Contribution of Sequence Motif, Chromatin State, and DNA Structure Features to Predictive Models of Transcription Factor Binding in Yeast

PLoS Computational Biology

Volumn 11, Issue 8, 2015, Pages

  Tsai, Zing Tsung Yeh ^a,b   Shiu, Shin Han ^b   Tsai, Huai Kuang ^a  

^a INSTITUTE OF INFORMATION SCIENCE   (Taiwan)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; DNA; DNA SEQUENCES; FORECASTING; FREE ENERGY; LEARNING SYSTEMS; TRANSCRIPTION; YEAST;

DNA STRUCTURE; DNA-BINDING DOMAIN; INTRINSIC PROPERTY; PREDICTIVE MODELS; PROPERTY MODELS; SEQUENCE MOTIFS; SPECIFIC BINDING; STRUCTURE FEATURES; TRANSCRIPTION FACTOR BINDING; TRANSCRIPTION FACTOR BINDING SITES;

TRANSCRIPTION FACTORS;

ACCURACY; ANALYTICAL PARAMETERS; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN STATE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CLASSIFICATION; CLASSIFIER; COMPUTER MODEL; CONTROLLED STUDY; DINUCLEOTIDE FREE ENERGY; DNA BINDING DOMAIN; DNA STRUCTURE; FEASIBILITY STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTONE MODIFICATION; INTRINSIC PROPERTY MODEL; MAJOR GROOVE GEOMETRY; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME OCCUPANCY; PREDICTIVE VALUE; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; RANDOM FOREST; SEQUENCE MOTIF; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION FACTOR AGNOSTIC PREDICTIVE MODEL; TRANSCRIPTION FACTOR BINDING; YEAST; BIOLOGY; CHEMISTRY; CHROMATIN; GENETICS; METABOLISM; NUCLEOTIDE MOTIF; SACCHAROMYCES CEREVISIAE;

CHROMATIN; FUNGAL DNA; FUNGAL PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

CHROMATIN; COMPUTATIONAL BIOLOGY; DNA, FUNGAL; FUNGAL PROTEINS; NUCLEOTIDE MOTIFS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS;

EID: 84940757344     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004418     Document Type: Article

References (72)

1. Weirauch MT, Cote A, Norel R, Annala M, Zhao Y, Riley TR, et al. Evaluation of methods for modeling transcription factor sequence specificity. Nat Biotechnol. Nature Publishing Group; 2013;31: 126–34. doi: 10.1038/nbt.2486 23354101
2. Bulyk ML, Computational prediction of transcription-factor binding site locations. Genome Biol. 2003;5: 201. 14709165
3. Tompa M, Li N, Bailey TL, Church GM, De Moor B, Eskin E, et al. Assessing computational tools for the discovery of transcription factor binding sites. Nat Biotechnol. 2005;23: 137–44. 15637633
4. Wunderlich Z, Mirny LA, Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet. 2009;25: 429–34.
5. Slattery M, Zhou T, Yang L, Dantas Machado AC, Gordân R, Rohs R, Absence of a simple code: how transcription factors read the genome. Trends Biochem Sci. 2014;39: 381–399. doi: 10.1016/j.tibs.2014.07.002 25129887
6. Hannenhalli S, Eukaryotic transcription factor binding sites—modeling and integrative search methods. Bioinformatics. 2008;24: 1325–31. doi: 10.1093/bioinformatics/btn198 18426806
7. Cuellar Partida G, Buske F a, McLeay RC, Whitington T, Noble WS, Bailey TL, Epigenetic priors for identifying active transcription factor binding sites. Bioinformatics. 2011;28: 56–62. doi: 10.1093/bioinformatics/btr614 22072382
8. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, et al. The accessible chromatin landscape of the human genome. Nature. Nature Publishing Group; 2012;489: 75–82. doi: 10.1038/nature11232 22955617
9. Pique-Regi R, Degner JF, Pai A a, Gaffney DJ, Gilad Y, Pritchard JK, Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res. 2011;21: 447–55. doi: 10.1101/gr.112623.110 21106904
10. Tewari AK, Yardimci GG, Shibata Y, Sheffield NC, Song L, Taylor BS, et al. Chromatin accessibility reveals insights into androgen receptor activation and transcriptional specificity. Genome Biol. BioMed Central Ltd; 2012;13.
11. Natarajan A, Yardimci GG, Sheffield NC, Crawford GE, Ohler U, Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res. 2012;22: 1711–22. doi: 10.1101/gr.135129.111 22955983
12. Hihara S, Pack C, Kaizu K, Tani T, Hanafusa T, Nozaki T, Local Nucleosome Dynamics Facilitate Chromatin Accessibility in Living Mammalian Cells. CellReports. The Authors; 2012;2: 1645–1656.
13. Arvey A, Agius P, Noble WS, Leslie C, Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Res. 2012;22: 1723–34. doi: 10.1101/gr.127712.111 22955984
14. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012;22: 1798–1812. doi: 10.1101/gr.139105.112 22955990
15. He HH, Meyer C a, Chen MW, Jordan VC, Brown M, Liu XS, Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res. 2012;22: 1015–25. doi: 10.1101/gr.133280.111 22508765
16. Li X-Y, Thomas S, Sabo PJ, Eisen MB, Stamatoyannopoulos J a, Biggin MD, The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol. BioMed Central Ltd; 2011;12: R34. doi: 10.1186/gb-2011-12-4-r34 21473766
17. Lickwar CR, Mueller F, Hanlon SE, McNally JG, Lieb JD, Genome-wide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function. Nature. Nature Publishing Group; 2012;484: 251–5. doi: 10.1038/nature10985 22498630
18. Steinfeld I, Shamir R, Kupiec M, A genome-wide analysis in Saccharomyces cerevisiae demonstrates the influence of chromatin modifiers on transcription. Nat Genet. 2007;39: 303–9. 17325681
19. Henikoff S, Shilatifard A, Histone modification: cause or cog? Trends Genet. Elsevier Ltd; 2011;27: 389–96. doi: 10.1016/j.tig.2011.06.006 21764166
20. Zentner GE, Henikoff S, Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol. Nature Publishing Group; 2013;20: 259–266. doi: 10.1038/nsmb.2470 23463310
21. Kaplan T, Li X-Y, Sabo PJ, Thomas S, Stamatoyannopoulos J a, Biggin MD, et al. Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet. 2011;7: e1001290. doi: 10.1371/journal.pgen.1001290 21304941
22. Cheng Q, Kazemian M, Pham H, Blatti C, Celniker SE, Wolfe S a, et al. Computational identification of diverse mechanisms underlying transcription factor-DNA occupancy. PLoS Genet. 2013;9: e1003571. doi: 10.1371/journal.pgen.1003571 23935523
23. Blatti C, Sinha S, Motif enrichment tool. Nucleic Acids Res. 2014;42: W20–5. doi: 10.1093/nar/gku456 24860165
24. Parker SCJ, Hansen L, Abaan HO, Tullius TD, Margulies EH, Local DNA topography correlates with functional noncoding regions of the human genome. Science. 2009;324: 389–392. doi: 10.1126/science.1169050 19286520
25. Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, Rastas P, et al. DNA-Binding Specificities of Human Transcription Factors. Cell. Elsevier Inc.; 2013;152: 327–339. doi: 10.1016/j.cell.2012.12.009 23332764
26. Gordân R, Shen N, Dror I, Zhou T, Horton J, Rohs R, et al. Genomic Regions Flanking E-Box Binding Sites Influence DNA Binding Specificity of bHLH Transcription Factors through DNA Shape. Cell Rep. 2013;3: 1093–1104. doi: 10.1016/j.celrep.2013.03.014 23562153
27. Heddi B, Oguey C, Lavelle C, Foloppe N, Hartmann B, Intrinsic flexibility of B-DNA: The experimental TRX scale. Nucleic Acids Res. 2009;38: 1034–1047. doi: 10.1093/nar/gkp962 19920127
28. Meysman P, Dang TH, Laukens K, De Smet R, Wu Y, Marchal K, et al. Use of structural DNA properties for the prediction of transcription-factor binding sites in Escherichia coli. Nucleic Acids Res. 2011;39: e6. doi: 10.1093/nar/gkq1071 21051340
29. Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, Rastas P, et al. DNA-Binding Specificities of Human Transcription Factors. Cell. Elsevier Inc.; 2013;152: 327–339. doi: 10.1016/j.cell.2012.12.009 23332764
30. Cheng C, Shou C, Yip KY, Gerstein MB, Genome-wide analysis of chromatin features identifies histone modification sensitive and insensitive yeast transcription factors. Genome Biol. BioMed Central Ltd; 2011;12: R111. doi: 10.1186/gb-2011-12-11-r111 22060676
31. Wang J, Computational study of associations between histone modification and protein-DNA binding in yeast genome by integrating diverse information. BMC Genomics. BioMed Central Ltd; 2011;12: 172. doi: 10.1186/1471-2164-12-172 21457549
32. Ramsey S a, Knijnenburg T a, Kennedy K a, Zak DE, Gilchrist M, Gold ES, et al. Genome-wide histone acetylation data improve prediction of mammalian transcription factor binding sites. Bioinformatics. 2010;26: 2071–5. doi: 10.1093/bioinformatics/btq405 20663846
33. Narlikar L, Gordan R, Hartemink AJ, A Nucleosome-Guided Map of Transcription Factor Binding Sites in Yeast. PLoS Comput Biol. 2007;3: 2199–2208.
34. Won K-J, Ren B, Wang W, Genome-wide prediction of transcription factor binding sites using an integrated model. Genome Biol. 2010;11: R7. doi: 10.1186/gb-2010-11-1-r7 20096096
35. Talebzadeh M, Zare-Mirakabad F, Transcription factor binding sites prediction based on modified nucleosomes. PLoS One. 2014;9: e89226. doi: 10.1371/journal.pone.0089226 24586611
36. Hooghe B, Broos S, van Roy F, De Bleser P, A flexible integrative approach based on random forest improves prediction of transcription factor binding sites. Nucleic Acids Res. 2012;40.
37. Maienschein-Cline M, Dinner AR, Hlavacek WS, Mu F, Improved predictions of transcription factor binding sites using physicochemical features of DNA. Nucleic Acids Res. 2012;40: e175. doi: 10.1093/nar/gks771 22923524
38. Bauer AL, Hlavacek WS, Unkefer PJ, Mu F, Using sequence-specific chemical and structural properties of DNA to predict transcription factor binding sites. PLoS Comput Biol. 2010;6: e1001007. doi: 10.1371/journal.pcbi.1001007 21124945
39. Venters BJ, Wachi S, Mavrich TN, Andersen BE, Jena P, Sinnamon AJ, et al. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell. Elsevier Inc.; 2011;41: 480–92. doi: 10.1016/j.molcel.2011.01.015 21329885
40. Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y, Moore IK, et al. A genomic code for nucleosome positioning. Nature. 2006;442: 772–8. 16862119
41. Friedel M, Nikolajewa S, Sühnel J, Wilhelm T, DiProDB: a database for dinucleotide properties. Nucleic Acids Res. 2009;37: D37–40. doi: 10.1093/nar/gkn597 18805906
42. Ernst J, Plasterer HL, Simon I, Bar-Joseph Z, Integrating multiple evidence sources to predict transcription factor binding in the human genome. Genome Res. 2010;20: 526–36. doi: 10.1101/gr.096305.109 20219943
43. Spivak AT, Stormo GD, ScerTF: a comprehensive database of benchmarked position weight matrices for Saccharomyces species. Nucleic Acids Res. 2012;40: D162–8. doi: 10.1093/nar/gkr1180 22140105
44. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell. 2005;122: 517–27. 16122420
45. Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature. 2007;446: 572–6. 17392789
46. Yuan G-C, Liu Y-J, Dion MF, Slack MD, Wu LF, Altschuler SJ, et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science. 2005;309: 626–30. 15961632
47. Karlić R, Chung H-R, Lasserre J, Vlahovicek K, Vingron M, Histone modification levels are predictive for gene expression. Proc Natl Acad Sci U S A. 2010;107: 2926–31. doi: 10.1073/pnas.0909344107 20133639
48. Meysman P, Marchal K, Engelen K, DNA structural properties in the classification of genomic transcription regulation elements. Bioinform Biol Insights. 2012;6: 155–68. doi: 10.4137/BBI.S9426 22837642
49. Cao X-Q, Zeng J, Yan H, Structural property of regulatory elements in human promoters. Phys Rev E. 2008;77: 041908.
50. Stella S, Cascio D, Johnson RC, The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev. 2010;24: 814–26. doi: 10.1101/gad.1900610 20395367
51. Gotea V, Visel A, Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I, Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res. 2010;20: 565–577. doi: 10.1101/gr.104471.109 20363979
52. Lifanov AP, Makeev VJ, Nazina AG, Papatsenko D a, Homotypic regulatory clusters in Drosophila. Genome Res. 2003;13: 579–88. 12670999
53. Breiman LEO, Random Forests. Mach Learn. 2001;45: 5–32.
54. Koudelka GB, Mauro S a, Ciubotaru M, Indirect readout of DNA sequence by proteins: the roles of DNA sequence-dependent intrinsic and extrinsic forces. Prog Nucleic Acid Res Mol Biol. 2006;81: 143–77. 16891171
55. Sherwood RI, Hashimoto T, O’Donnell CW, Lewis S, Barkal A a, van Hoff JP, et al. Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat Biotechnol. Nature Publishing Group; 2014;32: 171–8. doi: 10.1038/nbt.2798 24441470
56. Venters BJ, Pugh BF. A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. 2009; 360–371.
57. Rhee HS, Pugh BF, Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell. Elsevier Inc.; 2011;147: 1408–19. doi: 10.1016/j.cell.2011.11.013 22153082
58. Zhou X, O’Shea EK, Integrated Approaches Reveal Determinants of Genome-wide Binding and Function of the Transcription Factor Pho4. Mol Cell. Elsevier Inc.; 2011;42: 826–836. doi: 10.1016/j.molcel.2011.05.025 21700227
59. Kasinathan S, Orsi G a, Zentner GE, Ahmad K, Henikoff S, High-resolution mapping of transcription factor binding sites on native chromatin. Nat Methods. 2014;11: 203–9. doi: 10.1038/nmeth.2766 24336359
60. Knight B, Kubik S, Ghosh B, Bruzzone MJ, Geertz M, Martin V, et al. Two distinct promoter architectures centered on dynamic nucleosomes control ribosomal protein gene transcription. Genes Dev. 2014;28: 1695–1709. doi: 10.1101/gad.244434.114 25085421
61. Johnson DS, Mortazavi A, Myers RM, Wold B, Genome-wide mapping of in vivo protein-DNA interactions. Science. 2007;316: 1497–502. 17540862
62. Irie T, Park S-J, Yamashita R, Seki M, Yada T, Sugano S, et al. Predicting promoter activities of primary human DNA sequences. Nucleic Acids Res. 2011;39: e75–e75. doi: 10.1093/nar/gkr173 21486745
63. McLeay RC, Lesluyes T, Cuellar Partida G, Bailey TL, Genome-wide in silico prediction of gene expression. Bioinformatics. 2012;28: 2789–96. doi: 10.1093/bioinformatics/bts529 22954627
64. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, et al. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell. 1998;9: 3273–97. 9843569
65. Ronen M, Botstein D, Transcriptional response of steady-state yeast cultures to transient perturbations in carbon source. Proc Natl Acad Sci U S A. 2006;103: 389–94. 16381818
66. Chu S, DeRisi J, Eisen M, Mulholland J, Boststein D, Brown PO, et al. The Transcriptional Program of Sporulation in Budding Yeast. Science. 1998;282: 699–705. 9784122
67. Gasch a P, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell. 2000;11: 4241–57. 11102521
68. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, et al. Transcriptional regulatory code of a eukaryotic genome. 2004; 99–104.
69. Turatsinze J-V, Thomas-Chollier M, Defrance M, van Helden J, Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nat Protoc. 2008;3: 1578–88. doi: 10.1038/nprot.2008.97 18802439
70. Liaw A, Wiener M, Classification and Regression by randomForest. R News. 2002;2: 18–22.
71. Sing T, Sander O, Beerenwinkel N, Lengauer T, ROCR: visualizing classifier performance in R. Bioinformatics. 2005;21: 3940–1. 16096348
72. Shi Y, Mitchell T, Bar-Joseph Z, Inferring pairwise regulatory relationships from multiple time series datasets. Bioinformatics. 2007;23: 755–63. 17237067