Leveraging biological replicates to improve analysis in ChIP-seq experiments

Computational and Structural Biotechnology Journal

Volumn 9, Issue 13, 2014, Pages e201401002-

  Yang, Yajie ^a   Fear, Justin ^a   Hu, Jianhong ^b   Haecker, Irina ^c   Zhou, Lei ^a   Renne, Rolf ^a,d   Bloom, David ^a   McIntyre, Lauren M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

Biological replicates; ChIP seq; Peak identification

Indexed keywords

EID: 84901599336     PISSN: None     EISSN: 20010370     Source Type: Journal    
DOI: 10.5936/csbj.201401002     Document Type: Article

References (70)

1. Orlando V (2000) Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. Trends in Biochemical Sciences 25:99-104. (Pubitemid 30122417)
2. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, et al. (2000) Genome-Wide Location and Function of DNA Binding Proteins. Science 290:2306-2309. (Pubitemid 32041573)
3. Iyer VR Horak CE, Scafe CS, Botstein D, Snyder M, et al. (2001) Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409:533-538. (Pubitemid 32144361)
4. Jothi R Cuddapah S, Barski A, Cui K, Zhao K (2008) Genomewide identification of in vivo protein-DNA binding sites from ChlP-Seq data. Nucl Acids Res 36:5221-5231.
5. Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genomewide mapping of in vivo protein-DNA interactions. Science 316:1497-1502. (Pubitemid 46906620)
6. Robertson G, Hirst M, Bainbridge M, Bilenky M, Zhao Y, et al. (2007) Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Meth 4:651-657. (Pubitemid 47202477)
7. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, et al. (2007) High-Resolution Profiling of Histone Methylations in the Human Genome. Cell 129:823-837. (Pubitemid 46802390)
8. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineagecommitted cells. Nature 448:553-560. (Pubitemid 47206934)
9. Blahnik KR, Dou L, Echipare L, Iyengar S, O'Geen H, et al. (2011) Characterization of the Contradictory Chromatin Signatures at the 3' Exons of Zinc Finger Genes. PLoS ONE 6:e17121.
10. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T (2009) PeakSeq enables systematic scoring of ChlP-seq experiments relative to controls. Nature Biotechnology 27:66-75.
11. Baugh LR, De Modena J, Sternberg PW (2009) RNA Pol II Accumulates at Promoters of Growth Genes During Developmental Arrest. Science 324:92-94.
12. Chen Y, Negre N, Li Q, Mieczkowska JO, Slattery M, et al. (2012) Systematic evaluation of factors influencing ChlP-seq fidelity. Nat Meth 9:609-614.
13. Park PJ (2009) ChlP-seq: advantages and challenges of a maturing technology. Nat Rev Genet 10:669-680.
14. Vega VB, Cheung E, Palanisamy N, Sung W-K (2009) Inherent Signals in Sequencing-Based Chromatin-ImmunoPrecipitation Control Libraries. PLoS ONE 4:e5241.
15. Kuan PF, Chung D, Pan G, Thomson JA, Stewart R, et al. (2011) A Statistical Framework for the Analysis of ChlP-Seq Data. Journal of the American Statistical Association 106:891-903.
16. Dohm JC, Lottaz C, Borodina T, Himmelbauer H (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Research 36:e105-e105.
17. Wilbanks EG, Facciotti MT (2010) Evaluation of algorithm performance in ChlP-seq peak detection. PLoS One 5:e11471.
18. Tuteja G, White P, Schug J, Kaestner KH (2009) Extracting transcription factor targets from ChlP-Seq data. Nucleic Acids Research 37:e113-e113.
19. Churchill GA Fundamentals of experimental design for cDNA microarrays. Nat Genet.
20. Yang YH, Speed T (2002) Design issues for cDNA microarray experiments. Nat Rev Genet 3:579-588. (Pubitemid 34827132)
21. Kerr KM (2003) Design Considerations for Efficient and Effective Microarray Studies. Biometrics 59:822-828.
22. Chu T-M, Weir B, Wolfinger R (2002) A systematic statistical linear modeling approach to oligonucleotide array experiments. Mathematical Biosciences 176:35-51. (Pubitemid 34242098)
23. Oberg AL, Vitek O (2009) Statistical Design of Quantitative Mass Spectrometry-Based Proteomic Experiments. Journal of Proteome Research 8:2144-2156.
24. Bullard J, Purdom E, Hansen K, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11:94.
25. McIntyre LM, Lopiano K, A M M, V A, AL O, et al. (2011) RNA-seq: technical variability and sampling. BMC Genomics 12.
26. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, et al. (2012) ChlP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22:1813-1831.
27. Chen Y, Meyer C, Liu T, Li W, Liu J, et al. (2011) MM-ChIP enables integrative analysis of cross-platform and between-laboratory ChlP-chip or ChlP-seq data. Genome Biology 12:R11.
28. Hutchins AP, Diez D, Takahashi Y, Ahmad S, Jauch R, et al. (2013) Distinct transcriptional regulatory modules underlie STAT3's cell type-independent and cell type-specific functions. Nucl Acids Res 41:2155-2170.
29. Consortium TEP (2011) A User's Guide to the Encyclopedia of DNA Elements (ENCODE). PLoS Biol 9:e1001046.
30. Li Q, Brown JB, Huang H, Bickel PJ (2011) Measuring reproducibility of high-throughput experiments. Ann Appl Stat 5:1752-1779.
31. Kharchenko PV, Tolstorukov MY, Park PJ (2008) Design and analysis of ChlP-seq experiments for DNA-binding proteins. Nat Biotechnol 26:1351-1359.
32. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based Analysis of ChlP-Seq (MACS). Genome Biology 9:R137.
33. Ji H, Jiang H, Ma W, Johnson D, Myers R (2008) An integrated software system for analyzing ChlP-chip and ChlP-seq data. Nat Biotechnol 26:1293-1300.
34. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E, et al. (2008) Genome-wide analysis of transcription factor binding sites based on ChlP-Seq data. Nat Meth 5:829-834.
35. Blahnik KR, Dou L, O'Geen H, McPhillips T, Xu X (2009) Sole-Search: an integrated analysis program for peak detection and functional annotation using ChlP-seq data. Nucl Acids Res 38:e13.
36. Liang K, Keles S (2012) Detecting differential binding of transcription factors with ChlP-seq. Bioinformatics 28:121-122.
37. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, et al. (2010) Five-Vertebrate ChlP-seq Reveals the Evolutionary Dynamics of Transcription Factor Binding. Science 328:1036-1040.
38. Shao Z, Zhang Y, Yuan G-C, Orkin S, Waxman D (2012) MAnorm: a robust model for quantitative comparison of ChlP-Seq data sets. Genome Biology 13:R16.
39. Xu H, Wei C-L, Lin F, Sung W-K (2008) An HMM approach to genome-wide identification of differential histone modification sites from ChlP-seq data. Bioinformatics 24:2344-2349.
40. Zhu L, Gazin C, Lawson N, Pages H, Lin S, et al. (2010) ChlPpeakAnno: a Bioconductor package to annotate ChlP-seq and ChlP-chip data. BMC Bioinformatics 11:237.
41. Lu F, Tsai K, Chen H-S, Wikramasinghe P, Davuluri RV, et al. (2012) Identification of Host-Chromosome Binding Sites and Candidate Gene Targets for Kaposi's Sarcoma-Associated Herpesvirus LANA. Journal of Virology 86:5752-5762.
42. Revilla-i-Domingo R, Bilic I, Vilagos B, Tagoh H, Ebert A, et al. (2012) The B-cell identity factor Pax5 regulates distinct transcriptional programmes in early and late B lymphopoiesis. EMBO J 31:3130-3146.
43. Fujiwara T, OGeen H, Keles S, Blahnik K, Linnemann AK, et al. (2009) Discovering Hematopoietic Mechanisms through Genomewide Analysis of GATA Factor Chromatin Occupancy. Molecular cell 36:667-681.
44. Yu M, Riva L, Xie H, Schindler Y, Moran TB, et al. (2009) Insights into GATA-1-Mediated Gene Activation versus Repression via Genome-wide Chromatin Occupancy Analysis. Molecular cell 36:682-695.
45. Liu W, Tanasa B, Tyurina OV, Zhou TY, Gassmann R et al. (2010) PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 466:508-512.
46. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, et al. (2010) Variation in Transcription Factor Binding Among Humans. Science 328:232-235.
47. Soccio RE, Tuteja G, Everett LJ, Li Z, Lazar MA, et al. (2011) Species-Specific Strategies Underlying Conserved Functions of Metabolic Transcription Factors. Molecular Endocrinology 25:694-706.
48. Bochkis IM, Schug J, Ye DZ, Kurinna S, Stratton SA, et al. (2012) Genome-Wide Location Analysis Reveals Distinct Transcriptional Circuitry by Paralogous Regulators Foxal and Foxa2. PLoS Genet 8:e1002770.
49. Langmead B, Trapnell C, Pop M, Salzberg S (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10:R25.
50. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotech 29:24-26.
51. Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 14:178-192.
52. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628. (Pubitemid 351911867)
53. Fleiss J (1981) Statistical methods for rates and proportions. New York: Wiley.
54. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 307-310. (Pubitemid 16134762)
55. Bland JM, Altman DG (1988) Misleading Statistics: errors in textbooks, software and manuals. International Journal of Epidemiology 17:201-203.
56. Johnson RA, Wichern DW (1992) Applied multivariate Statistical Analysis: Prentice Hall.
57. Wu H, Lozano G (1994) NF-kappa B activation of p53. A potential mechanism for suppressing cell growth in response to stress. J Biol Chem 269:20067-20074.
58. Schumm K, Rocha S, Caamano J, Perkins ND (2006) Regulation of p53 tumour suppressor target gene expression by the p52 NF-[kappa]B subunit. Embo J 25:4820-4832. (Pubitemid 44607027)
59. Haskill S, Beg AA, Tompkins SM, Morris JS, Yurochko AD, et al. (1991) Characterization of an immediate-early gene induced in adherent monocytes that encodes iKB-like activity. Cell 65:1281-1289. (Pubitemid 121001340)
60. Sun SC, Ganchi PA, Ballard DW, Greene WC (1993) NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 259:1912-1915. (Pubitemid 23124465)
61. Ten RM, Paya CV, Israel N, Bail OL, Mattel MG, et al. (1992) The characterization of the promoter of the gene encoding the p50 subunit of NF-kappa B indicates that it participates in its own regulation. Embo j 11:195-203.
62. Kasperczyk H, Baumann B, Debatin K-M, Fulda S (2009) Characterization of sonic hedgehog as a novel NF-kB target gene that promotes NF-KB-mediated apoptosis resistance and tumor growth in vivo. Faseb j 23:21-33.
63. Wu K, Jiang S-W, Thangaraju M, Wu G, Couch FJ (2000) Induction of the BRCA2 Promoter by Nuclear Factor-KB. J Biol Chem 275:35548-35556.
64. Xia D, Srinivas H, Ahn Y-H, Sethi G, Sheng X, et al. (2007) Mitogen-activated Protein Kinase Kinase-4 Promotes Cell Survival by Decreasing PTEN Expression through an NFI°B-dependent Pathway. J Biol Chem 282:3507-3519. (Pubitemid 47084470)
65. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, et al. (2012) Ago HITS-CLIP Expands Understanding of Kaposi's Sarcoma-associated Herpesvirus miRNA Function in Primary Effusion Lymphomas. PLoS Pathog 8:e1002884.
66. Cao AR Rabinovich R Xu M, Xu X, Jin VX, et al. (2011) Genomewide Analysis of Transcription Factor E2F1 Mutant Proteins Reveals That N- and C-terminal Protein Interaction Domains Do Not Participate in Targeting E2F1 to the Human Genome. Journal of Biological Chemistry 286:11985-11996.
67. Bieda M, Xu X, Singer MA, Green R, Farnham PJ (2006) Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Research 16:595-605.
68. Allison DB, Cui X, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet 7:55-65. (Pubitemid 41828948)
69. Auer PL, Doerge RW (2010) Statistical Design and Analysis of RNA Sequencing Data. Genetics 185:405-416.
70. Anshul Kundaje, Lucy Yungsook Jung, Peter Kharchenko, Barbara Wold, Arend Sidow, Serafim Batzoglou, Peter Park (Submitted). Assessment of ChlP-seq data quality using cross-correlation analysis.