Combinatorial Modeling of Chromatin Features Quantitatively Predicts DNA Replication Timing in Drosophila

PLoS Computational Biology

Volumn 10, Issue 1, 2014, Pages

  Comoglio, Federico ^a   Paro, Renato ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FORECASTING; PROTEINS; TIMING CIRCUITS;

BINDING PROTEINS; CELL TYPES; COMBINATORIAL MODELING; DATA COLLECTION; DNA REPLICATIONS; DROSOPHILLA; GENES EXPRESSION; HISTONE CODES; HISTONE MODIFICATION; TRANSCRIPTIONAL REGULATION;

GENE EXPRESSION;

BINDING PROTEIN;

ACCURACY; ANIMAL CELL; ARTICLE; CELL TYPE; CHROMATIN; CONTROLLED STUDY; DNA REPLICATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE REPLICATION; HISTONE CODE; HISTONE MODIFICATION; INSECT CELL; INSECT GENOME; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; QUANTITATIVE ANALYSIS; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE; CHROMATIN; CLUSTER ANALYSIS; COMPUTER SIMULATION; DNA; DNA REPLICATION TIMING; DROSOPHILA; GENE EXPRESSION REGULATION; GENOME; HISTONES; MODELS, STATISTICAL;

EID: 84896738467     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003419     Document Type: Article

References (65)

1. Masai H, Matsumoto S, You Z, Yoshizawa-Sugata N, Oda M, (2010) Eukaryotic Chromosome DNA Replication: Where, When, and How?. Annu Rev Biochem 79: 89-130.
2. Bechhoefer J, Rhind N, (2012) Replication timing and its emergence from stochastic processes. Trends Genet 28: 374-81.
3. Rhind N, Yang SC, Bechhoefer J, (2010) Reconciling stochastic origin _ring with de_ned replication timing. Chromosome Res 18: 35-43.
4. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, et al. (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6: e245.
5. Hiratani I, Gilbert DM, (2009) Replication timing as an epigenetic mark. Epigenetics 4: 93-97.
6. Goren A, Cedar H, (2003) Replicating by the clock. Nat Rev Mol Cell Biol 4: 25-32.
7. Zhang J, Xu F, Hashimshony T, Keshet I, Cedar H, (2002) Establishment of transcriptional competence in early and late S phase. Nature 420: 198-202.
8. Alabert C, Groth A, (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153-167.
9. Bell SP, Dutta A, (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-74.
10. Yamazaki S, Ishii A, Kanoh Y, Oda M, Nishito Y, et al. (2012) Rif1 regulates the replication timing domains on the human genome. EMBO J 31: 3667-3677.
11. Cornacchia D, Dileep V, Quivy JP, Foti R, Tili F, et al. (2012) Mouse Rif1 is a key regulator of the replication-timing programme in mammalian cells. EMBO J 31: 3678-3690.
12. Hassan-Zadeh V, Chilaka S, Cadoret JC, Ma MK, Boggetto N, et al. (2012) USF binding sequences from the HS4 insulator element impose early replication timing on a vertebrate replicator. PLoS Biol 10: e1001277.
13. Tazumi A, Fukuura M, Nakato R, Kishimoto A, Takenaka T, et al. (2012) Telomere-binding protein Taz1 controls global replication timing through its localization near late replication origins in fission yeast. Genes Dev 26: 2050-2062.
14. Schübeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, et al. (2002) Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32: 438-442.
15. Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, et al. (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21: 164-174.
16. Gilbert DM, (2010) Evaluating genome-scale approaches to eukaryotic DNA replication. Nat Rev Genet 11: 673-684.
17. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, et al. (2010) Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20: 761-770.
18. Bell O, Schwaiger M, Oakeley EJ, Lienert F, Beisel C, et al. (2010) Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat Struct Mol Biol 17: 894-900.
19. Schwaiger M, Schübeler D, (2006) A question of timing: emerging links between transcription and replication. Curr Opin Genet Dev 16: 177-183.
20. Hayashi MT, Masukata H, (2011) Regulation of DNA replication by chromatin structures: accessibility and recruitment. Chromosoma 120: 39-46.
21. Karlic R, Chung HR, Lasserre J, Vlahovicek K, Vingron M, (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci U S A 107: 2926-31.
22. Cheng C, Gerstein M, (2012) Modeling the relative relationship of transcription factor binding and histone modifications to gene expression levels in mouse embryonic stem cells. Nucleic Acids Res 40: 553-568.
23. McLeay R, Lesluyes T, Cuellar Partida G, Bailey TL, (2012) Genome-wide in silico prediction of gene expression. Bioinformatics 28: 2789-2796.
24. Cheng C, Alexander R, Min R, Leng J, Yip KY, et al. (2012) Understanding transcriptional regulation by integrative analysis of transcription factor binding data. Genome Res 22: 1658-67.
25. Dong X, Greven MC, Kundaje A, Djebali S, Brown JB, et al. (2012) Modeling gene expression using chromatin features in various cellular contexts. Genome Biol 13: R53.
26. Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M, (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10: 1223-1233.
27. Lin CM, Fu H, Martinovsky M, Bouhassira E, Aladjem MI, (2003) Dynamic alterations of replication timing in mammalian cells. Curr Biol 13: 1019-1028.
28. Aggarwal BD, Calvi BR, (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature 430: 372-376.
29. Knott SR, Peace JM, Ostrow AZ, Gan Y, Rex AE, et al. (2012) Forkhead transcription factors establish origin timing and long-range clustering in S. cerevisiae. Cell 148: 99-111.
30. Yu Y, Song C, Zhang Q, DiMaggio PA, Garcia BA, et al. (2012) Histone H3 lysine 56 methylation regulates DNA replication through its interaction with PCNA. Mol Cell 46: 7-17.
31. Strahl BD, Allis CD, (2000) The language of covalent histone modifications. Nature 403: 41-45.
32. Turner BM, (2002) Cellular Memory and the Histone Code. Cell 111: 285-291.
33. Suganuma T, Workman JL, (2011) Signals and Combinatorial Functions of Histone Modi_cations. Annu Rev Biochem 80: 473-499.
34. Rando OJ, (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr Opin Genet Dev 22: 148-155.
35. Hastie T, Tibshirani R, Friedman J (2009) The elements of statistical learning. Data mining, inference and prediction (second edition). Springer, New York.
36. Cadoret JC, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C, et al. (2008) Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U S A 105: 15837-15842.
37. Schwaiger M, Stadler MB, Bell O, Kohler H, Oakeley EJ, et al. (2009) Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev 23: 589-601.
38. Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927-930.
39. Sequeira-Mendes J, Daz-Uriarte R, Apedaile A, Huntley D, Brockdorff N, et al. (2009) Transcription Initiation Activity Sets Replication Origin Efficiency in Mammalian Cells. PLoS Genet 5: e1000446.
40. MacAlpine HK, Gordan 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.
41. Deal RB, Henikoff JG, Henikoff S, (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: 1161-1164.
42. Fasulo B, Deuring R, Murawska M, Gause M, Dorighi KM, et al. (2012) The Drosophila MI-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet 8: e1002878.
43. Sawarkar R, Paro R, (2012) Hsp90@chromatin.nucleus: an emerging hub of a networker. Trends Cell Biol 23: 193-201.
44. Sawarkar R, Sievers C, Paro R, (2012) Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149: 807-818.
45. Tibshirani R, (1996) Regression shrinkage and selection via the Lasso. J Roy Statist Soc Ser B 58: 267-288.
46. Efron B, Hastie T, Johnstone I, Tibshirani R, (2004) Least angle regression. Ann Stat 32: 407-499.
47. Zamdborg L, Ma P, (2009) Discovery of proteinDNA interactions by penalized multivariate regression. Nucleic Acids Res 37: 5246-5254.
48. Sakoparnig T, Kockmann T, Paro R, Beisel C, Beerenwinkel N, (2012) Binding Profiles of Chromatin-Modifying Proteins Are Predictive for Transcriptional Activity and Promoter-Proximal Pausing. J Comp Biol 19: 126-138.
49. Sneppen K, Dodd IB, (2012) A simple histone code opens many paths to epigenetics. PLoS Comput Biol 8 (8):: e1002643.
50. Enderle D, Beisel C, Stadler MB, Gerstung M Athri P, et al. (2011) Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res 21: 216-226.
51. Ernst J, Kellis M, (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotech 28: 817-827.
52. Ernst J, Kellis M, (2012) ChromHMM: automating chromatin-state discovery and characterization. Nat Methods 9: 215-216.
53. Kharchenko PV, Alekseyenko AA, SchwartzYB, Minoda A, Riddle NC, et al. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480-485.
54. Zou H, Hastie T, (2005) Regularization and variable selection via the elastic net. J Roy Statist Soc Ser B 67: 301-320.
55. Pryde F, Jain D, Kerr A, Curley R, Mariotti FR, et al. (2009) H3 k36 methylation helps determine the timing of cdc45 association with replication origins. PLoS One 4: e5882.
56. Casas-Delucchi CS, van Bemmel JG, Haase S, Herce HD, Nowak D, (2012) Histone hypoacetylation is required to maintain late replication timing of constitutive heterochromatin. Nucleic Acids Res 40: 159-169.
57. Geng F, Tansey WP, (2008) Polyubiquitylation of histone H2B. Mol Biol Cell 19: 3616-3624.
58. Trujillo KM, Osley MA, (2012) A Role for H2B Ubiquitylation in DNA Replication. Mol Cell 48: 734-746.
59. Chandrasekharan MB, Huang F, Sun ZW, (2009) Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci U S A 10: 16686-16691.
60. Lo Sardo F, Lanzuolo C, Comoglio F, De Bardi M, Paro R, et al. (2013) PcG-Mediated Higher-Order Chromatin Structures Modulate Replication Programs at the Drosophila BX-C. PLoS Genet 9 (2):: e1003283.
61. Tippmann SC, Ivanek R, Gaidatzis D, Schler A, Hoerner L, et al. (2012) Chromatin measurements reveal contributions of synthesis and decay to steady-state mRNA levels,. Mol Syst Biol 8: 593.
62. Friedman JH, (1991) Multivariate Adaptive Regression Splines. Ann Stat 19: 1-67.
63. Lucchesi JC, Kelly WG, Panning B, (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39: 615-651.
64. Durinck S, Spellman PT, Birney E, Huber W, (2009) Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc 4: 1184-1191.
65. Riddle NC, Shaffer CD, Elgin SC, (2009) A lot about a little dot: Lessons learned from Drosophila melanogaster chromosome 4. Biochem Cell Biol 87: 229-241.