalce B, Balasubramanian S, Jackson SP (2012) Small-molecule–induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol 8:301–310. https://doi.org/10.1038/nchembio.780
Segurado M, de Luis A, Antequera F (2003) Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4:1048–1053. https://doi.org/10.1038/sj.embor.embor7400008
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. https://doi.org/10.1371/journal.pgen.1000446
Tanaka S, Nakato R, Katou Y, Shirahige K, Araki H (2011) Origin association of Sld3, Sld7, and Cdc45 proteins is a key step for determination of origin-firing timing. Curr Biol 21:2055–2063. https://doi.org/10.1016/j.cub.2011.11.038
Valton A-L, Prioleau M-N (2016) G-Quadruplexes in DNA replication: a problem or a necessity? Trends Genet 32:697–706. https://doi.org/10.1016/j.tig.2016.09.004
Valton A-L, Hassan-Zadeh V, Lema I, Boggetto N, Alberti P, Saintomé C, Riou J-F, Prioleau M-N (2014) G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBO J. https://doi.org/10.1002/embj.201387506
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. https://doi.org/10.3389/fmicb.2014.00735
Wu Z, Liu J, Yang H, Liu H, Xiang H (2014) Multiple replication origins with diverse control mechanisms in Haloarcula hispanica. Nucleic Acids Res 42:2282–2294. https://doi.org/10.1093/nar/gkt1214
Xu J, Yanagisawa Y, Tsankov AM, Hart C, Aoki K, Kommajosyula N, Steinmann KE, Bochicchio J, Russ C, Regev A, Rando OJ, Nusbaum C, Niki H, Milos P, Weng Z, Rhind N (2012) Genome-wide identification and characterization of replication origins by deep sequencing. Genome Biol 13:R27. https://doi.org/10.1186/gb-2012-13-4-r27
Zegerman P (2015) Evolutionary conservation of the CDK targets in eukaryotic DNA replication initiation. Chromosoma 124:309–321. https://doi.org/10.1007/s00412-014-0500-y
Acknowledgments
This work was supported by grants from the Association pour la Recherche sur le Cancer (Equipe labellisée), the Agence Nationale pour la Recherche (ANR-15-CE12-0004-01), and the IdEx Paris Sorbonne to M-N.P. M-N.P is supported by the Inserm.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Prioleau, MN. (2017). G-Quadruplexes and DNA Replication Origins. In: Masai, H., Foiani, M. (eds) DNA Replication. Advances in Experimental Medicine and Biology, vol 1042. Springer, Singapore. https://doi.org/10.1007/978-981-10-6955-0_13
Download citation
DOI: https://doi.org/10.1007/978-981-10-6955-0_13
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-10-6954-3
Online ISBN: 978-981-10-6955-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)