Advertisement

G-Quadruplexes and DNA Replication Origins

  • Marie-Noëlle PrioleauEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1042)

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.

Keywords

Replication origin G-quadruplex Chromatin Evolution 

Notes

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.

References

  1. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Berezney R, Dubey DD, Huberman JA (2000) Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108:471–484CrossRefPubMedGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. Bielinsky AK, Gerbi SA (1998) Discrete start sites for DNA synthesis in the yeast ARS1 origin. Science 279:95–98CrossRefPubMedGoogle Scholar
  5. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 96:2656–2661CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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
  23. 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
  24. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kelman LM, Kelman Z (2014) Archaeal DNA replication. Annu Rev Genet 48:71–97. https://doi.org/10.1146/annurev-genet-120213-092148 CrossRefPubMedGoogle Scholar
  29. 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 PubMedPubMedCentralGoogle Scholar
  30. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 CrossRefPubMedGoogle Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. 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
  43. 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 PubMedGoogle Scholar
  44. 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 CrossRefPubMedGoogle Scholar
  45. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Institut Jacques Monod, CNRS UMR7592, Université Paris Diderot, Equipe Labellisée Association pour la Recherche sur le CancerParisFrance

Personalised recommendations