Analysis of variation at transcription factor binding sites in Drosophila and humans

Genome Biology

Volumn 13, Issue 9, 2012, Pages

  Spivakov, Mikhail ^a,b   Akhtar, Junaid ^b   Kheradpour, Pouya ^c,d   Beal, Kathryn ^a   Girardot, Charles ^b   Koscielny, Gautier ^a   Herrero, Javier ^a   Kellis, Manolis ^c,d   Furlong, Eileen E M ^b   Birney, Ewan ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FUNCTIONAL GENOMICS; GENE FREQUENCY; GENE MUTATION; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; HUMAN VERSUS NONHUMAN DATA; NONHUMAN; PREDICTION; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SEQUENCE ANALYSIS; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL MODEL; DNA SEQUENCE; DROSOPHILA; GENETICS; GENOME; HUMAN GENOME; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE MOTIF; POSITION WEIGHT MATRIX; REGULATORY SEQUENCE;

ANALYSIS OF VARIANCE; ANIMALS; BINDING SITES; DROSOPHILA; GENETIC VARIATION; GENOME, HUMAN; GENOME, INSECT; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE ANNOTATION; MUTATION; NUCLEOTIDE MOTIFS; POSITION-SPECIFIC SCORING MATRICES; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 84865724466     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2012-13-9-r49     Document Type: Article

References (78)

1. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010, 38:D105-1010. 10.1093/nar/gkp950, 2808906, 19906716.
2. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EEM. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009, 462:65-70. 10.1038/nature08531, 19890324.
3. Junion G, Spivakov M, Girardot C, Braun M, Gustafson E, Birney E, Furlong E. A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell 2012, 148:473-486. 10.1016/j.cell.2012.01.030, 22304916.
4. Visel A, Blow M, Li Z, Zhang T, Akiyama J, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin E, Pennacchio LA. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858. 10.1038/nature07730, 2745234, 19212405.
5. Vavouri T, Elgar G. Prediction of cis-regulatory elements using binding site matrices-the successes, the failures and the reasons for both. Curr Opin Genet Dev 2005, 15:395-402. 10.1016/j.gde.2005.05.002, 15950456.
6. Lusk RW, Eisen MB. Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet 2010, 6:e1000829. 10.1371/journal.pgen.1000829, 2809757, 20107516.
7. Weirauch MT, Hughes TR. Conserved expression without conserved regulatory sequence: the more things change, the more they stay the same. Trends Genet 2010, 26:66-74. 10.1016/j.tig.2009.12.002, 20083321.
8. Hare EE, Peterson BK, Iyer VN, Meier R, Eisen MB. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet 2008, 4:e1000106. 10.1371/journal.pgen.1000106, 2430619, 18584029.
9. 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. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010, 328:1036-1040. 10.1126/science.1186176, 3008766, 20378774.
10. Crocker J, Tamori Y, Erives A. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 2008, 6:e263. 10.1371/journal.pbio.0060263, 2577699, 18986212.
11. Crocker J, Potter N, Erives A. Dynamic evolution of precise regulatory encodings creates the clustered site signature of enhancers. Nat Commun 2010, 1:99. 10.1038/ncomms1102, 2963808, 20981027.
12. He BZ, Holloway AK, Maerkl SJ, Kreitman M. Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules. PLoS Genet 2011, 7:e1002053. 10.1371/journal.pgen.1002053, 3084208, 21572512.
13. Garfield D, Haygood R, Nielsen W, Wray G. Population genetics of cis-regulatory sequences that operate during embryonic development in the sea urchin Strongylocentrotus purpuratus. Evol Dev 2012, 14:152-167.
14. Zheng W, Gianoulis TA, Karczewski KJ, Zhao H, Snyder M. Regulatory variation within and between species. Annu Rev Genomics Hum Genet 2010, 12:327-346.
15. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, Waszak SM, Habegger L, Rozowsky J, Shi M, Urban AE, Hong M-Y, Karczewski KJ, Huber W, Weissman SM, Gerstein MB, Korbel JO, Snyder M. Variation in transcription factor binding among humans. Science 2010, 328:232-235. 10.1126/science.1183621, 2938768, 20299548.
16. McDaniell R, Lee B-K, Song L, Liu Z, Boyle AP, Erdos MR, Scott LJ, Morken MA, Kucera KS, Battenhouse A, Keefe D, Collins FS, Willard HF, Lieb JD, Furey TS, Crawford GE, Iyer VR, Birney E. Heritable individual-specific and allele-specific chromatin signatures in humans. Science 2010, 328:235-239. 10.1126/science.1184655, 2929018, 20299549.
17. Zheng W, Zhao H, Mancera E, Steinmetz LM, Snyder M. Genetic analysis of variation in transcription factor binding in yeast. Nature 2010, 464:1187-1189. 10.1038/nature08934, 2941147, 20237471.
18. Chen K, van Nimwegen E, Rajewsky N, Siegal ML. Correlating gene expression variation with cis-regulatory polymorphism in Saccharomyces cerevisiae. Genome Biol Evol 2010, 2:697-707. 2953268, 20829281.
19. Majewski J, Pastinen T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet 2011, 27:72-79. 10.1016/j.tig.2010.10.006, 21122937.
20. Manolio T. Genomewide association studies and assessment of the risk of disease. N Engl J Med 2010, 363:166-176. 10.1056/NEJMra0905980, 20647212.
21. The 1000 genomes project consortium A map of human genome variation from population-scale sequencing. Nature 2010, 467:1061-1067. 10.1038/nature09534, 3042601, 20981092, The 1000 genomes project consortium.
22. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, Richardson MF, Anholt RRH, Barran M, Bess C, Blankenburg KP, Carbone MA, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan JC, Jhangiani SN, Jordan KW, Lara F, Lawrence F, Lee SL, Librado P, Linheiro RS, Lyman RF, et al. The Drosophila melanogaster Genetic Reference Panel. Nature 2012, 482:173-178. 10.1038/nature10811, 22318601.
23. The ENCODE Consortium An integrated Encyclopedia of DNA Elements in the human genome. Nature The ENCODE Consortium.
24. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, Lin MF, Washietl S, Arshinoff BI, Ay F, Meyer PE, Robine N, Washington NL, Di Stefano L, Berezikov E, Brown CD, Candeias R, Carlson JW, Carr A, Jungreis I, Marbach D, Sealfon R, Tolstorukov MY, Will S, Alekseyenko AA, Artieri C, Booth BW, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010, 330:1787-1797. 3192495, 21177974.
25. Nègre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, Li Z, Ishii H, Spokony RF, Chen J, Hwang L, Cheng C, Auburn RP, Davis MB, Domanus M, Shah PK, Morrison CA, Zieba J, Suchy S, Senderowicz L, Victorsen A, Bild NA, Grundstad AJ, Hanley D, MacAlpine DM, Mannervik M, et al. A cis-regulatory map of the Drosophila genome. Nature 2011, 471:527-531. 10.1038/nature09990, 3179250, 21430782.
26. Li X-Y, MacArthur S, Bourgon R, Nix D, Pollard DA, Iyer VN, Hechmer A, Simirenko L, Stapleton M, Hendriks CLL, 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, 6:24.
27. MacArthur S, Li X-Y, Li J, Brown JB, Chu HC, Zeng L, Grondona BP, Hechmer A, Simirenko L, Kernen SVE, 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, 2728534, 19627575.
28. Bushey AM, Ramos E, Corces VG. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev 2009, 23:1338-5010. 10.1101/gad.1798209, 2701583, 19443682.
29. Jakobsen JS, Braun M, Astorga J, Gustafson EH, Sandmann T, Karzynski M, Carlsson P, Furlong EEM. Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network. Genes Dev 2007, 21:2448-2460. 10.1101/gad.437607, 1993875, 17908931.
30. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, Furlong EEM. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev 2007, 21:436-449. 10.1101/gad.1509007, 1804332, 17322403.
31. Haldane JBS. The cost of natural selection. J Genet 1957, 55:511-524.
32. Muller HJ. Our load of mutations. Am J Hum Genet 1950, 2:111-176. 1716299, 14771033.
33. Stormo GD, Zhao Y. Determining the specificity of protein-DNA interactions. Nat Rev Genet 2010, 11:751-760.
34. Nuzhdin SV, Rychkova A, Hahn MW. The strength of transcription-factor binding modulates co-variation in transcriptional networks. Trends Genet 2010, 26:51-53. 10.1016/j.tig.2009.12.005, 2826431, 20080313.
35. Moses AM, Chiang DY, Kellis M, Lander ES, Eisen MB. Position specific variation in the rate of evolution in transcription factor binding sites. BMC Evol Biol 2003, 3:19. 10.1186/1471-2148-3-19, 212491, 12946282.
36. Kim J, He X, Sinha S. Evolution of regulatory sequences in 12 Drosophila species. PLoS Genet 2009, 5:e1000330. 10.1371/journal.pgen.1000330, 2607023, 19132088.
37. Huston M. Biological Diversity: The Coexistence of Species on Changing Landscapes 1994, Cambridge, UK: Cambridge University Press.
38. Kophengnavong T, Michnowicz JE, Blackwell TK. Establishment of distinct MyoD, E2A, and twist DNA binding specificities by different basic region-DNA conformations. Mol Cell Biol 2000, 20:261-272. 10.1128/MCB.20.1.261-272.2000, 85082, 10594029.
39. Charlesworth B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 2009, 10:195-205.
40. Kheradpour P, Stark A, Roy S, Kellis M. Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res 2007, 17:1919-1931. 10.1101/gr.7090407, 2099599, 17989251.
41. Godt D, Couderc JL, Cramton SE, Laski FA. Pattern formation in the limbs of Drosophila: bric à brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 1993, 119:799-812.
42. Ohlsson R, Bartkuhn M, Renkawitz R. CTCF shapes chromatin by multiple mechanisms: the impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 2010, 119:351-360. 10.1007/s00412-010-0262-0, 2910314, 20174815.
43. Fiston-Lavier A-S, Singh ND, Lipatov M, Petrov DA. Drosophila melanogaster recombination rate calculator. Gene 2010, 463:18-20. 10.1016/j.gene.2010.04.015, 20452408.
44. Maurano M, Wang H, Kutyavin T, Stamatoyannopoulos J. Widespread site-dependent buffering of human regulatory polymorphism. PLoS Genet 2012, 8:e1002599. 10.1371/journal.pgen.1002599, 3310774, 22457641.
45. Bradley RK, Li X-Y, 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, 2843597, 20351773.
46. Bulyk ML. Protein binding microarrays for the characterization of DNA-protein interactions. Adv Biochem Eng Biotechnol 2007, 104:65-85. 2727742, 17290819.
47. Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E, Taipale J. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 2006, 124:47-59. 10.1016/j.cell.2005.10.042, 16413481.
48. Gotea V, Visel A, Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res 2010, 20:565-577. 10.1101/gr.104471.109, 2860159, 20363979.
49. Halpern AL, Bruno WJ. Evolutionary distances for protein-coding sequences: modeling site-specific residue frequencies. Mol Biol Evol 1998, 15:910-917. 10.1093/oxfordjournals.molbev.a025995, 9656490.
50. Moses AM. Statistical tests for natural selection on regulatory regions based on the strength of transcription factor binding sites. BMC Evol Biol 2009, 9:286. 10.1186/1471-2148-9-286, 2800119, 19995462.
51. Meijsing SH, Pufall MA, So AY, Bates DL, Chen L, Yamamoto KR. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 2009, 324:407-410. 10.1126/science.1164265, 2777810, 19372434.
52. Swamy KBS, Cho C-Y, Chiang S, Tsai ZT-Y, Tsai H-K. Impact of DNA-binding position variants on yeast gene expression. Nucleic Acids Res 2009, 37:6991-7001. 10.1093/nar/gkp743, 2790881, 19767613.
53. Gibson G. Epistasis and pleiotropy as natural properties of transcriptional regulation. Theor Popul Biol 1996, 49:58-89. 10.1006/tpbi.1996.0003, 8813014.
54. 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, 170925, 12883007.
55. Barolo S. Shadow enhancers: Frequently asked questions about distributed cis-regulatory information and enhancer redundancy. BioEssays 2012, 34:135-141. 10.1002/bies.201100121, 22083793.
56. Hartman JL, Iv JLH, Hartwell L. Principles for the buffering of genetic variation. Science 2001, 291:1001-1004. 10.1126/science.291.5506.1001, 11232561.
57. Costanzo M, Baryshnikova A, Myers CL, Andrews B, Boone C. Charting the genetic interaction map of a cell. Curr Opin Biotechnol 2011, 22:66-74. 10.1016/j.copbio.2010.11.001, 21111604.
58. Ludwig MZ, Bergman C, Patel NH, Kreitman M. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 2000, 403:564-547. 10.1038/35000615, 10676967.
59. Sisodiya SM, Free SL, Williamson KA, Mitchell TN, Willis C, Stevens JM, Kendall BE, Shorvon SD, Hanson IM, Moore AT, Van Heyningen V. PAX6 haploinsufficiency causes cerebral malformation and olfactory dysfunction in humans. Nat Genet 2001, 28:214-216. 10.1038/90042, 11431688.
60. ENCODE Motif Browser. , http://www.broadinstitute.org/~pouyak/motif-disc/human
61. modENCODE Motif Browser. , http://www.broadinstitute.org/~pouyak/motif-disc/fly
62. Paten B, Herrero J, Fitzgerald S, Beal K, Flicek P, Holmes I, Birney E. Genome-wide nucleotide-level mammalian ancestor reconstruction. Genome Res 2008, 18:1829-1843. 10.1101/gr.076521.108, 2577868, 18849525.
63. Ensembl Genome Browser. , http://www.ensembl.org/index.html
64. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, Weinstock GM, Wilson RK, Gibbs RA, Kent WJ, Miller W, Haussler D. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15:1034-1050. 10.1101/gr.3715005, 1182216, 16024819.
65. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, Millburn G, Osumi-Sutherland D, Schroeder A, Seal R, Zhang H. FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 2009, 37:D555-559. 10.1093/nar/gkn788, 2686450, 18948289.
66. Flybase. , http://www.flybase.org
67. Hertz GZ, Stormo GD. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 1999, 15:563-577. 10.1093/bioinformatics/15.7.563, 10487864.
68. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842. 10.1093/bioinformatics/btq033, 2832824, 20110278.
69. Drosophila Population Genomics Project. , http://www.dpgp.org
70. Touzet H, Varré J-S. Efficient and accurate P-value computation for position weight matrices. Algorithms Mol Biol 2007, 2. 1510.1186/1748-7188-2-15.
71. Mahony S, Benos PV. STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 2007, 35:W253-W258. 10.1093/nar/gkm272, 1933206, 17478497.
72. STAMP: A Tool-kit for DNA Motif Comparison. , http://www.benoslab.pitt.edu/stamp
73. Stasinopoulos DM, Rigby RA. Generalised additive models for Location Scale and Shape (GAMLSS) in R. J Stat Software 2007, 23:1-46.
74. Cox D, Hinkley D. Theoretical Statistics 1974, 188. London: Chapman & Hall.
75. Dewey FE, Chen R, Cordero SP, Ormond KE, Caleshu C, Karczewski KJ, Whirl-Carrillo M, Wheeler MT, Dudley JT, Byrnes JK, Cornejo OE, Knowles JW, Woon M, Sangkuhl K, Gong L, Thorn CF, Hebert JM, Capriotti E, David SP, Pavlovic A, West A, Thakuria JV, Ball MP, Zaranek AW, Rehm HL, Church GM, West JS, Bustamante CD, Snyder M, Altman RB, et al. Phased whole-genome genetic risk in a family quartet using a major allele reference sequence. PLoS Genet 2011, 7. e100228010.1371.
76. Human Synthetic Major Allele Data from Dewey. , http://datadryad.org/handle/10255/dryad.34659
77. Fox J. Effect displays in R for generalised linear models. J Stat Software 2003, 8:1-27.
78. Nei M. Analysis of Gene Diversity in Subdivided Populations. Proc Natl Acad Sci USA 1973, 70:3321-3323. 10.1073/pnas.70.12.3321, 427228, 4519626.