Nucleotide Pool Depletion Induces G-Quadruplex-Dependent Perturbation of Gene Expression

Cell Reports

Volumn 13, Issue 11, 2015, Pages 2491-2503

  Papadopoulou, Charikleia ^a   Guilbaud, Guillaume ^a   Schiavone, Davide ^a   Sale, Julian E ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Epigenetic instability; G quadruplexes; Replication stress; Transcriptional memory

Indexed keywords

BLOOM SYNDROME HELICASE; GUANINE QUADRUPLEX; HELICASE; HISTONE H2AX; HYDROXYUREA; NUCLEOTIDE; PROTEIN FANCJ; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN; APHIDICOLIN; DNA; HISTONE; RECQ HELICASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL LINE; CELL STRESS; CHICKEN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEPLETION; DT40 CELL LINE; EPIGENETICS; GENE EXPRESSION; GENE LOCUS; GENETIC STABILITY; HISTONE MODIFICATION; HISTONE PHOSPHORYLATION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE POOL DEPLETION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BIOSYNTHESIS; CHEMISTRY; DNA REPLICATION; DOWN REGULATION; DRUG EFFECTS; GENOMIC INSTABILITY; METABOLISM; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PROMOTER REGION; REPORTER GENE; UPREGULATION;

ANIMALS; APHIDICOLIN; BASE SEQUENCE; CELL LINE; CHICKENS; DNA; DNA REPLICATION; DOWN-REGULATION; G-QUADRUPLEXES; GENES, REPORTER; GENETIC LOCI; GENOMIC INSTABILITY; HISTONES; HYDROXYUREA; NUCLEOTIDES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RECQ HELICASES; UP-REGULATION;

EID: 84952875156     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.039     Document Type: Article

References (48)

1. Alvino G.M., Collingwood D., Murphy J.M., Delrow J., Brewer B.J., Raghuraman M.K. Replication in hydroxyurea: it's a matter of time. Mol. Cell. Biol. 2007, 27:6396-6406.
2. Anglana M., Apiou F., Bensimon A., Debatisse M. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 2003, 114:385-394.
3. Ayrapetov M.K., Gursoy-Yuzugullu O., Xu C., Xu Y., Price B.D. DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc. Natl. Acad. Sci. USA 2014, 111:9169-9174.
4. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.-V.F., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
5. Bauer D.E., Kamran S.C., Lessard S., Xu J., Fujiwara Y., Lin C., Shao Z., Canver M.C., Smith E.C., Pinello L., et al. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level. Science 2013, 342:253-257.
6. Berdasco M., Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev. Cell 2010, 19:698-711.
7. Berger S.L., Kouzarides T., Shiekhattar R., Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009, 23:781-783.
8. Bester A.C., Roniger M., Oren Y.S., Im M.M., Sarni D., Chaoat M., Bensimon A., Zamir G., Shewach D.S., Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145:435-446.
9. Byun T.S., Pacek M., Yee M.-C., Walter J.C., Cimprich K.A. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 2005, 19:1040-1052.
10. De S., Michor F. DNA secondary structures and epigenetic determinants of cancer genome evolution. Nat. Struct. Mol. Biol. 2011, 18:950-955.
11. Di Micco R., Fumagalli M., Cicalese A., Piccinin S., Gasparini P., Luise C., Schurra C., Garre' M., Nuciforo P.G., Bensimon A., et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444:638-642.
12. Flanagan J.M., Steward S., Howard T.A., Mortier N.A., Kimble A.C., Aygun B., Hankins J.S., Neale G.A., Ware R.E. Hydroxycarbamide alters erythroid gene expression in children with sickle cell anaemia. Br. J. Haematol. 2012, 157:240-248.
13. Gautier L., Cope L., Bolstad B.M., Irizarry R.A. affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315.
14. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5:R80.
15. Guilbaud G., Rappailles A., Baker A., Chen C.-L., Arneodo A., Goldar A., d'Aubenton-Carafa Y., Thermes C., Audit B., Hyrien O. Evidence for sequential and increasing activation of replication origins along replication timing gradients in the human genome. PLoS Comput. Biol. 2011, 7:e1002322.
16. Halazonetis T.D., Gorgoulis V.G., Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008, 319:1352-1355.
17. Hansen K.D., Timp W., Bravo H.C., Sabunciyan S., Langmead B., McDonald O.G., Wen B., Wu H., Liu Y., Diep D., et al. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 2011, 43:768-775.
18. Huang W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
19. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
20. Jasencakova Z., Groth A. Replication stress, a source of epigenetic aberrations in cancer?. BioEssays 2010, 32:847-855.
21. Jasencakova Z., Scharf A.N.D., Ask K., Corpet A., Imhof A., Almouzni G., Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 2010, 37:736-743.
22. Letessier A., Millot G.A., Koundrioukoff S., Lachagès A.-M., Vogt N., Hansen R.S., Malfoy B., Brison O., Debatisse M. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 2011, 470:120-123.
23. Maizels N., Gray L.T. The G4 genome. PLoS Genet. 2013, 9:e1003468.
24. Neelsen K.J., Zanini I.M.Y., Herrador R., Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 2013, 200:699-708.
25. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
26. Nicoludis J.M., Barrett S.P., Mergny J.-L., Yatsunyk L.A. Interaction of human telomeric DNA with N-methyl mesoporphyrin IX. Nucleic Acids Res. 2012, 40:5432-5447.
27. Oguro M., Suzuki-Hori C., Nagano H., Mano Y., Ikegami S. The mode of inhibitory action by aphidicolin on eukaryotic DNA polymerase alpha. Eur. J. Biochem. 1979, 97:603-607.
28. Pacek M., Walter J.C. A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J. 2004, 23:3667-3676.
29. Pacek M., Tutter A.V., Kubota Y., Takisawa H., Walter J.C. Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell 2006, 21:581-587.
30. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
31. Piazza A., Serero A., Boulé J.-B., Legoix-Né P., Lopes J., Nicolas A. Stimulation of gross chromosomal rearrangements by the human CEB1 and CEB25 minisatellites in Saccharomyces cerevisiae depends on G-quadruplexes or Cdc13. PLoS Genet. 2012, 8:e1003033.
32. Platt O.S., Orkin S.H., Dover G., Beardsley G.P., Miller B., Nathan D.G. Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia. J. Clin. Invest. 1984, 74:652-656.
33. Poli J., Tsaponina O., Crabbé L., Keszthelyi A., Pantesco V., Chabes A., Lengronne A., Pasero P. dNTP pools determine fork progression and origin usage under replication stress. EMBO J. 2012, 31:883-894.
34. Ren J., Chaires J.B. Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry 1999, 38:16067-16075.
35. Ribeyre C., Lopes J., Boulé J.-B., Piazza A., Guédin A., Zakian V.A., Mergny J.-L., Nicolas A. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet. 2009, 5:e1000475.
36. Rodriguez R., Miller K.M., Forment J.V., Bradshaw C.R., Nikan M., Britton S., Oelschlaegel T., Xhemalce B., Balasubramanian S., Jackson S.P. Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat. Chem. Biol. 2012, 8:301-310.
37. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
38. Sarkies P., Sale J.E. Cellular epigenetic stability and cancer. Trends Genet. 2012, 28:118-127.
39. Sarkies P., Reams C., Simpson L.J., Sale J.E. Epigenetic instability due to defective replication of structured DNA. Mol. Cell 2010, 40:703-713.
40. Sarkies P., Murat P., Phillips L.G., Patel K.J., Balasubramanian S., Sale J.E. FANCJ coordinates two pathways that maintain epigenetic stability at G-quadruplex DNA. Nucleic Acids Res. 2012, 40:1485-1498.
41. Schiavone D., Guilbaud G., Murat P., Papadopoulou C., Sarkies P., Prioleau M.-N., Balasubramanian S., Sale J.E. Determinants of G quadruplex-induced epigenetic instability in REV1-deficient cells. EMBO J. 2014, 33:2507-2520.
42. Schwab R.A., Nieminuszczy J., Shin-ya K., Niedzwiedz W. FANCJ couples replication past natural fork barriers with maintenance of chromatin structure. J. Cell Biol. 2013, 201:33-48.
43. Shanbhag N.M., Rafalska-Metcalf I.U., Balane-Bolivar C., Janicki S.M., Greenberg R.A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 2010, 141:970-981.
44. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3. Article 3.
45. Timp W., Feinberg A.P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 2013, 13:497-510.
46. Tsantoulis P.K., Kotsinas A., Sfikakis P.P., Evangelou K., Sideridou M., Levy B., Mo L., Kittas C., Wu X.-R., Papavassiliou A.G., Gorgoulis V.G. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene 2008, 27:3256-3264.
47. Wickramasinghe C.M., Arzouk H., Frey A., Maiter A., Sale J.E. Contributions of the specialised DNA polymerases to replication of structured DNA. DNA Repair (Amst.) 2015, 29:83-90.
48. Zeman M.K., Cimprich K.A. Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16:2-9.