Widespread misinterpretable ChIP-seq bias in yeast

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Park, Daechan ^a   Lee, Yaelim ^a   Bhupindersingh, Gurvani ^a   Iyer, Vishwanath R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TUP1; UNCLASSIFIED DRUG;

ANALYTICAL ERROR; ARTICLE; BINDING KINETICS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; FALSE POSITIVE RESULT; FUNGAL GENE; GENE EXPRESSION; GENE INTERACTION; GENE LIBRARY; GENE REPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOSOME; PROTEIN BINDING; SEQUENCE ANALYSIS;

CHROMATIN IMMUNOPRECIPITATION; DNA, FUNGAL; FALSE POSITIVE REACTIONS; NUCLEAR PROTEINS; NUCLEOSOMES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84891945420     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083506     Document Type: Article

References (45)

1. Furey TS (2012) ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat Rev Genet 13:840-852. doi:10.1038/nrg3306. PubMed: 23090257.
2. Park PJ (2009) ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet 10:669-680. doi:10.1038/nrg2641. PubMed: 19736561.
3. Rougemont J, Naef F (2012) Computational analysis of protein-DNA interactions from ChIP-seq data. Methods Mol Biol 786:263-273. PubMed: 21938632.
4. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330:1775-1787. doi:10.1126/science.1196914. PubMed: 21177976.
5. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N et al. (2010) Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE. Science 330:1787-1797. doi:10.1126/science.1198374. PubMed: 21177974.
6. The ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57-74. doi:10.1038/nature11247. PubMed: 22955616.
7. Chadwick LH (2012) The NIH Roadmap Epigenomics Program data resource. Epigenomics 4:317-324. doi:10.2217/epi.12.18. PubMed: 22690667.
8. Lee B-K, Bhinge AA, Battenhouse A, McDaniell RM, Liu Z et al. (2012) Cell-type specific and combinatorial usage of diverse transcription factors revealed by genome-wide binding studies in multiple human cells. Genome Res 22:9-24. doi:10.1101/gr.127597.111. PubMed: 22090374.
9. Workman CT, Mak HC, McCuine S, Tagne J-B, Agarwal M et al. (2006) A systems approach to mapping DNA damage response pathways. Science 312:1054-1059. doi:10.1126/science.1122088. PubMed: 16709784.
10. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431:99-104. doi:10.1038/nature02800. PubMed: 15343339. (Pubitemid 39215116)
11. Venters BJ, Wachi S, Mavrich TN, Andersen BE, Jena P et al. (2011) A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 41:480-492. doi:10.1016/j.molcel.2011.01.015. PubMed: 21329885.
12. Rhee HS, Pugh BF (2011) Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147:1408-1419. doi:10.1016/j.cell.2011.11.013. PubMed: 22153082.
13. Lefrançois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T et al. (2009) Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10:37. doi:10.1186/1471-2164-10-37. PubMed: 19159457.
14. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF (2012) Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149:1461-1473. doi:10.1016/j.cell.2012.04.036. PubMed: 22726434.
15. Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A et al. (2003) Global analysis of protein expression in yeast. Nature 425:737-741. doi:10.1038/nature02046. PubMed: 14562106. (Pubitemid 37314318)
16. Wilbanks EG, Facciotti MT (2010) Evaluation of algorithm performance in ChIP-seq peak detection. PLOS ONE 5:e11471. doi:10.1371/journal.pone.0011471. PubMed: 20628599.
17. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906. doi:10.1126/science.285.5429.901. PubMed: 10436161. (Pubitemid 29381993)
18. Iyer V, Struhl K (1996) Absolute mRNA levels and transcriptional initiation rates in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93:5208-5212. doi:10.1073/pnas.93.11.5208. PubMed: 8643554. (Pubitemid 26159427)
19. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. doi: 10.1093/bioinformatics/btp324. PubMed: 19451168.
20. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH et al. (2002) The Human Genome Browser at UCSC. Genome Res 12:996-1006. doi:10.1101/gr.229102. Article published online before print in May 2002 PubMed: 12045153 (Pubitemid 34662293)
21. Hunter JD (2007) Matplotlib: A 2D graphics environment. Comput Sci Eng 9:90-95. doi:10.1109/MCSE.2007.116. (Pubitemid 350025537)
22. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS et al. (2008) Model-based Analysis of ChIP-Seq (MACS). Genome Biol 9:R137. doi: 10.1186/gb-2008-9-9-r137. PubMed: 18798982.
23. Preti M, Ribeyre C, Pascali C, Bosio MC, Cortelazzi B et al. (2010) The telomere-binding protein Tbf1 demarcates snoRNA gene promoters in Saccharomyces cerevisiae. Mol Cell 38:614-620. doi:10.1016/j.molcel. 2010.04.016. PubMed: 20513435.
24. Zhang L, Ma H, Pugh BF (2011) Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res 21:875-884. doi:10.1101/gr.117465. 110. PubMed: 21515815.
25. Shao Z, Zhang Y, Yuan G-C, Orkin SH, Waxman DJ (2012) MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets. Genome Biol 13:R16. doi:10.1186/gb-2012-13-3-r16. PubMed: 22424423.
26. Tippmann SC, Ivanek R, Gaidatzis D, Schöler A, Hoerner L et al. (2012) Chromatin measurements reveal contributions of synthesis and decay to steady-state mRNA levels. Mol Syst Biol 8:593. PubMed: 22806141.
27. Shivaswamy S, Iyer VR (2008) Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response. Mol Cell Biol 28:2221-2234. doi:10.1128/MCB. 01659-07. PubMed: 18212068. (Pubitemid 351429969)
28. Hardwick JS, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL (1999) Rapamycin-modulated transcription defines the subset of nutrientsensitive signaling pathways directly controlled by the Tor proteins. Proc Natl Acad Sci U S A 96:14866-14870. doi:10.1073/pnas. 96.26.14866. PubMed: 10611304. (Pubitemid 30019731)
29. Li X, Cai M (1999) Recovery of the yeast cell cycle from heat shockinduced G (1) arrest involves a positive regulation of G (1) cyclin expression by the S phase cyclin Clb5. J Biol Chem 274:24220-24231. doi:10.1074/jbc.274.34.24220. PubMed: 10446197.
30. Horak CE, Luscombe NM, Qian J, Bertone P, Piccirrillo S et al. (2002) Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae. Genes Dev 16:3017-3033. doi:10.1101/gad.1039602. PubMed: 12464632. (Pubitemid 35424190)
31. 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. doi:10.1038/35054095. PubMed: 11206552. (Pubitemid 32144361)
32. Smith RL, Johnson AD (2000) Turning genes off by Ssn6-Tup1: a conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci 25:325-330. doi:10.1016/S0968-0004 (00) 01592-9. PubMed: 10871883.
33. Zentner GE, Tsukiyama T, Henikoff S (2013) ISWI and CHD chromatin remodelers bind promoters but act in gene bodies. PLoS Genet 9:e1003317. PubMed: 23468649.
34. Hahn J-S, Hu Z, Thiele DJ, Iyer VR (2004) Genome-Wide Analysis of the Biology of Stress Responses through Heat Shock Transcription Factor. Mol Cell Biol 24:5249-5256. doi:10.1128/MCB. 24.12.5249-5256.2004. PubMed: 15169889. (Pubitemid 38738160)
35. Kidder BL, Hu G, Zhao K (2011) ChIP-Seq: technical considerations for obtaining high-quality data. Nat Immunol 12:918-922. doi:10.1038/ni. 2117. PubMed: 21934668.
36. Fan X, Struhl K (2009) Where does mediator bind in vivo? PLOS ONE 4:e5029. doi:10.1371/journal.pone.0005029. PubMed: 19343176.
37. Zhu X, Wirén M, Sinha I, Rasmussen NN, Linder T et al. (2006) Genome-wide occupancy profile of mediator and the Srb8-11 module reveals interactions with coding regions. Mol Cell 22:169-178. doi: 10.1016/j.molcel. 2006.03.032. PubMed: 16630887.
38. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD (2007) FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res 17:877-885. doi:10.1101/gr.5533506. PubMed: 17179217. (Pubitemid 46919722)
39. Auerbach RK, Euskirchen G, Rozowsky J, Lamarre-Vincent N, Moqtaderi Z et al. (2009) Mapping accessible chromatin regions using Sono-Seq. Proc Natl Acad Sci U S A 106:14926-14931. doi:10.1073/pnas.0905443106. PubMed: 19706456.
40. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT et al. (2012) The accessible chromatin landscape of the human genome. Nature 489:75-82. doi:10.1038/nature11232. PubMed: 22955617.
41. Moorman C, Sun LV, Wang J, De Wit E, Talhout W et al. (2006) Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci U S A 103:12027-12032. doi:10.1073/pnas.0605003103. PubMed: 16880385. (Pubitemid 44215805)
42. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6:e27. doi:10.1371/journal.pbio. 0060027. PubMed: 18271625.
43. Zaret K (2005) Micrococcal nuclease analysis of chromatin structure. Curr Protoc Mol Biol Chapter 21: Unit 21.1
44. Van Dijk EL, Chen CL, D'Aubenton-Carafa Y, Gourvennec S, Kwapisz M et al. (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475:114-117. doi:10.1038/nature10118. PubMed: 21697827.
45. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728. doi:10.1016/S0092-8674 (00) 81641-4. PubMed: 9845373. (Pubitemid 28544132)