Robust target gene discovery through transcriptome perturbations and genome-wide enhancer predictions in drosophila uncovers a regulatory basis for sensory specification

PLoS Biology

Volumn 8, Issue 7, 2010, Pages

  Aerts, Stein ^a,b   Quan, Xiao Jiang ^a,b   Claeys, Annelies ^a,b   Sanchez, Marina Naval ^b   Tate, Phillip ^a,b   Yan, Jiekun ^a,b   Hassan, Bassem A ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ATONAL PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ATO PROTEIN, DROSOPHILA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DL (DORSAL) PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN;

ACCURACY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS; ENHANCER REGION; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC REGULATION; IN VIVO STUDY; LARVAL DEVELOPMENT; MOLECULAR CLONING; MOLECULAR INTERACTION; NONHUMAN; PHOTORECEPTOR CELL; PLURIPOTENT STEM CELL; PREDICTION; PROTEIN MOTIF; RETINA DEVELOPMENT; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; ANIMAL; BINDING SITE; CYTOLOGY; DNA MICROARRAY; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; REPORTER GENE; REPRODUCIBILITY; RETINA; SENSATION;

DROSOPHILA ANANASSAE; DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENES, INSECT; GENES, REPORTER; GENOME; GREEN FLUORESCENT PROTEINS; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOPROTEINS; REPRODUCIBILITY OF RESULTS; RETINA; SENSATION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 77955015475     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000435.g001     Document Type: Article

References (72)

1. Hu Z, Killion PJ, Iyer VR (2007) Genetic reconstruction of a functional transcriptional regulatory network. Nat Genet 39: 683-687.
2. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
3. Imai K, Levine M, Satoh N, Satou Y (2006) Regulatory blueprint for a chordate embryo. Science 312: 1183-1187.
4. Davidson E, Rast J, Oliveri P, Ransick A, Calestani C, et al. (2002) A genomic regulatory network for development. Science 295: 1669-1678.
5. Stathopoulos A, Levine M (2005) Genomic regulatory networks and animal development. Dev Cell 9: 449-462.
6. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, et al. (2007) A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev 21: 436-449.
7. Zeitlinger J, Zinzen R, Stark A, Kellis M, Zhang H, et al. (2007) Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 21: 385-390.
8. Su YH, Li E, Geiss GK, Longabaugh WJ, Kramer A, et al. (2009) A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo. Dev Biol 329: 410-421.
9. Imai KS, Stolfi A, Levine M, Satou Y (2009) Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development 136: 285-293.
10. Georgescu C, Longabaugh WJ, Scripture-Adams DD, David-Fung ES, Yui MA, et al. (2008) A gene regulatory network armature for T lymphocyte specification. Proc Natl Acad Sci U S A 105: 20100-20105.
11. Zambelli F, Pesole G, Pavesi G (2009) Pscan: finding over-represented transcription factor binding site motifs in sequences from co-regulated or co expressed genes. Nucleic Acids Res 37: W247-252.
12. 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.
13. 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: W245-252.
14. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, et al. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32: 1372-1381.
15. Sinha S, Liang Y, Siggia E (2006) Stubb: a program for discovery and analysis of cis-regulatory modules. Nucleic Acids Res 34: W555-559.
16. Kim J, Cunningham R, James B, Wyder S, Gibson JD, et al. Functional characterization of transcription factor motifs using cross-species comparison across large evolutionary distances. PLoS Comput Biol 6: e1000652. doi:10.1371/journal.pcbi.1000652.
17. Frith CM, Li CM, Weng Z (2003) Cluster-Buster: finding dense clusters of motifs in DNA sequences. Nucleic Acids Res 31: 3666-3668.
18. Warner JB, Philippakis AA, Jaeger SA, He FS, Lin J, et al. (2008) Systematic identification of mammalian regulatory motifs' target genes and functions. Nat Methods 5: 347-353.
19. Gordan R, Hartemink AJ, Bulyk ML (2009) Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res 19: 2090-2100.
20. Van Loo P, Aerts S, Thienpont B, De Moor B, Moreau Y, et al. (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.
21. Morante J, Desplan C, Celik A (2007) Generating patterned arrays of photoreceptors. Curr Opin Genet Dev 17: 314-319.
22. Ferres-Marco D, Gutierrez-Garcia I, Vallejo DM, Bolivar J, Gutierrez-Avino FJ, et al. (2006) Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature 439: 430-436.
23. Bossuyt W, De Geest N, Aerts S, Leenaerts I, Marynen P, et al. (2009) The atonal proneural transcription factor links differentiation and tumor formation in Drosophila. PLoS Biol 7: e40. doi:10.1371/journal.pbio.1000040.
24. Zeitlinger J, Zinzen RP, Stark A, Kellis M, Zhang H, et al. (2007) Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 21: 385-390.
25. Stathopoulos A, Levine M (2005) Genomic regulatory networks and animal development. Dev Cell 9: 449-462.
26. Stathopoulos A, Van Drenth M, Erives A, Markstein M, Levine M (2002) Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. Cell 111: 687-701.
27. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, et al. The UCSC Genome Browser database: update 2010. Nucleic Acids Res 38: D613-619.
28. Aerts S, van Helden J, Sand O, Hassan BA (2007) Fine-tuning enhancer models to predict transcriptional targets across multiple genomes. PLoS ONE 2: e1115. doi:10.1371/journal.pone.0001115.
29. Aerts S, Lambrechts D, Maity S, Van Loo P, Coessens B, et al. (2006) Gene prioritization through genomic data fusion. Nat Biotechnol 24: 537-544.
30. Sukhanova MJ, Deb DK, Gordon GM, Matakatsu MT, Du W (2007) Proneural basic helix-loop-helix proteins and epidermal growth factor receptor signaling coordinately regulate cell type specification and cdk inhibitor expression during development. Mol Cell Biol 27: 2987-2996.
31. Powell LM, Zur Lage PI, Prentice DR, Senthinathan B, Jarman AP (2004) The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol Cell Biol 24: 9517-9526.
32. Pepple KL, Atkins M, Venken K, Wellnitz K, Harding M, et al. (2008) Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. Development 135: 4071-4079.
33. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW (2009) A microRNA imparts robustness against environmental fluctuation during development. Cell 137: 273-282.
34. Stark A, Lin M, Kheradpour P, Pedersen J, Parts L, et al. (2007) Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232.
35. Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN (1994) Atonal is the proneural gene for Drosophila photoreceptors. Nature 369: 398-400.
36. Reeves N, Posakony J (2005) Genetic programs activated by proneural proteins in the developing Drosophila PNS. Dev Cell 8: 413-425.
37. Nellesen DT, Lai EC, Posakony JW (1999) Discrete enhancer elements mediate selective responsiveness of enhancer of split complex genes to common transcriptional activators. Dev Biol 213: 33-53.
38. King DC, Taylor J, Elnitski L, Chiaromonte F, Miller W, et al. (2005) Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences. Genome Res 15: 1051-1060.
39. Bischof J, Maeda R, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific varphiC31 integrases. Proc Natl Acad Sci U S A 104: 3312-3317.
40. Groth AC, Fish M, Nusse R, Calos MP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775-1782.
41. Venken KJ, 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.
42. Zur Lage P, Powell L, Prentice D, McLaughlin P, Jarman A (2004) EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation. Dev Cell 7: 687-696.
43. Jarman AP, Sun Y, Jan LY, Jan YN (1995) Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121: 2019-2030.
44. Erwin DH, Davidson EH (2009) The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10: 141-148.
45. Ostrin JE, Li Y, Hoffman K, Liu J, Wang K, et al. (2006) Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Res 16: 466-476.
46. Newburger DE, Bulyk ML (2009) UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 37: D77-82.
47. Noyes MB, Meng X, Wakabayashi A, Sinha S, Brodsky MH, et al. (2008) A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system. Nucleic Acids Res 36: 2547-2560.
48. Workman C, Yin Y, Corcoran D, Ideker T, Stormo G, et al. (2005) enoLOGOS: a versatile web tool for energy normalized sequence logos. Nucleic Acids Res 33: W389-392.
49. Wasserman W, Sandelin A (2004) Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet 5: 276-287.
50. Stormo GD (2000) DNA binding sites: representation and discovery. Bioinformatics 16: 16-23.
51. Mao Y, Freeman M (2009) Fasciclin 2, the Drosophila orthologue of neural cell adhesion molecule, inhibits EGF receptor signalling. Development 136: 473-481.
52. Flora A, Klisch TJ, Schuster G, Zoghbi HY (2009) Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. Science 326: 1424-1427.
53. Bossuyt W, Kazanjian A, De Geest N, Van Kelst S, De Hertogh G, et al. (2009) Atonal homolog 1 is a tumor suppressor gene. PLoS Biol 7: e39. doi:10.1371/ journal.pbio.1000039.
54. Philippakis A, Busser B, Gisselbrecht S, He F, Estrada B, et al. (2006) Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput Biol 2: e53. doi:10.1371/ journal.pcbi.0020053.
55. Sandmann T, Jensen L, Jakobsen J, Karzynski M, Eichenlaub M, et al. (2006) A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev Cell 10: 797-807.
56. Wang VY, Hassan BA, Bellen HJ, Zoghbi HY (2002) Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts. Curr Biol 12: 1611-1616.
57. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
58. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
59. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
60. Aerts S, Thijs G, Coessens B, Staes M, Moreau Y, et al. (2003) Toucan: deciphering the cis-regulatory logic of coregulated genes. Nucleic Acids Res 31: 1753-1764.
61. Halfon MS, Gallo SM, Bergman CM (2008) REDfly 2.0: an integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila. Nucleic Acids Res 36: D594-D598.
62. Griffith O, Montgomery S, Bernier B, Chu B, Kasaian K, et al. (2007) ORegAnno: an open-access community-driven resource for regulatory annotation. Nucleic Acids Res.
63. Bergman MC, Carlson WJ, Celniker ES (2005) Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila. Bioinformatics 21: 1747-1749.
64. Barolo S, Carver LA, Posakony JW (2000) GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29: 726728730732.
65. Jafar-Nejad H, Acar M, Nolo R, Lacin H, Pan H, et al. (2003) Senseless acts as a binary switch during sensory organ precursor selection. Genes Dev 17: 2966-2978.
66. Rosay P, Colas JF, Maroteaux L (1995) Dual organisation of the Drosophila neuropeptide receptor NKD gene promoter. Mech Dev 51: 329-339.
67. Helms AW, Abney AL, Ben-Arie N, Zoghbi HY, Johnson JE (2000) Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127: 1185-1196.
68. Skowronska-Krawczyk D, Ballivet M, Dynlacht BD, Matter JM (2004) Highly specific interactions between bHLH transcription factors and chromatin during retina development. Development 131: 4447-4454.
69. Stramer B, Winfield M, Shaw T, Millard TH, Woolner S, et al. (2008) Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. EMBO Rep 9: 465-471.
70. Jakobsen JS, Braun M, Astorga J, Gustafson EH, Sandmann T, et al. (2007) Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network. Genes Dev 21: 2448-2460.
71. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA, et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6: e27. doi:10.1371/journal.pbio.0060027.
72. Nolo R, Abbott LA, Bellen HJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102: 349-362.