CoChat
Sign Up
Cited by 96Genomics and Chromatin DynamicsGenetic Associations and EpidemiologyBioinformatics and Genomic Networks

Multi-species, multi-transcription factor binding highlights conserved control of tissue-specific biological pathways

Open access
Ballester, Benoit, Medina-Rivera, Alejandra, Schmidt, Dominic, Gonzàlez-Porta, Mar, Carlucci, Matthew, Chen, Xiaoting, Chessman, Kyle, Faure, Andre J +14 more·2014·eLife
DOI 10.7554/elife.02626PMC PMC4359374
Open this paper in CoChat — free account

Abstract

As exome sequencing gives way to genome sequencing, the need to interpret the function of regulatory DNA becomes increasingly important. To test whether evolutionary conservation of cis-regulatory modules (CRMs) gives insight into human gene regulation, we determined transcription factor (TF) binding locations of four liver-essential TFs in liver tissue from human, macaque, mouse, rat, and dog. Approximately, two thirds of the TF-bound regions fell into CRMs. Less than half of the human CRMs were found as a CRM in the orthologous region of a second species. Shared CRMs were associated with liver pathways and disease loci identified by genome-wide association studies. Recurrent rare human disease causing mutations at the promoters of several blood coagulation and lipid metabolism genes were also identified within CRMs shared in multiple species. This suggests that multi-species analyses of experimentally determined combinatorial TF binding will help identify genomic regions critical for tissue-specific gene control.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.02626

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 82

  1. 1000 Genomes Project Consortium Abecasis GR Altshuler D Auton A Brooks LD Durbin RM Gibbs RA Hurles ME McVean GA 2010 A map of human genome variation from population-scale sequencing Nature 467 1061 1073 10.1038/nature09534 20981092 PMC3042601 · DOI · Paper page
  2. 1000 Genomes Project Consortium Abecasis GR Auton A Brooks LD DePristo MA Durbin RM Handsaker RE Kang HM Marth GT McVean GA 2012 An integrated map of genetic variation from 1,092 human genomes Nature 491 56 65 10.1038/nature11632 23128226 PMC3498066 · DOI · Paper page
  3. Badis G Berger MF Philippakis AA Talukder S Gehrke AR Jaeger SA Chan ET Metzler G Vedenko A Chen X Kuznetsov H Wang CF Coburn D Newburger DE Morris Q Hughes TR Bulyk ML 2009 Diversity and complexity in DNA recognition by transcription factors Science 324 1720 1723 10.1126/science.1162327 19443739 PMC2905877 · DOI
  4. Bailey TL Boden M Buske FA Frith M Grant CE Clementi L Ren J Li WW Noble WS 2009 MEME SUITE: tools for motif discovery and searching Nucleic Acids Research 37 W202 W208 10.1093/nar/gkp335 19458158 PMC2703892 · DOI · Paper page
  5. Blow MJ McCulley DJ Li Z Zhang T Akiyama JA Holt A Plajzer-Frick I Shoukry M Wright C Chen F Afzal V Bristow J Ren B Black BL Rubin EM Visel A Pennacchio LA 2010 ChIP-Seq identification of weakly conserved heart enhancers Nature Genetics 42 806 810 10.1038/ng.650 20729851 PMC3138496 · DOI
  6. Bond GL Hu W Bond EE Robins H Lutzker SG Arva NC Bargonetti J Bartel F Taubert H Wuerl P Onel K Yip L Hwang SJ Strong LC Lozano G Levine AJ 2004 A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans Cell 119 591 602 10.1016/j.cell.2004.11.022 15550242 · DOI · Paper page
  7. Boyle AP Hong EL Hariharan M Cheng Y Schaub MA Kasowski M Karczewski KJ Park J Hitz BC Weng S Cherry JM Snyder M 2012 Annotation of functional variation in personal genomes using RegulomeDB Genome Research 22 1790 1797 10.1101/gr.137323.112 22955989 PMC3431494 · DOI · Paper page
  8. Claussnitzer M Dankel SN Klocke B Grallert H Glunk V Berulava T Lee H Oskolkov N Fadista J Ehlers K Wahl S Hoffmann C Qian K Rönn T Riess H Müller-Nurasyid M Bretschneider N Schroeder T Skurk T Horsthemke B, DIAGRAM+Consortium Spieler D Klingenspor M Seifert M Kern MJ Mejhert N Dahlman I Hansson O Hauck SM Blüher M Arner P Groop L Illig T Suhre K Hsu YH Mellgren G Hauner H Laumen H 2014 Leveraging cross-species transcription factor binding site patterns: from diabetes risk loci to disease mechanisms Cell 156 343 358 10.1016/j.cell.2013.10.058 24439387 PMC7116609 · DOI
  9. Cooper GM Stone EA Asimenos G, NISC Comparative Sequencing Program Green ED Batzoglou S Sidow A 2005 Distribution and intensity of constraint in mammalian genomic sequence Genome Research 15 901 913 10.1101/gr.3577405 15965027 PMC1172034 · DOI · Paper page
  10. Cotney J Leng J Yin J Reilly SK DeMare LE Emera D Ayoub AE Rakic P Noonan JP 2013 The evolution of lineage-specific regulatory activities in the human embryonic limb Cell 154 185 196 10.1016/j.cell.2013.05.056 23827682 PMC3785101 · DOI
  11. Crossley M Brownlee GG 1990 Disruption of a C/EBP binding site in the factor IX promoter is associated with haemophilia B Nature 345 444 446 10.1038/345444a0 2342576 · DOI
  12. Crossley M Ludwig M Stowell KM De Vos P Olek K Brownlee GG 1992 Recovery from hemophilia B Leyden: an androgen-responsive element in the factor IX promoter Science 257 377 379 10.1126/science.1631558 1631558 · DOI
  13. ENCODE Project Consortium 2012 An integrated encyclopedia of DNA elements in the human genome Nature 489 57 74 10.1038/nature11247 22955616 PMC3439153 · DOI · Paper page
  14. Ernst J Kellis M 2013 Interplay between chromatin state, regulator binding, and regulatory motifs in six human cell types Genome Research 23 1142 1154 10.1101/gr.144840.112 23595227 PMC3698507 · DOI
  15. Erwin GD Oksenberg N Truty RM Kostka D Murphy KK Ahituv N Pollard KS Capra JA 2014 Integrating diverse datasets improves developmental enhancer prediction PLOS Computational Biology 10 e1003677 10.1371/journal.pcbi.1003677 24967590 PMC4072507 · DOI
  16. Fisher WW Li JJ Hammonds AS Brown JB Pfeiffer BD Weiszmann R Macarthur S Thomas S Stamatoyannopoulos JA Eisen MB Bickel PJ Biggin MD Celniker SE 2012 DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila Proceedings of the National Academy of Sciences of USA 109 21330 21335 10.1073/pnas.1209589110 PMC3535648 23236164 · DOI
  17. Flicek P Aken BL Ballester B Beal K Bragin E Brent S Chen Y Clapham P Coates G Fairley S Fitzgerald S Fernandez-Banet J Gordon L Gräf S Haider S Hammond M Howe K Jenkinson A Johnson N Kähäri A Keefe D Keenan S Kinsella R Kokocinski F Koscielny G Kulesha E Lawson D Longden I Massingham T McLaren W Megy K Overduin B Pritchard B Rios D Ruffier M Schuster M Slater G Smedley D Spudich G Tang YA Trevanion S Vilella A Vogel J White S Wilder SP Zadissa A Birney E Cunningham F Dunham I Durbin R Fernández-Suarez XM Herrero J Hubbard TJ Parker A Proctor G Smith J Searle SM 2010 Ensembl's 10th year Nucleic Acids Research 38 D557 D562 10.1093/nar/gkp972 19906699 PMC2808936 · DOI
  18. Funnell AP Wilson MD Ballester B Mak KS Burdach J Magan N Pearson RC Lemaigre FP Stowell KM Odom DT Flicek P Crossley M 2013 A CpG mutational hotspot in a onecut binding site accounts for the prevalent variant of hemophilia B leyden The American Journal of Human Genetics 92 460 467 10.1016/j.ajhg.2013.02.003 PMC3591849 23472758 · DOI
  19. Furey TS 2012 ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions Nature Reviews Genetics 13 840 852 10.1038/nrg3306 PMC3591838 23090257 · DOI
  20. Gerstein MB Kundaje A Hariharan M Landt SG Yan KK Cheng C Mu XJ Khurana E Rozowsky J Alexander R Min R Alves P Abyzov A Addleman N Bhardwaj N Boyle AP Cayting P Charos A Chen DZ Cheng Y Clarke D Eastman C Euskirchen G Frietze S Fu Y Gertz J Grubert F Harmanci A Jain P Kasowski M Lacroute P Leng J Lian J Monahan H O'Geen H Ouyang Z Partridge EC Patacsil D Pauli F Raha D Ramirez L Reddy TE Reed B Shi M Slifer T Wang J Wu L Yang X Yip KY Zilberman-Schapira G Batzoglou S Sidow A Farnham PJ Myers RM Weissman SM Snyder M 2012 Architecture of the human regulatory network derived from ENCODE data Nature 489 91 100 10.1038/nature11245 22955619 PMC4154057 · DOI
  21. Giannelli F Green PM Sommer SS Poon M Ludwig M Schwaab R Reitsma PH Goossens M Yoshioka A Figueiredo MS Brownlee GG 1998 Haemophilia B: database of point mutations and short additions and deletions–eighth edition Nucleic Acids Research 26 265 268 10.1093/nar/26.1.265 9399849 PMC147172 · DOI
  22. Gibbs RA Weinstock GM Metzker ML Muzny DM Sodergren EJ Scherer S Scott G Steffen D Worley KC Burch PE Okwuonu G Hines S Lewis L DeRamo C Delgado O Dugan-Rocha S Miner G Morgan M Hawes A Gill R Celera Holt RA Adams C Amanatides PG Baden-Tillson H Barnstead M Chin S Evans CA Ferriera S Fosler C Glodek A Gu Z Jennings D Kraft CL Nguyen T Pfannkoch CM Sitter C Sutton GG Venter JC Woodage T Smith D Lee HM Gustafson E Cahill P Kana A Doucette-Stamm L Weinstock K Fechtel K Weiss RB Dunn DM Green ED Blakesley RW Bouffard GG De Jong PJ Osoegawa K Zhu B Marra M Schein J Bosdet I Fjell C Jones S Krzywinski M Mathewson C Siddiqui A Wye N McPherson J Zhao S Fraser CM Shetty J Shatsman S Geer K Chen Y Abramzon S Nierman WC Havlak PH Chen R Durbin KJ Egan A Ren Y Song XZ Li B Liu Y Qin X Cawley S Worley KC Cooney AJ D'Souza LM Martin K Wu JQ Gonzalez-Garay ML Jackson AR Kalafus KJ McLeod MP Milosavljevic A Virk D Volkov A Wheeler DA Zhang Z Bailey JA Eichler EE Tuzun E Birney E Mongin E Ureta-Vidal A Woodwark C Zdobnov E Bork P Suyama M Torrents D Alexandersson M Trask BJ Young JM Huang H Wang H Xing H Daniels S Gietzen D Schmidt J Stevens K Vitt U Wingrove J Camara F Mar Albà M Abril JF Guigo R Smit A Dubchak I Rubin EM Couronne O Poliakov A Hübner N Ganten D Goesele C Hummel O Kreitler T Lee YA Monti J Schulz H Zimdahl H Himmelbauer H Lehrach H Jacob HJ Bromberg S Gullings-Handley J Jensen-Seaman MI Kwitek AE Lazar J Pasko D Tonellato PJ Twigger S Ponting CP Duarte JM Rice S Goodstadt L Beatson SA Emes RD Winter EE Webber C Brandt P Nyakatura G Adetobi M Chiaromonte F Elnitski L Eswara P Hardison RC Hou M Kolbe D Makova K Miller W Nekrutenko A Riemer C Schwartz S Taylor J Yang S Zhang Y Lindpaintner K Andrews TD Caccamo M Clamp M Clarke L Curwen V Durbin R Eyras E Searle SM Cooper GM Batzoglou S Brudno M Sidow A Stone EA Venter JC Payseur BA Bourque G López-Otín C Puente XS Chakrabarti K Chatterji S Dewey C Pachter L Bray N Yap VB Caspi A Tesler G Pevzner PA Haussler D Roskin KM Baertsch R Clawson H Furey TS Hinrichs AS Karolchik D Kent WJ Rosenbloom KR Trumbower H Weirauch M Cooper DN Stenson PD Ma B Brent M Arumugam M Shteynberg D Copley RR Taylor MS Riethman H Mudunuri U Peterson J Guyer M Felsenfeld A Old S Mockrin S Collins F, Rat Genome Sequencing Project Consortium 2004 Genome sequence of the Brown Norway rat yields insights into mammalian evolution Nature 428 493 521 10.1038/nature02426 15057822 · DOI
  23. Gonzalez FJ Nebert DW 1990 Evolution of the P450 gene superfamily: animal-plant ‘warfare’, molecular drive and human genetic differences in drug oxidation Trends in Genetics 6 182 186 10.1016/0168-9525(90)90174-5 2196721 · DOI
  24. Goode DL Cooper GM Schmutz J Dickson M Gonzales E Tsai M Karra K Davydov E Batzoglou S Myers RM Sidow A 2010 Evolutionary constraint facilitates interpretation of genetic variation in resequenced human genomes Genome Research 20 301 310 10.1101/gr.102210.109 20067941 PMC2840986 · DOI
  25. Gordân R Narlikar L Hartemink AJ 2010 Finding regulatory DNA motifs using alignment-free evolutionary conservation information Nucleic Acids Research 38 e90 10.1093/nar/gkp1166 20047961 PMC2847231 · DOI
  26. Guo Y Mahony S Gifford DK 2012 High resolution genome wide binding event finding and motif discovery reveals transcription factor spatial binding constraints PLOS Computational Biology 8 e1002638 10.1371/journal.pcbi.1002638 22912568 PMC3415389 · DOI
  27. Hardison RC Taylor J 2012 Genomic approaches towards finding cis-regulatory modules in animals Nature Reviews Genetics 13 469 483 10.1038/nrg3242 PMC3541939 22705667 · DOI
  28. Hedges SB Dudley J Kumar S 2006 TimeTree: a public knowledge-base of divergence times among organisms Bioinformatics 22 2971 2972 10.1093/bioinformatics/btl505 17021158 · DOI · Paper page
  29. Heger A Webber C Goodson M Ponting CP Lunter G 2013 GAT: a simulation framework for testing the association of genomic intervals Bioinformatics 29 2046 2048 10.1093/bioinformatics/btt343 23782611 PMC3722528 · DOI
  30. Huang da W Sherman BT Lempicki RA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nature Protocols 4 44 57 10.1038/nprot.2008.211 19131956 · DOI · Paper page
  31. Hurtado A Holmes KA Ross-Innes CS Schmidt D Carroll JS 2011 FOXA1 is a key determinant of estrogen receptor function and endocrine response Nature Genetics 43 27 33 10.1038/ng.730 21151129 PMC3024537 · DOI
  32. Jolma A Yan J Whitington T Toivonen J Nitta KR Rastas P Morgunova E Enge M Taipale M Wei G Palin K Vaquerizas JM Vincentelli R Luscombe NM Hughes TR Lemaire P Ukkonen E Kivioja T Taipale J 2013 DNA-binding specificities of human transcription factors Cell 152 327 339 10.1016/j.cell.2012.12.009 23332764 · DOI
  33. Kim MJ Skewes-Cox P Fukushima H Hesselson S Yee SW Ramsey LB Nguyen L Eshragh JL Castro RA Wen CC Stryke D Johns SJ Ferrin TE Kwok PY Relling MV Giacomini KM Kroetz DL Ahituv N 2011 Functional characterization of liver enhancers that regulate drug-associated transporters Clinical Pharmacology and Therapeutics 89 571 578 10.1038/clpt.2010.353 21368754 PMC3227682 · DOI
  34. Kunarso G Chia NY Jeyakani J Hwang C Lu X Chan YS Ng HH Bourque G 2010 Transposable elements have rewired the core regulatory network of human embryonic stem cells Nature Genetics 42 631 634 10.1038/ng.600 20526341 · DOI
  35. Kutter C Brown GD Goncalves A Wilson MD Watt S Brazma A White RJ Odom DT 2011 Pol III binding in six mammals shows conservation among amino acid isotypes despite divergence among tRNA genes Nature Genetics 43 948 955 10.1038/ng.906 21873999 PMC3184141 · DOI
  36. Kyrmizi I Hatzis P Katrakili N Tronche F Gonzalez FJ Talianidis I 2006 Plasticity and expanding complexity of the hepatic transcription factor network during liver development Genes & Development 20 2293 2305 10.1101/gad.390906 16912278 PMC1553211 · DOI · Paper page
  37. Landt SG Marinov GK Kundaje A Kheradpour P Pauli F Batzoglou S Bernstein BE Bickel P Brown JB Cayting P Chen Y DeSalvo G Epstein C Fisher-Aylor KI Euskirchen G Gerstein M Gertz J Hartemink AJ Hoffman MM Iyer VR Jung YL Karmakar S Kellis M Kharchenko PV Li Q Liu T Liu XS Ma L Milosavljevic A Myers RM Park PJ Pazin MJ Perry MD Raha D Reddy TE Rozowsky J Shoresh N Sidow A Slattery M Stamatoyannopoulos JA Tolstorukov MY White KP Xi S Farnham PJ Lieb JD Wold BJ Snyder M 2012 ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia Genome Research 22 1813 1831 10.1101/gr.136184.111 22955991 PMC3431496 · DOI · Paper page
  38. Lenhard B Wasserman WW 2002 TFBS: computational framework for transcription factor binding site analysis Bioinformatics 18 1135 1136 10.1093/bioinformatics/18.8.1135 12176838 · DOI
  39. Li H Ruan J Durbin R 2008 Mapping short DNA sequencing reads and calling variants using mapping quality scores Genome Research 18 1851 1858 10.1101/gr.078212.108 18714091 PMC2577856 · DOI · Paper page
  40. Lindblad-Toh K Garber M Zuk O Lin MF Parker BJ Washietl S Kheradpour P Ernst J Jordan G Mauceli E Ward LD Lowe CB Holloway AK Clamp M Gnerre S Alföldi J Beal K Chang J Clawson H Cuff J Di Palma F Fitzgerald S Flicek P Guttman M Hubisz MJ Jaffe DB Jungreis I Kent WJ Kostka D Lara M Martins AL Massingham T Moltke I Raney BJ Rasmussen MD Robinson J Stark A Vilella AJ Wen J Xie X Zody MC, Broad Institute Sequencing Platform and Whole Genome Assembly Team Baldwin J Bloom T Chin CW Heiman D Nicol R Nusbaum C Young S Wilkinson J Worley KC Kovar CL Muzny DM Gibbs RA, Baylor College of Medicine Human Genome Sequencing Center Sequencing Team Cree A Dihn HH Fowler G Jhangiani S Joshi V Lee S Lewis LR Nazareth LV Okwuonu G Santibanez J Warren WC Mardis ER Weinstock GM Wilson RK, Genome Institute at Washington University Delehaunty K Dooling D Fronik C Fulton L Fulton B Graves T Minx P Sodergren E Birney E Margulies EH Herrero J Green ED Haussler D Siepel A Goldman N Pollard KS Pedersen JS Lander ES Kellis M 2011 A high-resolution map of human evolutionary constraint using 29 mammals Nature 478 476 482 10.1038/nature10530 21993624 PMC3207357 · DOI · Paper page
  41. Malone J Holloway E Adamusiak T Kapushesky M Zheng J Kolesnikov N Zhukova A Brazma A Parkinson H 2010 Modeling sample variables with an Experimental Factor Ontology Bioinformatics 26 1112 1118 10.1093/bioinformatics/btq099 20200009 PMC2853691 · DOI
  42. Marcos R Monteiro RA Rocha E 2006 Design-based stereological estimation of hepatocyte number, by combining the smooth optical fractionator and immunocytochemistry with anti-carcinoembryonic antigen polyclonal antibodies Liver International 26 116 124 10.1111/j.1478-3231.2005.01201.x 16420517 · DOI
  43. Marinov GK Kundaje A Park PJ Wold BJ 2014 Large-scale quality analysis of published ChIP-seq data G3 4 209 223 10.1534/g3.113.008680 24347632 PMC3931556 · DOI
  44. Markiewski MM Nilsson B Nilsson Ekdahl K Mollnes TE Lambris JD 2007 Complement and coagulation: strangers or partners in crime? Trends in Immunology 28 184 192 10.1016/j.it.2007.02.006 17336159 · DOI
  45. May D Blow MJ Kaplan T McCulley DJ Jensen BC Akiyama JA Holt A Plajzer-Frick I Shoukry M Wright C Afzal V Simpson PC Rubin EM Black BL Bristow J Pennacchio LA Visel A 2012 Large-scale discovery of enhancers from human heart tissue Nature Genetics 44 89 93 10.1038/ng.1006 22138689 PMC3246570 · DOI
  46. Medina-Rivera A Abreu-Goodger C Thomas-Chollier M Salgado H Collado-Vides J van Helden J 2011 Theoretical and empirical quality assessment of transcription factor-binding motifs Nucleic Acids Research 39 808 824 10.1093/nar/gkq710 20923783 PMC3035439 · DOI
  47. Mikkelsen TS Xu Z Zhang X Wang L Gimble JM Lander ES Rosen ED 2010 Comparative epigenomic analysis of murine and human adipogenesis Cell 143 156 169 10.1016/j.cell.2010.09.006 20887899 PMC2950833 · DOI
  48. Motallebipour M Ameur A Reddy Bysani MS Patra K Wallerman O Mangion J Barker MA McKernan KJ Komorowski J Wadelius C 2009 Differential binding and co-binding pattern of FOXA1 and FOXA3 and their relation to H3K4me3 in HepG2 cells revealed by ChIP-seq Genome Biology 10 R129 10.1186/gb-2009-10-11-r129 19919681 PMC3091322 · DOI
  49. Musunuru K Strong A Frank-Kamenetsky M Lee NE Ahfeldt T Sachs KV Li X Li H Kuperwasser N Ruda VM Pirruccello JP Muchmore B Prokunina-Olsson L Hall JL Schadt EE Morales CR Lund-Katz S Phillips MC Wong J Cantley W Racie T Ejebe KG Orho-Melander M Melander O Koteliansky V Fitzgerald K Krauss RM Cowan CA Kathiresan S Rader DJ 2010 From noncoding variant to phenotype via SORT1 at the 1p13 cholesterol locus Nature 466 714 719 10.1038/nature09266 20686566 PMC3062476 · DOI · Paper page
  50. Neph S Vierstra J Stergachis AB Reynolds AP Haugen E Vernot B Thurman RE John S Sandstrom R Johnson AK Maurano MT Humbert R Rynes E Wang H Vong S Lee K Bates D Diegel M Roach V Dunn D Neri J Schafer A Hansen RS Kutyavin T Giste E Weaver M Canfield T Sabo P Zhang M Balasundaram G Byron R MacCoss MJ Akey JM Bender MA Groudine M Kaul R Stamatoyannopoulos JA 2012 An expansive human regulatory lexicon encoded in transcription factor footprints Nature 489 83 90 10.1038/nature11212 22955618 PMC3736582 · DOI
  51. Newburger DE Bulyk ML 2009 UniPROBE: an online database of protein binding microarray data on protein-DNA interactions Nucleic Acids Research 37 D77 D82 10.1093/nar/gkn660 18842628 PMC2686578 · DOI
  52. Paris M Kaplan T Li XY Villalta JE Lott SE Eisen MB 2013 Gene expression in early Drosophila embryos is highly conserved despite extensive divergence of transcription factor binding arXiv preprint arXiv:13030216 PMC3772039 24068946
  53. Paten B Herrero J Beal K Fitzgerald S Birney E 2008 Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs Genome Research 18 1814 1828 10.1101/gr.076554.108 18849524 PMC2577869 · DOI
  54. Pennacchio LA Ahituv N Moses AM Prabhakar S Nobrega MA Shoukry M Minovitsky S Dubchak I Holt A Lewis KD Plajzer-Frick I Akiyama J De Val S Afzal V Black BL Couronne O Eisen MB Visel A Rubin EM 2006 In vivo enhancer analysis of human conserved non-coding sequences Nature 444 499 502 10.1038/nature05295 17086198 · DOI · Paper page
  55. Pique-Regi R Degner JF Pai AA Gaffney DJ Gilad Y Pritchard JK 2011 Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data Genome Research 21 447 455 10.1101/gr.112623.110 21106904 PMC3044858 · DOI · Paper page
  56. Plumb-Rudewiez N Clotman F Strick-Marchand H Pierreux CE Weiss MC Rousseau GG Lemaigre FP 2004 Transcription factor HNF-6/OC-1 inhibits the stimulation of the HNF-3alpha/Foxa1 gene by TGF-beta in mouse liver Hepatology 40 1266 1274 10.1002/hep.20459 15562441 · DOI
  57. Razick S Magklaras G Donaldson IM 2008 iRefIndex: a consolidated protein interaction database with provenance BMC Bioinformatics 9 405 10.1186/1471-2105-9-405 18823568 PMC2573892 · DOI
  58. Reddy TE Gertz J Pauli F Kucera KS Varley KE Newberry KM Marinov GK Mortazavi A Williams BA Song L Crawford GE Wold B Willard HF Myers RM 2012 Effects of sequence variation on differential allelic transcription factor occupancy and gene expression Genome Research 22 860 869 10.1101/gr.131201.111 22300769 PMC3337432 · DOI
  59. Reijnen MJ Peerlinck K Maasdam D Bertina RM Reitsma PH 1993 Hemophilia B Leyden: substitution of thymine for guanine at position -21 results in a disruption of a hepatocyte nuclear factor 4 binding site in the factor IX promoter Blood 82 151 158 8324220
  60. Rhee HS Pugh BF 2011 Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution Cell 147 1408 1419 10.1016/j.cell.2011.11.013 22153082 PMC3243364 · DOI
  61. Rios D McLaren WM Chen Y Birney E Stabenau A Flicek P Cunningham F 2010 A database and API for variation, dense genotyping and resequencing data BMC Bioinformatics 11 238 10.1186/1471-2105-11-238 20459810 PMC2882931 · DOI
  62. Sandelin A Alkema W Engstrom P Wasserman WW Lenhard B 2004 JASPAR: an open-access database for eukaryotic transcription factor binding profiles Nucleic Acids Research 32 D91 D94 10.1093/nar/gkh012 14681366 PMC308747 · DOI
  63. Schaub MA Boyle AP Kundaje A Batzoglou S Snyder M 2012 Linking disease associations with regulatory information in the human genome Genome Research 22 1748 1759 10.1101/gr.136127.111 22955986 PMC3431491 · DOI
  64. Schmidt D Schwalie PC Wilson MD Ballester B Goncalves A Kutter C Brown GD Marshall A Flicek P Odom DT 2012 Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages Cell 148 335 348 10.1016/j.cell.2011.11.058 22244452 PMC3368268 · DOI
  65. Schmidt D Wilson M Spyrou C Brown G Hadfield J Odom D 2009 ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions Methods 48 240 248 10.1016/j.ymeth.2009.03.001 19275939 PMC4052679 · DOI
  66. Schmidt D Wilson MD Ballester B Schwalie PC Brown GD Marshall A Kutter C Watt S Martinez-Jimenez CP Mackay S Talianidis I Flicek P Odom DT 2010 Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding Science 328 1036 1040 10.1126/science.1186176 20378774 PMC3008766 · DOI · Paper page
  67. Springer MS Murphy WJ Eizirik E O'Brien SJ 2003 Placental mammal diversification and the Cretaceous-Tertiary boundary Proceedings of the National Academy of Sciences of USA 100 1056 1061 10.1073/pnas.0334222100 PMC298725 12552136 · DOI
  68. Stefflova K Thybert D Wilson MD Streeter I Aleksic J Karagianni P Brazma A Adams DJ Talianidis I Marioni JC Flicek P Odom DT 2013 Cooperativity and rapid evolution of cobound transcription factors in closely related mammals Cell 154 530 540 10.1016/j.cell.2013.07.007 23911320 PMC3732390 · DOI
  69. Stenson PD Ball EV Mort M Phillips AD Shaw K Cooper DN 2012 The Human Gene Mutation Database (HGMD) and its exploitation in the fields of personalized genomics and molecular evolution Current Protocols in Bioinformatics Chapter 1: Unit1 13 10.1002/0471250953.bi0113s39 22948725 · DOI
  70. Sugawara H Iwata H Souri M Ichinose A 2007 Regulation of human protein Z gene expression by liver-enriched transcription factor HNF-4alpha and ubiquitous factor Sp1 Journal of Thrombosis and Haemostasis 5 2250 2258 10.1111/j.1538-7836.2007.02738.x 17958743 · DOI
  71. Tagle DA Koop BF Goodman M Slightom JL Hess DL Jones RT 1988 Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints Journal of Molecular Biology 203 439 455 10.1016/0022-2836(88)90011-3 3199442 · DOI
  72. Thomas-Chollier M Defrance M Medina-Rivera A Sand O Herrmann C Thieffry D van Helden J 2011 RSAT 2011: regulatory sequence analysis tools Nucleic Acids Research 39 W86 W91 10.1093/nar/gkr377 21715389 PMC3125777 · DOI
  73. Trapnell C Roberts A Goff L Pertea G Kim D Kelley DR Pimentel H Salzberg SL Rinn JL Pachter L 2012 Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks Nature Protocols 7 562 578 10.1038/nprot.2012.016 PMC3334321 22383036 · DOI
  74. Ward LD Kellis M 2012a HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants Nucleic Acids Research 40 D930 D934 10.1093/nar/gkr917 22064851 PMC3245002 · DOI · Paper page
  75. Ward LD Kellis M 2012b Interpreting noncoding genetic variation in complex traits and human disease Nature Biotechnology 30 1095 1106 10.1038/nbt.2422 PMC3703467 23138309 · DOI · Paper page
  76. Warde-Farley D Donaldson SL Comes O Zuberi K Badrawi R Chao P Franz M Grouios C Kazi F Lopes CT Maitland A Mostafavi S Montojo J Shao Q Wright G Bader GD Morris Q 2010 The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function Nucleic Acids Research 38 W214 W220 10.1093/nar/gkq537 20576703 PMC2896186 · DOI · Paper page
  77. Wilson MD Barbosa-Morais NL Schmidt D Conboy CM Vanes L Tybulewicz VL Fisher EM Tavare S Odom DT 2008 Species-specific transcription in mice carrying human chromosome 21 Science 322 434 438 10.1126/science.1160930 18787134 PMC3717767 · DOI
  78. Wu G Feng X Stein L 2010 A human functional protein interaction network and its application to cancer data analysis Genome Biology 11 R53 10.1186/gb-2010-11-5-r53 20482850 PMC2898064 · DOI · Paper page
  79. Xiao S Xie D Cao X Yu P Xing X Chen CC Musselman M Xie M West FD Lewin HA Wang T Zhong S 2012 Comparative epigenomic annotation of regulatory DNA Cell 149 1381 1392 10.1016/j.cell.2012.04.029 22682255 PMC3372872 · DOI
  80. Zanon A Rakovic A Blankenburg H Doncheva NT Schwienbacher C Serafin A Alexa A Weichenberger CX Albrecht M Klein C Hicks AA Pramstaller PP Domingues FS Pichler I 2013 Profiling of Parkin-binding partners using tandem affinity purification PLOS ONE 8 e78648 10.1371/journal.pone.0078648 24244333 PMC3823883 · DOI
  81. Zheng XW Kudaravalli R Russell TT DiMichele DM Gibb C Russell JE Margaritis P Pollak ES 2011 Mutation in the factor VII hepatocyte nuclear factor 4alpha-binding site contributes to factor VII deficiency Blood Coagulation & Fibrinolysis 22 624 627 10.1097/MBC.0b013e3283497699 21760481 · DOI
  82. Zinzen RP Girardot C Gagneur J Braun M Furlong EE 2009 Combinatorial binding predicts spatio-temporal cis-regulatory activity Nature 462 65 70 10.1038/nature08531 19890324 · DOI

Cited by

Sorted by citations

Authors
Ballester, B., Medina-Rivera, A., Schmidt, D., Gonzàlez-Porta, M., Carlucci, M., Chen, X., Chessman, K., Faure, A. J., Funnell, A. P., Goncalves, A., Kutter, C., Lukk, M., Menon, S., McLaren, W. M., Stefflova, K., Watt, S., Weirauch, M. T., Crossley, M., Marioni, J. C., Odom, D. T., Flicek, P., & Wilson, M. D.
Affiliations
  • European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Cambridge, United Kingdom
  • Sickkids Research Institute (CA)
  • University of Cambridge (GB)
  • European Bioinformatics Institute (GB)
  • University of Cincinnati (US)
  • UNSW Sydney (AU)
  • Cincinnati Children's Hospital Medical Center (US)
  • University of Toronto (CA)
Corresponding author
Wilson, Michael D
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2014-10-03
Volume
3
Pages
e02626-e02626
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.02626
PMC
PMC4359374
OpenAlex
W2160953907
Cited by
96
References
9
Citations by year
2026: 4 · 2025: 5 · 2024: 8 · 2023: 9 · 2022: 7 · 2021: 9 · 2020: 3 · 2019: 3 · 2018: 13 · 2017: 11 · 2016: 13 · 2015: 10 · 2014: 1
FWCI
4.78
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • European Research Council (202218)
  • EMBO (Young Investigator Award)
  • SickKids Foundation
  • Natural Sciences and Engineering Research Council of Canada (436194-2013)
  • Wellcome Trust (WT098051, WT095908)
  • INSERM
  • Canada Research Chairs
  • Marie Curie Reintegration Grant
  • Swiss National Science Foundation
  • Cancer Research UK
  • Consejo Nacional de Ciencia y Tecnología
  • European Molecular Biology Laboratory (EMBL)
  • European Molecular Biology Laboratory (International PhD Progam)
  • Heart and Stroke Foundation of Ontario (Bridge grant:7486)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
Keywords
cis-regulatory modules, transcription factor binding, liver gene regulation, tissue-specific gene regulation, disease loci, genome-wide association study, promoter mutations, lipid metabolism genes
MeSH terms
Animals, Blood Coagulation, Humans, Liver, Male, Mammals, Organ Specificity, Phylogeny, Protein Binding, Regulatory Sequences, Nucleic Acid, Species Specificity, Transcription Factors, Signal Transduction, Polymorphism, Single Nucleotide, Genomics, Chromatin Immunoprecipitation, Lipid Metabolism, Gene Regulatory Networks, Genome-Wide Association Study, Molecular Sequence Annotation

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 ›

Are you an author, or do you see a problem with this page? Request a review