Large-Scale Quality Analysis of Published ChIP-seq Data

Abstract

ChIP-seq has become the primary method for identifying in vivo protein–DNA interactions on a genome-wide scale, with nearly 800 publications involving the technique appearing in PubMed as of December 2012. Individually and in aggregate, these data are an important and information-rich resource. However, uncertainties about data quality confound their use by the wider research community. Recently, the Encyclopedia of DNA Elements (ENCODE) project developed and applied metrics to objectively measure ChIP-seq data quality. The ENCODE quality analysis was useful for flagging datasets for closer inspection, eliminating or replacing poor data, and for driving changes in experimental pipelines. There had been no similarly systematic quality analysis of the large and disparate body of published ChIP-seq profiles. Here, we report a uniform analysis of vertebrate transcription factor ChIP-seq datasets in the Gene Expression Omnibus (GEO) repository as of April 1, 2012. The majority (55%) of datasets scored as being highly successful, but a substantial minority (20%) were of apparently poor quality, and another ∼25% were of intermediate quality. We discuss how different uses of ChIP-seq data are affected by specific aspects of data quality, and we highlight exceptional instances for which the metric values should not be taken at face value. Unexpectedly, we discovered that a significant subset of control datasets (i.e., no immunoprecipitation and mock immunoprecipitation samples) display an enrichment structure similar to successful ChIP-seq data. This can, in turn, affect peak calling and data interpretation. Published datasets identified here as high-quality comprise a large group that users can draw on for large-scale integrated analysis. In the future, ChIP-seq quality assessment similar to that used here could guide experimentalists at early stages in a study, provide useful input in the publication process, and be used to stratify ChIP-seq data for different community-wide uses.

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     Lu F. Tsai K. Chen H. S. Wikramasinghe P. Davuluri R. V., 2012 Identification of host-chromosome binding sites and candidate gene targets for Kaposi’s sarcoma-associated herpesvirus LANA. J. Virol. 86: 5752–5762

     Not in our library10.1128/jvi.07216-11

101. 101.

     Ma Z. Swigut T. Valouev A. Rada-Iglesias A. Wysocka J., 2010 Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18: 120–127

     Not in our library10.1038/nsmb.2000

102. 102.

     MacIsaac K. D. Lo K. A. Gordon W. Motola S. Mazor T., 2010 A quantitative model of transcriptional regulation reveals the influence of binding location on expression. PLOS Comput. Biol. 6: e1000773

     Not in our library10.1371/journal.pcbi.1000773

103. 103.

     Mahony S. Mazzoni E. O. McCuine S. Young R. A. Wichterle H., 2010 Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Genome Biol. 12: R2

     Not in our library10.1186/gb-2011-12-1-r2

104. 104.

     Marban C. Su T. Ferrari R. Li B. Vatakis D., 2011 Genome-wide binding map of the HIV-1 Tat protein to the human genome. PLoS ONE 6: e26894

     Not in our library10.1371/journal.pone.0026894

105. 105.

     Marson A. Levine S. S. Cole M. F. Frampton G. M. Brambrink T., 2008 Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521–533

     Not in our library10.1016/j.cell.2008.07.020

106. 106.

     Martinez P. Thanasoula M. Carlos A. R. Gómez-López G. Tejera A. M., 2010 Mammalian Rap1 controls telomere function and gene expression through binding to telomeric and extratelomeric sites. Nat. Cell Biol. 12: 768–780

     Not in our library10.1038/ncb2081

107. 107.

     Mazzoni E. O. Mahony S. Iacovino M. Morrison C. A. Mountoufaris G., 2011 Embryonic stem cell-based mapping of developmental transcriptional programs. Nat. Methods 8: 1056–1058

     Not in our library10.1038/nmeth.1775

108. 108.

     McManus S. Ebert A. Salvagiotto G. Medvedovic J. Sun Q., 2011 The transcription factor Pax5 regulates its target genes by recruiting chromatin-modifying proteins in committed B cells. EMBO J. 30: 2388–2404

     Not in our library10.1038/emboj.2011.140

109. 109.

     Mendoza-Parra M. A. Walia M. Sankar M. Gronemeyer H., 2011 Dissecting the retinoid-induced differentiation of F9 embryonal stem cells by integrative genomics. Mol. Syst. Biol. 7: 538

     Not in our library10.1038/msb.2011.73

110. 110.

     Mendoza-Parra M. A. Van Gool M. Mohamed Saleem M. A. Ceschin D. G. Gronemeyer H., 2013 A quality control system for profiles obtained by ChIP sequencing. Nucleic Acids Res. 41: e196

     Not in our library10.1093/nar/gkt829

111. 111.

     Meyer M. B. Goetsch P. D. Pike J. W., 2012 VDR/RXR and TCF4/β-catenin cistromes in colonic cells of colorectal tumor origin: impact on c-FOS and c-MYC gene expression. Mol. Endocrinol. 26: 37–51

     Not in our library10.1210/me.2011-1109

112. 112.

     Mikkelsen T. S. Ku M. Jaffe D. B. Issac B. Lieberman E., 2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553–560

     Not in our library10.1038/nature06008

113. 113.

     Miller T. W. Balko J. M. Fox E. M. Ghazoui Z. Dunbier A., 2011 ERα-dependent E2F transcription can mediate resistance to estrogen deprivation in human breast cancer. Cancer Discov. 1: 338–351

     Not in our library10.1158/2159-8290.cd-11-0101

114. 114.

     Miyazaki M. Rivera R. R. Miyazaki K. Lin Y. C. Agata Y., 2011 The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat. Immunol. 12: 992–1001

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115. 115.

     Mullen A. C. Orlando D. A. Newman J. J. Lovén J. Kumar R. M., 2011 Master transcription factors determine cell-type-specific responses to TGFβ signaling. Cell 147: 565–576

     Not in our library10.1016/j.cell.2011.08.050

116. 116.

     Mullican S. E. Gaddis C. A. Alenghat T. Nair M. G. Giacomin P. R., 2011 Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev. 25: 2480–2488

     Not in our library10.1101/gad.175950.111

117. 117.

     Nakayamada S. Kanno Y. Takahashi H. Jankovic D. Lu K. T., 2011 Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 35: 919–931

     Not in our library10.1016/j.immuni.2011.11.012

118. 118.

     Nishiyama A. Xin L. Sharov A. A. Thomas M. Mowrer G., 2009 Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 5: 420–433

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119. 119.

     Nitzsche A. Paszkowski-Rogacz M. Matarese F. Janssen-Megens E. M. Hubner N. C., 2011 RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS ONE 6: e19470

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120. 120.

     Norton L. Fourcaudot M. Abdul-Ghani M. A. Winnier D. Mehta F. F., 2011 Chromatin occupancy of transcription factor 7-like 2 (TCF7L2) and its role in hepatic glucose metabolism. Diabetologia 54: 3132–3142

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121. 121.

     Novershtern N. Subramanian A. Lawton L. N. Mak R. H. Haining W. N., 2011 Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 144: 296–309

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122. 122.

     Ntziachristos P. Tsirigos A. van Vlierberghe P. Nedjic J. Trimarchi T., 2012 Genetic inactivation of the polycomb repressive complex 2 in T cell acute lymphoblastic leukemia. Nat. Med. 18: 298–301

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123. 123.

     Palii C. G. Perez-Iratxeta C. Yao Z. Cao Y. Dai F., 2010 Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J. 30: 494–509

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124. 124.

     Pehkonen P. Welter-Stahl L. Diwo J. Ryynänen J. Wienecke-Baldacchino A., 2012 Genome-wide landscape of liver X receptor chromatin binding and gene regulation in human macrophages. BMC Genomics 13: 50

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125. 125.

     Peng S. Alekseyenko A. A. Larschan E. Kuroda M. I. Park P. J., 2007 Normalization and experimental design for ChIP-chip data. BMC Bioinformatics 8: 219

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126. 126.

     Pepke S. Wold B. Mortazavi A., 2009 Computation for ChIP-seq and RNA-seq studies. Nat. Methods 6: S22–S32

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127. 127.

     Ptasinska A. Assi S. A. Mannari D. James S. R. Williamson D., 2012 Depletion of RUNX1/ETO in t(8;21) AML cells leads to genome-wide changes in chromatin structure and transcription factor binding. Leukemia 26: 1829–1841

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128. 128.

     Qi H. H. Sarkissian M. Hu G. Q. Wang Z. Bhattacharjee A., 2010 Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466: 503–507

     Not in our library10.1038/nature09261

129. 129.

     Quenneville S. Verde G. Corsinotti A. Kapopoulou A. Jakobsson J., 2011 In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol. Cell 44: 361–372

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130. 130.

     Rada-Iglesias A. Bajpai R. Swigut T. Brugmann S. A. Flynn R. A., 2010 A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279–283

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131. 131.

     Rahl P. B. Lin C. Y. Seila A. C. Flynn R. A. McCuine S., 2010 c-Myc regulates transcriptional pause release. Cell 141: 432–445

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132. 132.

     Ramagopalan S. V. Heger A. Berlanga A. J. Maugeri N. J. Lincoln M. R., 2010 A ChIP-seq defined genome-wide map of vitamin D receptor binding: associations with disease and evolution. Genome Res. 20: 1352–1360

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133. 133.

     Ramos Y. F. Hestand M. S. Verlaan M. Krabbendam E. Ariyurek Y., 2010 Genome-wide assessment of differential roles for p300 and CBP in transcription regulation. Nucleic Acids Res. 38: 5396–5408

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134. 134.

     Rao N. A. McCalman M. T. Moulos P. Francoijs K. J. Chatziioannou A., 2011 Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res. 21: 1404–1416

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135. 135.

     Remeseiro S. Cuadrado A. Gómez-López G. Pisano D. G. Losada A., 2012 A unique role of cohesin-SA1 in gene regulation and development. EMBO J. 31: 2090–2102

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136. 136.

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137. 137.
     Genome-Wide and Phase-Specific DNA-Binding Rhythms of BMAL1 Control Circadian Output Functions in Mouse Liver · 2011

     No notice
138. 138.

     Robertson G. Hirst M. Bainbridge M. Bilenky M. Zhao Y., 2007 Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 4: 651–657

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139. 139.

     Sadasivam S. Duan S. DeCaprio J. A., 2012 The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev. 26: 474–489

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140. 140.

     Sahu B. Laakso M. Ovaska K. Mirtti T. Lundin J., 2011 Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J. 30: 3962–3976

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141. 141.

     Sakabe N. J. Aneas I. Shen T. Shokri L. Park S. Y., 2012 Dual transcriptional activator and repressor roles of TBX20 regulate adult cardiac structure and function. Hum. Mol. Genet. 21: 2194–2204

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142. 142.

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143. 143.
     The Cardiac Transcription Network Modulated by Gata4, Mef2a, Nkx2.5, Srf, Histone Modifications, and MicroRNAs · 2011

     No notice
144. 144.

     Schmitz S. U. Albert M. Malatesta M. Morey L. Johansen J. V., 2011 Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J. 30: 4586–4600

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145. 145.
     CHD7 Targets Active Gene Enhancer Elements to Modulate ES Cell-Specific Gene Expression · 2010

     No notice
146. 146.

     Sehat B. Tofigh A. Lin Y. Trocmé E. Liljedahl U., 2010 SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor. Sci. Signal. 3: ra10

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147. 147.

     Seitz V. Butzhammer P. Hirsch B. Hecht J. Gütgemann I., 2011 Deep sequencing of MYC DNA-binding sites in Burkitt lymphoma. PLoS ONE 6: e26837

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148. 148.

     Shen T. Aneas I. Sakabe N. Dirschinger R. J. Wang G., 2011 Tbx20 regulates a genetic program essential to adult mouse cardiomyocyte function. J. Clin. Invest. 121: 4640–4654

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149. 149.

     Shukla S. Kavak E. Gregory M. Imashimizu M. Shutinoski B., 2011 CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479: 74–79

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150. 150.

     Siersbæk R. Nielsen R. John S. Sung M. H. Baek S., 2011 Extensive chromatin remodelling and establishment of transcription factor hotspots’ during early adipogenesis. EMBO J. 30: 1459–1472

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151. 151.
     Role of p53 Serine 46 in p53 Target Gene Regulation · 2011

     No notice
152. 152.

     Smith E. R. Lin C. Garrett A. S. Thornton J. Mohaghegh N., 2011 The little elongation complex regulates small nuclear RNA transcription. Mol. Cell 44: 954–965

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153. 153.

     Soccio R. E. Tuteja G. Everett L. J. Li Z. Lazar M. A., 2011 Species-specific strategies underlying conserved functions of metabolic transcription factors. Mol. Endocrinol. 25: 694–706

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154. 154.

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155. 155.

     Stadler M. B. Murr R. Burger L. Ivanek R. Lienert F., 2011 DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490–495

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156. 156.

     Steger D. J. Grant G. R. Schupp M. Tomaru T. Lefterova M. I., 2010 Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. 24: 1035–1044

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157. 157.

     Sun J. Pan H. Lei C. Yuan B. Nair S. J., 2011 Genetic and genomic analyses of RNA polymerase II-pausing factor in regulation of mammalian transcription and cell growth. J. Biol. Chem. 286: 36248–36257

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158. 158.

     Tallack M. R. Whitington T. Yuen W. S. Wainwright E. N. Keys J. R., 2010 A global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cells. Genome Res. 20: 1052–1063

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159. 159.

     Tan P. Y. Chang C. W. Chng K. R. Wansa K. D. Sung W. K., 2011a Integration of regulatory networks by NKX3–1 promotes androgen-dependent prostate cancer survival. Mol. Cell. Biol. 32: 399–414

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160. 160.

     Tan S. K. Lin Z. H. Chang C. W. Varang V. Chng K. R., 2011b AP-2γ regulates oestrogen receptor-mediated long-range chromatin interaction and gene transcription. EMBO J. 30: 2569–2581

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161. 161.

     Tang C. Shi X. Wang W. Zhou D. Tu J., 2010 Global analysis of in vivo EGR1-binding sites in erythroleukemia cell using chromatin immunoprecipitation and massively parallel sequencing. Electrophoresis 31: 2936–2943

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162. 162.

     Teo A. K. Arnold S. J. Trotter M. W. Brown S. Ang L. T., 2011 Pluripotency factors regulate definitive endoderm specification through eomesodermin. Genes Dev. 25: 238–250

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163. 163.
     Genome-wide Analysis of Simultaneous GATA1/2, RUNX1, FLI1, and SCL Binding in Megakaryocytes Identifies Hematopoietic Regulators · 2011

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164. 164.

     Tiwari V. K. Burger L. Nikoletopoulou V. Deogracias R. Thakurela S., 2011b Target genes of Topoisomerase IIβ regulate neuronal survival and are defined by their chromatin state. Proc. Natl. Acad. Sci. USA 109: E934–E943

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165. 165.

     Tiwari V. K. Stadler M. B. Wirbelauer C. Paro R. Schübeler D., 2011 A chromatin-modifying function of JNK during stem cell differentiation. Nat. Genet. 44: 94–100

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166. 166.

     Trompouki E. Bowman T. V. Lawton L. N. Fan Z. P. Wu D. C., 2011 Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 147: 577–589

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167. 167.

     Trowbridge J. J. Sinha A. U. Zhu N. Li M. Armstrong S. A., 2012 Haploinsufficiency of Dnmt1 impairs leukemia stem cell function through derepression of bivalent chromatin domains. Genes Dev. 26: 344–349

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168. 168.

     van Heeringen S. J. Akhtar W. Jacobi U. G. Akkers R. C. Suzuki Y., 2011 Nucleotide composition-linked divergence of vertebrate core promoter architecture. Genome Res. 21: 410–421

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169. 169.

     Vermeulen M. Eberl H. C. Matarese F. Marks H. Denissov S., 2010 Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967–980

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170. 170.

     Verzi M. P. Shin H. He H. H. Sulahian R. Meyer C. A., 2010 Differentiation-specific histone modifications reveal dynamic chromatin interactions and partners for the intestinal transcription factor CDX2. Dev. Cell 19: 713–726

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171. 171.

     Verzi M. P. Shin H. Ho L. L. Liu X. S. Shivdasani R. A., 2011 Essential and redundant functions of caudal family proteins in activating adult intestinal genes. Mol. Cell. Biol. 31: 2026–2039

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172. 172.

     Vilagos B. Hoffmann M. Souabni A. Sun Q. Werner B., 2012 Essential role of EBF1 in the generation and function of distinct mature B cell types. J. Exp. Med. 209: 775–792

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173. 173.

     Visel A. Blow M. J. Li Z. Zhang T. Akiyama J. A., 2009 ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854–858

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174. 174.

     Vivar O. I. Zhao X. Saunier E. F. Griffin C. Mayba O. S., 2010 Estrogen receptor beta binds to and regulates three distinct classes of target genes. J. Biol. Chem. 285: 22059–22066

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175. 175.

     Wang D. Garcia-Bassets I. Benner C. Li W. Su X., 2011a Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474: 390–394

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176. 176.

     Wang H. Zou J. Zhao B. Johannsen E. Ashworth T., 2011b Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc. Natl. Acad. Sci. USA 108: 14908–14913

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177. 177.

     Wang J. Zhuang J. Iyer S. Lin X. Whitfield T. W., 2012 Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22: 1798–1812

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178. 178.

     Wei L. Vahedi G. Sun H. W. Watford W. T. Takatori H., 2010 Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation. Immunity 32: 840–851

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183. 183.

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184. 184.

     Woodfield G. W. Chen Y. Bair T. B. Domann F. E. Weigel R. J., 2010 Identification of primary gene targets of TFAP2C in hormone responsive breast carcinoma cells. Genes Chromosomes Cancer 49: 948–962

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188. 188.

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     Xu C. Fan Z. P. Müller P. Fogley R. DiBiase A., 2011 Nanog-like regulates endoderm formation through the Mxtx2-Nodal pathway. Dev. Cell 22: 625–638

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192. 192.

     Yang X. P. Ghoreschi K. Steward-Tharp S. M. Rodriguez-Canales J. Zhu J., 2011 Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12: 247–254

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193. 193.

     Yao H. Brick K. Evrard Y. Xiao T. Camerini-Otero R. D., 2010 Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 24: 2543–2555

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194. 194.

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195. 195.

     Yoon S. J. Wills A. E. Chuong E. Gupta R. Baker J. C., 2011 HEB and E2A function as SMAD/FOXH1 cofactors. Genes Dev. 25: 1654–1661

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197. 197.

     Yu M. Mazor T. Huang H. Huang H. T. Kathrein K. L., 2012 Direct recruitment of polycomb repressive complex 1 to chromatin by core binding transcription factors. Mol. Cell 45: 330–343

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198. 198.

     Yu S. Cui K. Jothi R. Zhao D. M. Jing X., 2010 GABP controls a critical transcription regulatory module that is essential for maintenance and differentiation of hematopoietic stem/progenitor cells. Blood 117: 2166–2178

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199. 199.

     Yuan P. Han J. Guo G. Orlov Y. L. Huss M., 2009 Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23: 2507–2520

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     Zhang Y. Laz E. V. Waxman D. J., 2011 Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell. Biol. 32: 880–896

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202. 202.

     Zhao B. Zou J. Wang H. Johannsen E. Peng C. W., 2011a Epstein-Barr virus exploits intrinsic B-lymphocyte transcription programs to achieve immortal cell growth. Proc. Natl. Acad. Sci. USA 108: 14902–14907

     Not in our library10.1073/pnas.1108892108

203. 203.

     Zhao L. Glazov E. A. Pattabiraman D. R. Al-Owaidi F. Zhang P., 2011b Integrated genome-wide chromatin occupancy and expression analyses identify key myeloid pro-differentiation transcription factors repressed by Myb. Nucleic Acids Res. 39: 4664–4679

     Not in our library10.1093/nar/gkr024

Cited by papers we hold 5

• Principles of RNA processing from analysis of enhanced CLIP maps for 150 RNA binding proteins · 2020
  No notice
• An atlas of dynamic chromatin landscapes in mouse fetal development · 2020
  Corrected
• Brd4 binds to active enhancers to control cell identity gene induction in adipogenesis and myogenesis · 2017
  No notice
• Characterization of the direct targets of FOXO transcription factors throughout evolution · 2016
  No notice
• Impact of artifact removal on ChIP quality metrics in ChIP-seq and ChIP-exo data · 2014
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.