Cited by 217Genomics and Chromatin DynamicsChromatin Remodeling and CancerDiffusion and Search Dynamics

The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding

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Li, Xiao-Yong, Thomas, Sean, Sabo, Peter J, Eisen, Michael B, Stamatoyannopoulos, John A, Biggin, Mark D·2011·Genome Biology

Abstract

Background: In Drosophila embryos, many biochemically and functionally unrelated transcription factors bind quantitatively to highly overlapping sets of genomic regions, with much of the lowest levels of binding being incidental, non-functional interactions on DNA. The primary biochemical mechanisms that drive these genome-wide occupancy patterns have yet to be established. Results: Here we use data resulting from the DNaseI digestion of isolated embryo nuclei to provide a biophysical measure of the degree to which proteins can access different regions of the genome. We show that the in vivo binding patterns of 21 developmental regulators are quantitatively correlated with DNA accessibility in chromatin. Furthermore, we find that levels of factor occupancy in vivo correlate much more with the degree of chromatin accessibility than with occupancy predicted from in vitro affinity measurements using purified protein and naked DNA. Within accessible regions, however, the intrinsic affinity of the factor for DNA does play a role in determining net occupancy, with even weak affinity recognition sites contributing. Finally, we show that programmed changes in chromatin accessibility between different developmental stages correlate with quantitative alterations in factor binding. Conclusions: Based on these and other results, we propose a general mechanism to explain the widespread, overlapping DNA binding by animal transcription factors. In this view, transcription factors are expressed at sufficiently high concentrations in cells such that they can occupy their recognition sequences in highly accessible chromatin without the aid of physical cooperative interactions with other proteins, leading to highly overlapping, graded binding of unrelated factors.

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  • Other RFX members have been demonstrated to regulate MHC class II expression.

    “as other RFX members have been demonstrated to regulate MHC class II expression 35,64”

    From Type 1 interferon perturbates clonal competition by reshaping human blood development (2026) · cites this paper as [64]

    Our copy’s Discussion addresses chromatin accessibility and transcription-factor binding in Drosophila, not regulation of MHC class II expression. Searches for RFX, MHC class II, and major histocompatibility complex found no passage addressing the claim. (LLM, conf=0.75)

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  1. Walter J Dever CA Biggin MD Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev 1994 8 1678 1692 10.1101/gad.8.14.1678 7958848 · DOI
  2. Liang Z Biggin MD Eve and ftz regulate a wide array of genes in blastoderm embryos: the selector homeoproteins directly or indirectly regulate most genes in Drosophila. Development 1998 125 4471 4482 9778506
  3. Carr A Biggin MD A comparison of in vivo and in vitro DNA-binding specificities suggests a new model for homeoprotein DNA binding in Drosophila embryos. EMBO J 1999 18 1598 1608 10.1093/emboj/18.6.1598 10075930 PMC1171247 · DOI
  4. Boyer LA Lee TI Cole MF Johnstone SE Levine SS Zucker JP Guenther MG Kumar RM Murray HL Jenner RG Gifford DK Melton DA Jaenisch R Young RA Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005 122 947 956 10.1016/j.cell.2005.08.020 16153702 PMC3006442 · DOI · Paper page
  5. Bieda M Xu X Singer MA Green R Farnham PJ Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006 16 595 605 10.1101/gr.4887606 16606705 PMC1457046 · DOI
  6. Yang A Zhu Z Kapranov P McKeon F Church GM Gingeras TR Struhl K Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006 24 593 602 10.1016/j.molcel.2006.10.018 17188034 · DOI
  7. Zeitlinger J Zinzen RP Stark A Kellis M Zhang H Young RA Levine M Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 2007 21 385 390 10.1101/gad.1509607 17322397 PMC1804326 · DOI · Paper page
  8. Johnson DS Mortazavi A Myers RM Wold B Genome-wide mapping of in vivo protein-DNA interactions. Science 2007 316 1497 1502 10.1126/science.1141319 17540862 · DOI · Paper page
  9. Robertson G Hirst M Bainbridge M Bilenky M Zhao Y Zeng T Euskirchen G Bernier B Varhol R Delaney A Thiessen N Griffith OL He A Marra M Snyder M Jones S Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 2007 4 651 657 10.1038/nmeth1068 17558387 · DOI · Paper page
  10. Chen X Xu H Yuan P Fang F Huss M Vega VB Wong E Orlov YL Zhang W Jiang J Loh YH Yeo HC Yeo ZX Narang V Govindarajan KR Leong B Shahab A Ruan Y Bourque G Sung WK Clarke ND Wei CL Ng HH Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008 133 1106 1117 10.1016/j.cell.2008.04.043 18555785 · DOI
  11. Consortium TEP Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007 447 799 816 10.1038/nature05874 17571346 PMC2212820 · DOI · Paper page
  12. Georlette D Ahn S MacAlpine DM Cheung E Lewis PW Beall EL Bell SP Speed T Manak JR Botchan MR Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 2007 21 2880 2896 10.1101/gad.1600107 17978103 PMC2049191 · DOI
  13. Li XY MacArthur S Bourgon R Nix D Pollard DA Iyer VN Hechmer A Simirenko L Stapleton M Luengo Hendriks CL Chu HC Ogawa N Inwood W Sementchenko V Beaton A Weiszmann R Celniker SE Knowles DW Gingeras T Speed TP Eisen MB Biggin MD Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 2008 6 e27 10.1371/journal.pbio.0060027 18271625 PMC2235902 · DOI
  14. Fullwood MJ Liu MH Pan YF Liu J Xu H Mohamed YB Orlov YL Velkov S Ho A Mei PH Chew EG Huang PY Welboren WJ Han Y Ooi HS Ariyaratne PN Vega VB Luo Y Tan PY Choy PY Wansa KD Zhao B Lim KS Leow SC Yow JS Joseph R Li H Desai KV Thomsen JS Lee YK An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009 462 58 64 10.1038/nature08497 19890323 PMC2774924 · DOI
  15. Boj SF Servitja JM Martin D Rios M Talianidis I Guigo R Ferrer J Functional targets of the monogenic diabetes transcription factors HNF-1alpha and HNF-4alpha are highly conserved between mice and humans. Diabetes 2009 58 1245 1253 10.2337/db08-0812 19188435 PMC2671044 · DOI
  16. MacArthur S Li XY Li J Brown JB Chu HC Zeng L Grondona BP Hechmer A Simirenko L Keranen SV Knowles DW Stapleton M Bickel P Biggin MD Eisen MB Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol 2009 10 R80 10.1186/gb-2009-10-7-r80 19627575 PMC2728534 · DOI
  17. Cao Y Yao Z Sarkar D Lawrence M Sanchez GJ Parker MH MacQuarrie KL Davison J Morgan MT Ruzzo WL Gentleman RC Tapscott SJ Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 2010 18 662 674 10.1016/j.devcel.2010.02.014 20412780 PMC2910615 · DOI
  18. Bradley RK Li XY Trapnell C Davidson S Pachter L Chu HC Tonkin LA Biggin MD Eisen MB Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 2010 8 e1000343 10.1371/journal.pbio.1000343 20351773 PMC2843597 · DOI
  19. Moorman C Sun LV Wang J de Wit E Talhout W Ward LD Greil F Lu XJ White KP Bussemaker HJ van Steensel B Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci USA 2006 103 12027 12032 10.1073/pnas.0605003103 16880385 PMC1567692 · DOI
  20. Zinzen RP Girardot C Gagneur J Braun M Furlong EE Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009 462 65 70 10.1038/nature08531 19890324 · DOI
  21. 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 USA 2009 106 21521 21526 10.1073/pnas.0904863106 19995984 PMC2789751 · DOI
  22. Wunderlich Z Mirny LA Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 2009 25 434 440 10.1016/j.tig.2009.08.003 19815308 PMC3697852 · DOI
  23. Iyer VR Horak CE Scafe CS Botstein D Snyder M Brown PO Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 2001 409 533 538 10.1038/35054095 11206552 · DOI
  24. Liu X Lee CK Granek JA Clarke ND Lieb JD Whole-genome comparison of Leu3 binding in vitro and in vivo reveals the importance of nucleosome occupancy in target site selection. Genome Res 2006 16 1517 1528 10.1101/gr.5655606 17053089 PMC1665635 · DOI
  25. Johnson AD Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Genet Dev 1995 5 552 558 10.1016/0959-437X(95)80022-0 8664541 · DOI
  26. Thanos D Maniatis T Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 1995 83 1091 1100 10.1016/0092-8674(95)90136-1 8548797 · DOI · Paper page
  27. Bolouri H Davidson EH Transcriptional regulatory cascades in development: initial rates, not steady state, determine network kinetics. Proc Natl Acad Sci USA 2003 100 9371 9376 10.1073/pnas.1533293100 12883007 PMC170925 · DOI
  28. Oliveri P Tu Q Davidson EH Global regulatory logic for specification of an embryonic cell lineage. Proc Natl Acad Sci USA 2008 105 5955 5962 10.1073/pnas.0711220105 18413610 PMC2329687 · DOI · Paper page
  29. Mann RS Lelli KM Joshi R Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 2009 88 63 101 full_text 19651302 PMC2810641
  30. Wu C Two protein-binding sites in chromatin implicated in the activation of heat shock genes. Nature 1984 309 229 234 10.1038/309229a0 6325944 · DOI
  31. Wallrath LL Lu Q Granok H Elgin SC Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. Bioessays 1994 16 165 170 10.1002/bies.950160306 8166669 · DOI
  32. Felsenfeld G Groudine M Controlling the double helix. Nature 2003 421 448 453 10.1038/nature01411 12540921 · DOI
  33. Li B Carey M Workman JL The role of chromatin during transcription. Cell 2007 128 707 719 10.1016/j.cell.2007.01.015 17320508 · DOI
  34. Berger SL The complex language of chromatin regulation during transcription. Nature 2007 447 407 412 10.1038/nature05915 17522673 · DOI · Paper page
  35. Boeger H Griesenbeck J Kornberg RD Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 2008 133 716 726 10.1016/j.cell.2008.02.051 18485878 PMC2409070 · DOI
  36. Henikoff S Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet 2008 9 15 26 10.1038/nrg2206 18059368 · DOI
  37. Cairns BR The logic of chromatin architecture and remodelling at promoters. Nature 2009 461 193 198 10.1038/nature08450 19741699 · DOI
  38. Floer M Wang X Prabhu V Berrozpe G Narayan S Spagna D Alvarez D Kendall J Krasnitz A Stepansky A Hicks J Bryant GO Ptashne M A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 2010 141 407 418 10.1016/j.cell.2010.03.048 20434983 PMC3032599 · DOI
  39. Felsenfeld G Chromatin unfolds. Cell 1996 86 13 19 10.1016/S0092-8674(00)80073-2 8689680 · DOI
  40. Carr A Biggin MD Accessibility of transcriptionally inactive genes in specifically reduced at homeoprotein-DNA binding sites in Drosophila. Nucleic Acids Res 2000 28 2839 2846 10.1093/nar/28.14.2839 10908343 PMC102649 · DOI
  41. Morse RH Transcription factor access to promoter elements. J Cell Biochem 2007 102 560 570 10.1002/jcb.21493 17668451 · DOI
  42. Boyle AP Davis S Shulha HP Meltzer P Margulies EH Weng Z Furey TS Crawford GE High-resolution mapping and characterization of open chromatin across the genome. Cell 2008 132 311 322 10.1016/j.cell.2007.12.014 18243105 PMC2669738 · DOI · Paper page
  43. John S Sabo PJ Johnson TA Sung MH Biddie SC Lightman SL Voss TC Davis SR Meltzer PS Stamatoyannopoulos JA Hager GL Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 2008 29 611 624 10.1016/j.molcel.2008.02.010 18342607 · DOI
  44. Biggin MD McGinnis W Regulation of segmentation and segmental identity by Drosophila homeoproteins: the role of DNA binding in functional activity and specificity. Development 1997 124 4425 4433 9409661
  45. Fascher KD Schmitz J Horz W Role of trans-activating proteins in the generation of active chromatin at the PHO5 promoter in S. cerevisiae. EMBO J 1990 9 2523 2528 2196175 PMC552282
  46. Taylor IC Workman JL Schuetz TJ Kingston RE Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev 1991 5 1285 1298 10.1101/gad.5.7.1285 2065977 · DOI
  47. Archer TK Lefebvre P Wolford RG Hager GL Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science 1992 255 1573 1576 10.1126/science.1347958 1347958 · DOI
  48. Adams CC Workman JL Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol Cell Biol 1995 15 1405 1421 7862134 PMC230365
  49. Polach KJ Widom J A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J Mol Biol 1996 258 800 812 10.1006/jmbi.1996.0288 8637011 · DOI
  50. Vashee S Melcher K Ding WV Johnston SA Kodadek T Evidence for two modes of cooperative DNA binding in vivo that do not involve direct protein-protein interactions. Curr Biol 1998 8 452 458 10.1016/S0960-9822(98)70179-4 9550700 · DOI
  51. Miller JA Widom J Collaborative competition mechanism for gene activation in vivo. Mol Cell Biol 2003 23 1623 1632 10.1128/MCB.23.5.1623-1632.2003 12588982 PMC151720 · DOI
  52. Hebbar PB Archer TK Chromatin-dependent cooperativity between site-specific transcription factors in vivo. J Biol Chem 2007 282 8284 8291 10.1074/jbc.M610554200 17186943 PMC2528297 · DOI
  53. Wasson T Hartemink AJ An ensemble model of competitive multi-factor binding of the genome. Genome Res 2009 19 2101 2112 10.1101/gr.093450.109 19720867 PMC2775586 · DOI
  54. Mirny L Nucleosome-mediated cooperativity between transcription factors. Proc Natl Acad Sci USA 2010 107 22534 22539 10.1073/pnas.0913805107 21149679 PMC3012490 · DOI · Paper page
  55. Peterson CL Tamkun JW The SWI-SNF complex: a chromatin remodeling machine? Trends Biochem Sci 1995 20 143 146 10.1016/S0968-0004(00)88990-2 7770913 · DOI
  56. Kadonaga JT Eukaryotic transcription: an interlaced network of transcription factors and chromatin-modifying machines. Cell 1998 92 307 313 10.1016/S0092-8674(00)80924-1 9476891 · DOI
  57. Wu C The 5' end of Drosophila heat shock genes in chromatin are hypersensitive to DNAse I. Nature 1980 286 854 860 10.1038/286854a0 6774262 · DOI
  58. Elgin SC Anatomy of hypersensitive sites. Nature 1984 309 213 214 10.1038/309213a0 6325942 · DOI
  59. Gross DS Garrard WT Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 1988 57 159 197 10.1146/annurev.bi.57.070188.001111 3052270 · DOI
  60. Sekimata M Perez-Melgosa M Miller SA Weinmann AS Sabo PJ Sandstrom R Dorschner MO Stamatoyannopoulos JA Wilson CB CCCTC-binding factor and the transcription factor T-bet orchestrate T helper 1 cell-specific structure and function at the interferon-gamma locus. Immunity 2009 31 551 564 10.1016/j.immuni.2009.08.021 19818655 PMC2810421 · DOI
  61. Campos-Ortega JA Hartenstein V The Embryonic Development of Drosophila melanogaster 1997 2 Berlin: Springer-Verlag
  62. Toth J Biggin MD The specificity of protein-DNA crosslinking by formaldehyde: in vitro and in Drosophila embryos. Nucleic Acids Res 2000 28 e4 10.1093/nar/28.2.e4 10606672 PMC102536 · DOI
  63. Auerbach RK Euskirchen G Rozowsky J Lamarre-Vincent N Moqtaderi Z Lefrancois P Struhl K Gerstein M Snyder M Mapping accessible chromatin regions using Sono-Seq. Proc Natl Acad Sci USA 2009 106 14926 14931 10.1073/pnas.0905443106 19706456 PMC2736440 · DOI
  64. Arnosti DN Barolo S Levine M Small S The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 1996 122 205 214 8565831
  65. Fujioka M Emi-Sarker Y Yusibova GL Goto T Jaynes JB Analysis of an even-skipped rescue transgene reveals both composite and discrete neuronal and early blastoderm enhancers, and multi-stripe positioning by gap gene repressor gradients. Development 1999 126 2527 2538 10226011 PMC2778309
  66. Clyde DE Corado MS Wu X Pare A Papatsenko D Small S A self-organizing system of repressor gradients establishes segmental complexity in Drosophila. Nature 2003 426 849 853 10.1038/nature02189 14685241 · DOI
  67. Halfon MS Gallo SM Bergman CM REDfly 2.0: an integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila. Nucleic Acids Res 2008 36 D594 598 10.1093/nar/gkm876 18039705 PMC2238825 · DOI
  68. Kambadur R Koizumi K Stivers C Nagle J Poole SJ Odenwald WF Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev 1998 12 246 260 10.1101/gad.12.2.246 9436984 PMC316437 · DOI
  69. Knirr S Frasch M Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev Biol 2001 238 13 26 10.1006/dbio.2001.0397 11783990 · DOI
  70. Raftery LA Sutherland DJ TGF-beta family signal transduction in Drosophila development: from Mad to Smads. Dev Biol 1999 210 251 268 10.1006/dbio.1999.9282 10357889 · DOI
  71. Sutherland DJ Li M Liu XQ Stefancsik R Raftery LA Stepwise formation of a SMAD activity gradient during dorsal-ventral patterning of the Drosophila embryo. Development 2003 130 5705 5716 10.1242/dev.00801 14534137 · DOI
  72. Kaplan T Li XY Sabo PJ Thomas S Stamatoyannopoulos JA Biggin MD Eisen MB Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet 2011 7 e1001290 10.1371/journal.pgen.1001290 21304941 PMC3033374 · DOI
  73. John S Sabo PJ Thurman RE Sung MH Biddie SC Johnson TA Hager GL Stamatoyannopoulos JA Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 2011 43 264 268 10.1038/ng.759 21258342 PMC6386452 · DOI · Paper page
  74. Lin S Riggs AD The general affinity of lac repressor for E. coli DNA: Implications for gene regulation in procaryotes and eukaryotes. Cell 1975 4 107 111 10.1016/0092-8674(75)90116-6 1092468 · DOI · Paper page
  75. von Hippel PH Revzin A Gross CA Wang AC Nonspecific DNA binding of genome regulating proteins as a biological control mechanism: 1. The lac operon: Equilibrium aspects. Proc Natl Acad Sci USA 1974 71 4808 4812 10.1073/pnas.71.12.4808 4612528 PMC433986 · DOI
  76. Yang Sw Nash HA Comparison of protein binding to DNA in vivo and in vitro: defining an effective intracellular target. EMBO J 1995 14 6292 6300 8557048 PMC394753
  77. Janssen S Cuvier O Muller M Laemmli UK Specific gain- and loss-of-function phenotypes induced by satellite-specific DNA-binding drugs fed to Drosophila melanogaster. Mol Cell 2000 6 1013 1024 10.1016/S1097-2765(00)00100-3 11106741 · DOI
  78. Phair RD Scaffidi P Elbi C Vecerova J Dey A Ozato K Brown DT Hager G Bustin M Misteli T Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol Cell Biol 2004 24 6393 6402 10.1128/MCB.24.14.6393-6402.2004 15226439 PMC434243 · DOI
  79. Liu X Wu B Szary J Kofoed EM Schaufele F Functional sequestration of transcription factor activity by repetitive DNA. J Biol Chem 2007 282 20868 20876 10.1074/jbc.M702547200 17526489 PMC3812952 · DOI
  80. Garvie CW Wolberger C Recognition of specific DNA sequences. Mol Cell 2001 8 937 946 10.1016/S1097-2765(01)00392-6 11741530 · DOI
  81. Krause HM Klemenz R Gehring WJ Expression, modification, and localization of the fushi tarazu protein in Drosophila embryos. Genes Dev 1988 2 1021 1036 10.1101/gad.2.8.1021 3049237 · DOI
  82. Hahn MW Stajich JE Wray GA The effects of selection against spurious transcription factor binding sites. Mol Biol Evol 2003 20 901 906 10.1093/molbev/msg096 12716998 · DOI
  83. Wagner A A computational genomics approach to the identification of gene networks. Nucleic Acids Res 1997 25 3594 3604 10.1093/nar/25.18.3594 9278479 PMC146952 · DOI
  84. Wasserman WW Fickett JW Identification of regulatory regions which confer muscle-specific gene expression. J Mol Biol 1998 278 167 181 10.1006/jmbi.1998.1700 9571041 · DOI
  85. Kel AE Kel-Margoulis OV Farnham PJ Bartley SM Wingender E Zhang MQ Computer-assisted identification of cell cycle-related genes: new targets for E2F transcription factors. J Mol Biol 2001 309 99 120 10.1006/jmbi.2001.4650 11491305 · DOI
  86. Schroeder MD Pearce M Fak J Fan H Unnerstall U Emberly E Rajewsky N Siggia ED Gaul U Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol 2004 2 E271 10.1371/journal.pbio.0020271 15340490 PMC514885 · DOI
  87. 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 10.1186/gb-2004-5-9-r61 15345045 PMC522868 · DOI
  88. Kantorovitz MR Kazemian M Kinston S Miranda-Saavedra D Zhu Q Robinson GE Gottgens B Halfon MS Sinha S Motif-blind, genome-wide discovery of cis-regulatory modules in Drosophila and mouse. Dev Cell 2009 17 568 579 10.1016/j.devcel.2009.09.002 19853570 PMC2768654 · DOI
  89. Narlikar L Gordan R Hartemink AJ A nucleosome-guided map of transcription factor binding sites in yeast. PLoS Comput Biol 2007 3 e215 10.1371/journal.pcbi.0030215 17997593 PMC2065891 · DOI
  90. Lahdesmaki H Rust AG Shmulevich I Probabilistic inference of transcription factor binding from multiple data sources. PLoS One 2008 3 e1820 10.1371/journal.pone.0001820 18364997 PMC2268002 · DOI
  91. Ward LD Bussemaker HJ Predicting functional transcription factor binding through alignment-free and affinity-based analysis of orthologous promoter sequences. Bioinformatics 2008 24 i165 171 10.1093/bioinformatics/btn154 18586710 PMC2718632 · DOI
  92. Dai Z Dai X Xiang Q Feng J Nucleosomal context of binding sites influences transcription factor binding affinity and gene regulation. Genomics Proteomics Bioinformatics 2009 7 155 162 10.1016/S1672-0229(08)60045-5 20172488 PMC5054407 · DOI
  93. Whitington T Perkins AC Bailey TL High-throughput chromatin information enables accurate tissue-specific prediction of transcription factor binding sites. Nucleic Acids Res 2009 37 14 25 10.1093/nar/gkn866 18988630 PMC2662491 · DOI
  94. 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 10.1101/gr.096305.109 20219943 PMC2847756 · DOI
  95. Ramsey SA Knijnenburg TA Kennedy KA Zak DE Gilchrist M Gold ES Johnson CD Lampano AE Litvak V Navarro G Stolyar T Aderem A Shmulevich I Genome-wide histone acetylation data improve prediction of mammalian transcription factor binding sites. Bioinformatics 2010 26 2071 2075 10.1093/bioinformatics/btq405 20663846 PMC2922897 · DOI
  96. Walter J Biggin MD DNA binding specificity of two homeodomain proteins in vitro and in Drosophila embryos. Proc Natl Acad Sci USA 1996 93 2680 2685 10.1073/pnas.93.7.2680 8610101 PMC39690 · DOI
  97. Sabo PJ Kuehn MS Thurman R Johnson BE Johnson EM Cao H Yu M Rosenzweig E Goldy J Haydock A Weaver M Shafer A Lee K Neri F Humbert R Singer MA Richmond TA Dorschner MO McArthur M Hawrylycz M Green RD Navas PA Noble WS Stamatoyannopoulos JA Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 2006 3 511 518 10.1038/nmeth890 16791208 · DOI
  98. Bickel PJ Boley N Brown JB Huang H Zhang NR Subsampling methods for genomic inference. Ann Appl Stat 2010 in press
  99. Bailey TL Boden M Buske FA Frith M Grant CE Clementi L Ren J Li WW Noble WS MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009 37 W202 208 10.1093/nar/gkp335 19458158 PMC2703892 · DOI · Paper page
  100. Gupta S Stamatoyannopoulos JA Bailey TL Noble WS Quantifying similarity between motifs. Genome Biol 2007 8 R24 10.1186/gb-2007-8-2-r24 17324271 PMC1852410 · DOI · Paper page

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Authors
Li, X.-Y., Thomas, S., Sabo, P. J., Eisen, M. B., Stamatoyannopoulos, J. A., & Biggin, M. D.
Affiliations
  • University of Washington (US)
  • Howard Hughes Medical Institute (US)
  • Lawrence Berkeley National Laboratory (US)
Corresponding author
  • Stamatoyannopoulos, John A
  • Biggin, Mark D
Venue
Genome Biology
Published
2011-04-07
Volume
12
Issue
4
Pages
R34-R34
ISSN
  • 1465-6906 (ISSN-L)
  • 1474-760X
OpenAlex
W2155718935
Cited by
217
References
6
Citations by year
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FWCI
10.84
Type
journal article
Language
en
Open access
Locations
  • Genome biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • U.S. Department of Energy (-AC02-05CH11231, 05CH11231, DE AC02 05CH11231, DE-AC02-)
  • National Institutes of Health (DE-AC02–05CH11231, 5t90hg004007-05)
  • National Human Genome Research Institute (T90 HG 004007-04)
  • National Institute of General Medical Sciences (GM704403, R01GM071923, R01GM070444)
  • Lawrence Berkeley National Laboratory (AC02‐05CH11231, DE-AC02-05CH11231, 05CH11231)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Diffusion and Search Dynamics
Keywords
chromatin accessibility, transcription factor binding, Drosophila embryo, DNase I footprinting, developmental regulators, transcriptional regulation
MeSH terms
Animals, Base Sequence, Binding Sites, Cell Nucleus, Chromatin, Deoxyribonuclease I, DNA, DNA-Binding Proteins, Drosophila melanogaster, Models, Genetic, Protein Binding, Transcription Factors, Computational Biology, Chromatin Immunoprecipitation, Genome, Insect

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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