Comparative motif discovery combined with comparative transcriptomics yields accurate targetome and enhancer predictions

Genome Research

Volumn 23, Issue 1, 2013, Pages 74-88

  Naval Sańchez, Marina ^a   Potier, Delphine ^a   Haagen, Lotte ^a   Sánchez, Máximo ^b   Munck, Sebastian ^c   Van De Sande, Bram ^a   Casares, Fernando ^b   Christiaens, Valerie ^a   Aerts, Stein ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Universidad Pablo de Olavide   (Spain)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EYE PROTEIN; PROTEIN CG6329; PROTEIN CHP; PROTEIN DMRT99B; PROTEIN DPR10; PROTEIN LIM3; PROTEIN RETN; PROTEIN SCRT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER GLASS;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS; DROSOPHILA YAKUBA; EYE DEVELOPMENT; EYE DISCHARGE; GENE EXPRESSION; GENE LOCATION; GENE TARGETING; GENOME; IMMUNOHISTOCHEMISTRY; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN MOTIF; RNA SEQUENCE; TARGETOME; TRANSCRIPTOMICS; VALIDATION STUDY;

ANIMALS; BINDING SITES; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENOMICS; NUCLEOTIDE MOTIFS; ORGAN SPECIFICITY; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS; DROSOPHILA YAKUBA;

EID: 84871991022     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.140426.112     Document Type: Article

References (70)

1. Adli M, Bernstein BE. 2011. Whole-genome chromatin profiling from limited numbers of cells using nano-ChIP-seq. Nat Protoc 6: 1656-1668.
2. Aerts S. 2012. Computational strategies for the genome-wide identification of cis-regulatory elements and transcriptional targets. Curr Top Dev Biol 98: 121-145.
3. Aerts S, Thijs G, Coessens B, Staes M, Moreau Y, De Moor B. 2003. Toucan: Deciphering the cis -regulatory logic of coregulated genes. Nucleic Acids Res 31: 1753-1764. (Pubitemid 36336577)
4. Aerts S, Lambrechts D, Maity S, Van Loo P, Coessens B, De Smet F, Tranchevent L-C, De Moor B, Marynen P, Hassan B, et al. 2006. Gene prioritization through genomic data fusion. Nat Biotechnol 24: 537-544.
5. Aerts S, Quan X-J, Claeys A, Naval Sanchez M, Tate P, Yan J, Hassan BA. 2010. Robust target gene discovery through transcriptome perturbations and genome-wide enhancer predictions in Drosophila uncovers a regulatory basis for sensory specification. PLoS Biol 8: e1000435. doi: 10.1371/journal.pbio.1000435.
6. Amore G, Casares F. 2010. Size matters: The contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network. Dev Biol 344: 569-577.
7. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106. doi: 10.1186/gb-2010-11-10-r106.
8. Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF, Magwire MM, Rollmann SM, Duncan LH, Lawrence F, Anholt RRH, et al. 2009. Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41: 299-307.
9. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, et al. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
10. Bui QT, Zimmerman JE, Liu H, Gray-Board GL, Bonini NM. 2000. Functional analysis of an eye enhancer of the Drosophila eyes absent gene: Differential regulation by eye specification genes. Dev Biol 221: 355-364. (Pubitemid 30322516)
11. Bullard JH, Purdom E, Hansen KD, Dudoit S. 2010. Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11: 94. doi: 10.1186/1471-2105-11-94.
12. Carroll SB, Grenier J, Weatherbee S. 2009. From DNA to diversity: Molecular genetics and the evolution of animal design, 2nd ed. Wiley, New York. http://books.google.be/books?id=tayrCszYKdkC.
13. Curtiss J, Heilig JS. 1997. Arrowhead encodes a LIM homeodomain protein that distinguishes subsets of Drosophila imaginal cells. Dev Biol 190: 129-141. (Pubitemid 27444742)
14. Davidson EH. 2001. Genomic regulatory systems. Academic Press, San Diego.
15. Diederich RJ, Pattatucci AM, Kaufman TC. 1991. Developmental and evolutionary implications of labial, deformed and engrailed expression in the Drosophila head. Development 113: 273-281.
16. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48. doi: 10.1186/1471-2105-10-48.
17. Ellis MC, O'Neill EM, Rubin GM. 1993. Expression of Drosophila glass protein and evidence for negative regulation of its activity in nonneuronal cells by another DNA-binding protein. Development 119: 855-865. (Pubitemid 23337426)
18. Firth LC, Baker NE. 2007. Spitz from the retina regulates genes transcribed in the second mitotic wave, peripodial epithelium, glia and plasmatocytes of the Drosophila eye imaginal disc. Dev Biol 307: 521-538. (Pubitemid 47001355)
19. Frith MC, Fu Y, Yu L, Chen J-F, Hansen U, Weng Z. 2004. Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32: 1372-1381. (Pubitemid 38854738)
20. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, ClineMS, Goldman M, Barber GP, Clawson H, Coelho A, et al. 2010. The UCSC Genome Browser database: Update 2011. Nucleic Acids Res 39: D876-D882.
21. Gordân R, Hartemink AJ, Bulyk ML. 2009. Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res 19: 2090-2100.
22. Herrmann C, Van de Sande B, Potier D, Aerts S. 2012. i-cisTarget: An integrative genomics method for the prediction of regulatory features and cis-regulatory modules. Nucleic Acids Res 40: e114. doi: 10.1093/nar/gks543.
23. Hong LZ, Li J, Schmidt-Kuntzel A,Warren WC, Barsh GS. 2011. Digital gene expression for non-model organisms. Genome Res 21: 1905-1915.
24. Ho Sui SJ, Fulton DL, Arenillas DJ, Kwon AT, Wasserman WW. 2007. oPOSSUM: Integrated tools for analysis of regulatory motif over-representation. Nucleic Acids Res 35: W245-W252.
25. Jaeger J, Surkova S, Blagov M, Janssens H, Kosman D, Kozlov KN, Manu, Myasnikova E, Vanario-Alonso CE, Samsonova M, et al. 2004. Dynamic control of positional information in the early Drosophila embryo. Nature 430: 368-371. (Pubitemid 38937746)
26. Jemc J, Rebay I. 2007. Identification of transcriptional targets of the dual function transcription factor/phosphatase eyes absent. Dev Biol 310: 416-429. (Pubitemid 47483675)
27. Jordan KW, Carbone MA, Yamamoto A, Morgan TJ, Mackay TFC. 2007. Quantitative genomics of locomotor behavior in Drosophila melanogaster. Genome Biol 8: R172. doi: 10.1186/gb-2007-8-8-r172.
28. Kumar JP. 2010. Retinal determination: The beginning of eye development. Curr Top Dev Biol 93: 1-28.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25.
30. Mahony S, Benos PV. 2007. STAMP: A web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 35: W253-W258.
31. McLeay RC, Bailey TL. 2010. Motif Enrichment Analysis: A unified framework and an evaluation on ChIP data. BMC Bioinformatics 11: 165. doi: 10.1186/1471-2105-11-165.
32. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. 2010. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20: 816-825.
33. Mishra M, Oke A, Lebel C, McDonald EC, Plummer Z, Cook TA, Zelhof AC. 2010. Pph13 and orthodenticle define a dual regulatory pathway for photoreceptor cell morphogenesis and function. Development 137: 2895-2904.
34. Morgan M, Anders S, Lawrence M, Aboyoun P, Pagès H, Gentleman R. 2009. ShortRead: A bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25: 2607-2608.
35. Moses K, Rubin GM. 1991. Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5: 583-593. (Pubitemid 21905979)
36. Moses K, Ellis MC, Rubin GM. 1989. The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340: 531-536. (Pubitemid 19201693)
37. Ostrin EJ, Li Y, Hoffman K, Liu J,Wang K, Zhang L, Mardon G, Chen R. 2006. Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Res 16: 466-476.
38. Pauli T, Seimiya M, Blanco J, GehringWJ. 2005. Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog. Development 132: 2771-2782. (Pubitemid 40932867)
39. Pfeiffer BD, Jenett A, Hammonds AS, Ngo T-TB, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila . Proc Natl Acad Sci 105: 9715-9720. (Pubitemid 352031366)
40. Pfreundt U, James DP, Tweedie S,Wilson D, Teichmann SA, Adryan B. 2010. FlyTF: Improved annotation and enhanced functionality of the Drosophila transcription factor database. Nucleic Acids Res 38: D443-D447.
41. 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 Res 21: 447-455.
42. Potier D, Atak ZK, Sanchez MN, Herrmann C, Aerts S. 2012. Using cisTargetX to predict transcriptional targets and networks in Drosophila. Methods Mol Biol 786: 291-314.
43. Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25. doi: 10.1186/gb-2010-11-3-r25.
44. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
45. Rogers EM, Brennan CA, Mortimer NT, Cook S, Morris AR, Moses K. 2005. Pointed regulates an eye-specific transcriptional enhancer in the Drosophila hedgehog gene, which is required for the movement of the morphogenetic furrow. Development 132: 4833-4843. (Pubitemid 41685292)
46. Roider HG, Manke T, O'Keeffe S, Vingron M, Haas SA. 2009. PASTAA: Identifying transcription factors associated with sets of co-regulated genes. Bioinformatics 25: 435-442.
47. Roignant J-Y, Legent K, Janody F, TreismanJessica E. 2010. The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila. Development 137: 273-281.
48. Sabo PJ, Kuehn MS, Thurman R, Johnson BE, Johnson EM, Cao H, Yu M, Rosenzweig E, Goldy J, Haydock A, et al. 2006. Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 3: 511-518. (Pubitemid 43941768)
49. Saha S, Sparks AB, Rago C, Akmaev V, Wang CJ, Vogelstein B, Kinzler KW, Velculescu VE. 2002. Using the transcriptome to annotate the genome. Nat Biotechnol 20: 508-512. (Pubitemid 34495940)
50. Silver SJ, Rebay I. 2005. Signaling circuitries in development: Insights from the retinal determination gene network. Development 132: 3-13. (Pubitemid 40207962)
51. Small S, Arnosti DN, Levine M. 1993. Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 119: 767-772. (Pubitemid 23337418)
52. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. 2011. Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27: 431-432.
53. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Gräf S, HussM, Keefe D, et al. 2011. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 21: 1757-1767.
54. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. 2011. Differential expression in RNA-seq: A matter of depth. Genome Res 21: 2213-2223.
55. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
56. Treisman JE, Rubin GM. 1996. Targets of glass regulation in the Drosophila eye disc. Mech Dev 56: 17-24. (Pubitemid 26182617)
57. Van Loo P, Aerts S, Thienpont B, De Moor B, Moreau Y, Marynen P. 2008. ModuleMiner-improved computational detection of cis-regulatory modules: Are there different modes of gene regulation in embryonic development and adult tissues? Genome Biol 9: R66. doi: 10.1186/gb-2008-9-4-r66.
58. Venken KJT, He Y, Hoskins RA, Bellen HJ. 2006. P[acman]: A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314: 1747-1751. (Pubitemid 44969080)
59. Venken KJT, Kasprowicz J, Kuenen S, Yan J, Hassan BA, Verstreken P. 2008. Recombineering-mediated tagging of Drosophila genomic constructs for in vivo localization and acute protein inactivation. Nucleic Acids Res 36: e114. doi: 10.1093/nar/gkn486.
60. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
61. Wang VY, Hassan BA, Bellen HJ, Zoghbi HY. 2002. Drosophila atonal fully rescues the phenotype ofMath1 nullmice: New functions evolve in new cellular contexts. Curr Biol 12: 1611-1616.
62. Warner JB, Philippakis AA, Jaeger SA, He FS, Lin J, Bulyk ML. 2008. Systematic identification of mammalian regulatory motifs' target genes and functions. Nat Methods 5: 347-353. (Pubitemid 351459368)
63. Warsow G, Greber B, Falk SSI, Harder C, Siatkowski M, Schordan S, Som A, Endlich N, Schöler H, RepsilberD, et al. 2010. ExprEssence - revealing the essence of differential experimental data in the context of an interaction/regulation net-work. BMC Syst Biol 4: 164. doi: 10.1186/1752-0509-4- 164.
64. Wittkopp PJ, Kalay G. 2012. Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13: 59-69.
65. Won K-J, Ren B, Wang W. 2010. Genome-wide prediction of transcription factor binding sites using an integrated model. Genome Biol 11: R7. doi: 10.1186/gb-2010-11-1-r7.
66. Worsley-Hunt R, Bernard V, Wasserman WW. 2011. Identification of cisregulatory sequence variations in individual genome sequences. Genome Med 3: 65. doi: 10.1186/gm281.
67. Wray GA. 2007. The evolutionary significance of cis -regulatory mutations. Nat Rev Genet 8: 206-216.
68. Yan H, Canon J, Banerjee U. 2003. A transcriptional chain linking eye specification to terminal determination of cone cells in the Drosophila eye. Dev Biol 263: 323-329. (Pubitemid 37338613)
69. Zelhof AC, Koundakjian E, Scully AL, Hardy RW, Pounds L. 2003. Mutation of the photoreceptor specific homeodomain gene Pph13 results in defects in phototransduction and rhabdomere morphogenesis. Development 130: 4383-4392. (Pubitemid 37185326)
70. Zhu LJ, Christensen RG, Kazemian M, Hull CJ, Enuameh MS, Basciotta MD, Brasefield JA, Zhu C, Asriyan Y, Lapointe DS, et al. 2011. FlyFactorSurvey: A database of Drosophila transcription factor binding specificities determined using the bacterial one-hybrid system. Nucleic Acids Res 39: D111-D117.