Enhancer identification in mouse embryonic stem cells using integrative modeling of chromatin and genomic features

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Chen, Chih Yu ^a   Morris, Quaid ^b   Mitchell, Jennifer A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Chip seq; Embryonic stem cells; Enhancer; Histone methylation; Regulation of gene expression; Transcription factor

Indexed keywords

CELL PROTEIN; COHESIN; E1A ASSOCIATED P300 PROTEIN; HISTONE H3; LYSINE; LYSINE 27; LYSINE 4; MED12 PROTEIN; MYC PROTEIN; NIPBL PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; EP300 PROTEIN, MOUSE; HISTONE; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 4; MED12 PROTEIN, MOUSE; MEDIATOR COMPLEX; NIPBL PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL SPECIFICITY; CELL TYPE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; EMBRYO; EMBRYONIC STEM CELL; ENHANCER REGION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCUS; GENOME; HISTONE MODIFICATION; METHYLATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ANIMALS; CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; E1A-ASSOCIATED P300 PROTEIN; EMBRYONIC STEM CELLS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENOME; HISTONES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MEDIATOR COMPLEX; MICE; MODELS, GENETIC; OCTAMER TRANSCRIPTION FACTOR-3; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MYC; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84862163181     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-152     Document Type: Article

References (98)

1. Kharchenko PV, Tolstorukov MY, Park PJ. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 2008, 26:1351-1359.
2. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev Cell 2009, 16:47-57.
3. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R. Interchromosomal interactions and olfactory receptor choice. Cell 2006, 126:403-413.
4. Tuan DY, Solomon WB, London IM, Lee DP. An erythroid-specific, developmental-stage-independent enhancer far upstream of the human " beta-like globin" genes. Proc Natl Acad Sci U S A 1989, 86:2554-2558.
5. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
6. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, et al. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009, 462:58-64.
7. Yu M, Riva L, Xie H, Schindler Y, Moran TB, Cheng Y, Yu D, Hardison R, Weiss MJ, Orkin SH, et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 2009, 36:682-695.
8. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
9. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
10. Visel A, Rubin EM, Pennacchio LA. Genomic views of distant-acting enhancers. Nature 2009, 461:199-205.
11. Wingender E, Dietze P, Karas H, Knuppel R. TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res 1996, 24:238-241.
12. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010, 38:D105-D110.
13. Aerts S, van Helden J, Sand O, Hassan BA. Fine-tuning enhancer models to predict transcriptional targets across multiple genomes. PLoS One 2007, 2:e1115.
14. Berman BP, Pfeiffer BD, Laverty TR, Salzberg SL, Rubin GM, Eisen MB, Celniker SE. Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol 2004, 5:R61.
15. Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E, Taipale J. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 2006, 124:47-59.
16. Palin K, Taipale J, Ukkonen E. Locating potential enhancer elements by comparative genomics using the EEL software. Nat Protoc 2006, 1:368-374.
17. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD, et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
18. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Afzal V, Rubin EM, Pennacchio LA. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet 2008, 40:158-160.
19. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007, 39:311-318.
20. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL, Natoli G. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 2010, 8:e1000384.
21. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
22. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
23. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet 2010, 42:806-810.
24. He A, Kong SW, Ma Q, Pu WT. Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc Natl Acad Sci U S A 2011, 108:5632-5637.
25. Friedman J, Hastie T, Tibshirani R. Regularization Paths for Generalized Linear Models via Coordinate Descent. J Stat Softw 2010, 33:1-22.
26. Tibshirani R. Regression shrinkage and selection via the Lasso. J Roy Stat Soc B Met 1996, 58:267-288.
27. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, Weng Z. Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 2004, 32:1372-1381.
28. Goren A, Ozsolak F, Shoresh N, Ku M, Adli M, Hart C, Gymrek M, Zuk O, Regev A, Milos PM, Bernstein BE. Chromatin profiling by directly sequencing small quantities of immunoprecipitated DNA. Nat Methods 2010, 7:47-49.
29. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
30. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
31. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15:1034-1050.
32. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28:503-510.
33. Miller W, Rosenbloom K, Hardison RC, Hou M, Taylor J, Raney B, Burhans R, King DC, Baertsch R, Blankenberg D, et al. 28-way vertebrate alignment and conservation track in the UCSC Genome Browser. Genome Res 2007, 17:1797-1808.
34. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987, 196:261-282.
35. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A, et al. The UCSC Genome Browser database: update 2011. Nucleic Acids Res 2010, 39:D876-882.
36. Won KJ, Ren B, Wang W. Genome-wide prediction of transcription factor binding sites using an integrated model. Genome Biol 2010, 11:R7.
37. Schnetz MP, Handoko L, Akhtar-Zaidi B, Bartels CF, Pereira CF, Fisher AG, Adams DJ, Flicek P, Crawford GE, Laframboise T, et al. CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 2010, 6:e1001023.
38. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
39. Miles J, Mitchell JA, Chakalova L, Goyenechea B, Osborne CS, O'Neill L, Tanimoto K, Engel JD, Fraser P. Intergenic transcription, cell-cycle and the developmentally regulated epigenetic profile of the human beta-globin locus. PLoS One 2007, 2:e630.
40. Gribnau J, Diderich K, Pruzina S, Calzolari R, Fraser P. Intergenic transcription and developmental remodeling of chromatin subdomains in the human beta-globin locus. Mol Cell 2000, 5:377-386.
41. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227.
42. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
43. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
44. Merico D, Isserlin R, Stueker O, Emili A, Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 2010, 5:e13984.
45. Inoue M, Kamachi Y, Matsunami H, Imada K, Uchikawa M, Kondoh H. PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 2007, 12:1049-1061.
46. Takemoto T, Uchikawa M, Yoshida M, Bell DM, Lovell-Badge R, Papaioannou VE, Kondoh H. Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 2011, 470:394-398.
47. Catena R, Tiveron C, Ronchi A, Porta S, Ferri A, Tatangelo L, Cavallaro M, Favaro R, Ottolenghi S, Reinbold R, et al. Conserved POU binding DNA sites in the Sox2 upstream enhancer regulate gene expression in embryonic and neural stem cells. J Biol Chem 2004, 279:41846-41857.
48. Sikorska M, Sandhu JK, Deb-Rinker P, Jezierski A, Leblanc J, Charlebois C, Ribecco-Lutkiewicz M, Bani-Yaghoub M, Walker PR. Epigenetic modifications of SOX2 enhancers, SRR1 and SRR2, correlate with in vitro neural differentiation. J Neurosci Res 2008, 86:1680-1693.
49. Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 2003, 4:509-519.
50. Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M, Okuda A. Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex. Nucleic Acids Res 2002, 30:3202-3213.
51. Lichner Z, Pall E, Kerekes A, Pallinger E, Maraghechi P, Bosze Z, Gocza E. The miR-290-295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation 2011, 81:11-24.
52. Zovoilis A, Smorag L, Pantazi A, Engel W. Members of the miR-290 cluster modulate in vitro differentiation of mouse embryonic stem cells. Differentiation 2009, 78:69-78.
53. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
54. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473:398-402.
55. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011, 8:200-213.
56. Lim LS, Loh YH, Zhang W, Li Y, Chen X, Wang Y, Bakre M, Ng HH, Stanton LW. Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol Biol Cell 2007, 18:1348-1358.
57. Xu J, Watts JA, Pope SD, Gadue P, Kamps M, Plath K, Zaret KS, Smale ST. Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cells. Genes Dev 2009, 23:2824-2838.
58. Marin M, Karis A, Visser P, Grosveld F, Philipsen S. Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell 1997, 89:619-628.
59. Lim LS, Hong FH, Kunarso G, Stanton LW. The pluripotency regulator Zic3 is a direct activator of the Nanog promoter in ESCs. Stem Cells 2010, 28:1961-1969.
60. Leung L, Kwong M, Hou S, Lee C, Chan JY. Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J Biol Chem 2003, 278:48021-48029.
61. Melin F, Miranda M, Montreau N, DePamphilis ML, Blangy D. Transcription enhancer factor-1 (TEF-1) DNA binding sites can specifically enhance gene expression at the beginning of mouse development. EMBO J 1993, 12:4657-4666.
62. Delacroix L, Moutier E, Altobelli G, Legras S, Poch O, Choukrallah MA, Bertin I, Jost B, Davidson I. Cell-specific interaction of retinoic acid receptors with target genes in mouse embryonic fibroblasts and embryonic stem cells. Mol Cell Biol 30:231-244.
63. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 2006, 20:3475-3486.
64. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Noda T, Mikoshiba K. Mouse Zic1 is involved in cerebellar development. J Neurosci 1998, 18:284-293.
65. Aruga J. The role of Zic genes in neural development. Mol Cell Neurosci 2004, 26:205-221.
66. Bensinger SJ, Tontonoz P. A Nurr1 pathway for neuroprotection. Cell 2009, 137:26-28.
67. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009, 4:80-93.
68. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
69. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. From the Cover: Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 2010, 107:21931-21936.
70. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, Chan ET, Metzler G, Vedenko A, Chen X, et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
71. Zentner GE. Tesar PJ 2011, Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res, Scacheri PC.
72. Pasini D, Malatesta M, Jung HR, Walfridsson J, Willer A, Olsson L, Skotte J, Wutz A, Porse B, Jensen ON, Helin K. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res 2010, 38:4958-4969.
73. Conaway RC, Conaway JW. Function and regulation of the Mediator complex. Curr Opin Genet Dev 2011, 21:225-230.
74. Boube M, Joulia L, Cribbs DL, Bourbon HM. Evidence for a mediator of RNA polymerase II transcriptional regulation conserved from yeast to man. Cell 2002, 110:143-151.
75. Knuesel MT, Meyer KD, Bernecky C, Taatjes DJ. The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev 2009, 23:439-451.
76. Tutter AV, Kowalski MP, Baltus GA, Iourgenko V, Labow M, Li E, Kadam S. Role for Med12 in regulation of Nanog and Nanog target genes. J Biol Chem 2009, 284:3709-3718.
77. Rollins RA, Korom M, Aulner N, Martens A, Dorsett D. Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol 2004, 24:3100-3111.
78. Rollins RA, Morcillo P, Dorsett D. Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 1999, 152:577-593.
79. Firpi HA, Ucar D, Tan K. Discover regulatory DNA elements using chromatin signatures and artificial neural network. Bioinformatics 2010, 26:1579-1586.
80. 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, 20:526-536.
81. Narlikar L, Sakabe NJ, Blanski AA, Arimura FE, Westlund JM, Nobrega MA, Ovcharenko I. Genome-wide discovery of human heart enhancers. Genome Res 2010, 20:381-392.
82. Ernst J, Kellis M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotechnol 2010, 28:817-825.
83. Hon G, Ren B, Wang W. ChromaSig: a probabilistic approach to finding common chromatin signatures in the human genome. PLoS Comput Biol 2008, 4:e1000201.
84. Pekowska A, Benoukraf T, Zacarias-Cabeza J, Belhocine M, Koch F, Holota H, Imbert J, Andrau JC, Ferrier P, Spicuglia S. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J 2011, 30:4198-4210.
85. Pekowska A, Benoukraf T, Ferrier P, Spicuglia S. A unique H3K4me2 profile marks tissue-specific gene regulation. Genome Res 2010, 20:1493-1502.
86. Ong CT, Corces VG. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet 2011, 12:283-293.
87. Carter D, Chakalova L, Osborne CS, Dai YF, Fraser P. Long-range chromatin regulatory interactions in vivo. Nat Genet 2002, 32:623-626.
88. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 2002, 10:1453-1465.
89. Pesce M, Marin Gomez M, Philipsen S, Scholer HR. Binding of Sp1 and Sp3 transcription factors to the Oct-4 gene promoter. Cell Mol Biol (Noisy-le-grand) 1999, 45:709-716.
90. Wu DY, Yao Z. Functional analysis of two Sp1/Sp3 binding sites in murine Nanog gene promoter. Cell Res 2006, 16:319-322.
91. Gentleman RC, Carey VJ, Bates DM, 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.
92. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, et al. NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 2010, 39:D1005-D1010.
93. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
94. Jothi R, Cuddapah S, Barski A, Cui K, Zhao K. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res 2008, 36:5221-5231.
95. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
96. Ouyang Z, Zhou Q, Wong WH. ChIP-Seq of transcription factors predicts absolute and differential gene expression in embryonic stem cells. Proc Natl Acad Sci U S A 2009, 106:21521-21526.
97. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, et al. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 2008, 5:613-619.
98. Kohl M, Wiese S, Warscheid B. Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol 2011, 696:291-303.