Interpreting the regulatory genome: The genomics of transcription factor function in Drosophila melanogaster

Briefings in Functional Genomics

Volumn 11, Issue 5, 2012, Pages 336-346

  Slattery, Matthew ^a   Nègre, Nicolas ^a   White, Kevin P ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Drosophila; Enhancer; Genomics; Transcription factor; Zelda

Indexed keywords

DNA BINDING PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR;

ARTICLE; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC CONSERVATION; GENOME; GENOMICS; HIGH THROUGHPUT SEQUENCING; HUMAN; NONHUMAN; PHYLOGENY; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; GENOME, INSECT; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER;

EID: 84867120185     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els034     Document Type: Article

References (100)

1. Adams MD, Celniker SE, Holt RA, et al. The genome sequence of Drosophila melanogaster. Science 2000;287: 2185-95.
2. Clark AG, Eisen MB, Smith DR, et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007; 450:203-18.
3. Mann RS, Morata G. The developmental and molecular biology of genes that subdivide the body of Drosophila. Annu Rev CellDev Biol 2000;16:243-71.
4. Jamrich M, Haars R, Wulf E, et al. Correlation of RNA polymerase B and transcriptional activity in the chromosomes of Drosophila melanogaster. Chromosoma 1977;64:319-26.
5. Lis JT, Mason P, Peng J, et al. P-TEFb kinase recruitment and function at heat shock loci. Genes Dev 2000;14: 792-803.
6. Ritossa FM. Experimental activation of specific loci in polytene chromosomes of Drosophila. Exp Cell Res 1964;35: 601-7.
7. Thummel CS. Ecdysone-regulated puff genes 2000. Insect BiochemMol Biol 2002;32:113-20.
8. Evans NC, Swanson CI, Barolo S. Sparkling insights into enhancer structure, function, and evolution. CurrTop Dev Biol 2012;98:97-120.
9. Driever W, Nusslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 1989;337:138-43.
10. Stanojevic D, Small S, Levine M. Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 1991;254:1385-7.
11. Swanson CI, Evans NC, Barolo S. Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. DevCell 2010;18:359-70.
12. Dunipace L, Ozdemir A, Stathopoulos A. Complex interactions between cis-regulatory modules in native conformation are critical for Drosophila snail expression. Development 2011;138:4075-84.
13. Arnosti DN, Kulkarni MM. Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards? J Cell Biochem 2005;94:890-8.
14. Kulkarni MM, Arnosti DN. Information display by transcriptional enhancers. Development 2003;130:6569-75.
15. Juven-Gershon T, Kadonaga JT. Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol 2010;339:225-9.
16. Papai G, Weil PA, Schultz P. New insights into the function of transcription factor TFIID from recent structural studies. Curr Opin GenetDev 2011;21:219-24.
17. Deng W, Roberts SG. TFIIB and the regulation of transcription by RNA polymerase II. Chromosoma 2007;116:417-29.
18. Arbeitman MN, Furlong EE, Imam F, et al. Gene expression during the life cycle of Drosophila melanogaster. Science 2002;297:2270-5.
19. Reinke V, White KP. Developmental genomic approaches in model organisms. Annu Rev GenomicsHum Genet 2002;3: 153-78.
20. White KP, Rifkin SA, Hurban P, et al. Microarray analysis of Drosophila development during metamorphosis. Science 1999;286:2179-84.
21. Li TR, White KP. Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell 2003;5:59-72.
22. Klebes A, Biehs B, Cifuentes F, et al. Expression profiling of Drosophila imaginal discs. Genome Biol 2002;3: RESEARCH0038.
23. Butler MJ, Jacobsen TL, Cain DM, et al. Discovery of genes with highly restricted expression patterns in the Drosophila wing disc using DNA oligonucleotide microarrays. Development 2003;130:659-70.
24. Baig J, Chanut F, Kornberg TB, et al. The chromatinremodeling protein Osa interacts with CyclinE in Drosophila eye imaginal discs. Genetics 2010;184:731-44.
25. Furlong EE, Andersen EC, Null B, et al. Patterns of gene expression during Drosophila mesoderm development. Science 2001;293:1629-33.
26. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978;276:565-70.
27. Hersh BM, Nelson CE, Stoll SJ, et al. The UBX-regulated network in the haltere imaginal disc of D. melanogaster. Dev Biol 2007;302:717-27.
28. Mohit P, Makhijani K, Madhavi MB, et al. Modulation of AP and DV signaling pathways by the homeotic gene Ultrabithorax during haltere development in Drosophila. Dev Biol 2006;291:356-67.
29. Pavlopoulos A, Akam M. Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis. Proc Natl Acad Sci USA 2011;108: 2855-60.
30. Crickmore MA, Mann RS. Hox control of organ size by regulation of morphogen production and mobility. Science 2006;313:63-8.
31. Crickmore MA, Mann RS. Hox control of morphogen mobility and organ development through regulation of glypican expression. Development 2007;134:327-34.
32. Quiring R, Walldorf U, Kloter U, et al. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 1994;265:785-9.
33. Michaut L, Flister S, Neeb M, et al. Analysis of the eye developmental pathway in Drosophila using DNA microarrays. Proc Natl Acad Sci USA 2003;100:4024-9.
34. Ostrin EJ, Li Y, Hoffman K, et al. Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Res 2006;16:466-76.
35. Jemc J, Rebay I. Targeting Drosophila eye development. Genome Biol 2006;7:226.
36. Aerts S, Van Helden J, Sand O, et al. Fine-tuning enhancer models to predict transcriptional targets across multiple genomes. PLoS One 2007;2:e1115.
37. Aerts S, Quan XJ, Claeys A, et al. Robust target gene discovery through transcriptome perturbations and genomewide enhancer predictions in Drosophila uncovers a regulatory basis for sensory specification. PLoS Biol 2010;8: e1000435.
38. Slattery MG, Heideman W. Coordinated regulation of growth genes in Saccharomyces cerevisiae. Cell Cycle 2007;6:1210-9.
39. Gasch AP, Spellman PT, Kao CM, et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000;11:4241-57.
40. Kim TH, Ren B. Genome-wide analysis of protein-DNA interactions. Annu Rev Genomics Hum Genet 2006;7: 81-102.
41. Iyer VR, Horak CE, Scafe CS, et al. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 2001;409:533-8.
42. Ren B, Robert F, Wyrick JJ, et al. Genome-wide location and function of DNA binding proteins. Science 2000;290: 2306-9.
43. Johnson DS, Mortazavi A, Myers RM, et al. Genome-wide mapping of in vivo protein-DNA interactions. Science 2007; 316:1497-502.
44. Southall TD, Brand AH. Chromatin profiling in model organisms. Brief Funct Genomic Proteomic 2007;6:133-40.
45. van Steensel B, Henikoff S. Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat Biotechnol 2000;18:424-8.
46. Greil F, Moorman C, Van Steensel B. Dam ID. mapping of in vivo protein-genome interactions using tethered DNA adenine methyltransferase. Methods Enzymol 2006; 410:342-59.
47. Xiao R, Roman-Sanchez R, Moore DD. Dam IP. a novel method to identify DNA binding sites in vivo. Nucl Recept Signal 2010;8:e003.
48. Luo SD, Shi GW, Baker BS. Direct targets of the D. melanogaster DSXF protein and the evolution of sexual development. Development 2011;138:2761-71.
49. Zeitlinger J, Stark A, Kellis M, et al. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 2007;39:1512-6.
50. Weake VM, Workman JL. Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 2010;11: 426-37.
51. Rougvie AE, Lis JT. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 1988;54:795-804.
52. O'Brien T, Lis JT. RNA polymerase II pauses at the 5' end of the transcriptionally induced Drosophila hsp70 gene. Mol Cell Biol 1991;11:5285-90.
53. Rasmussen EB, Lis JT. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad SciUSA 1993;90:7923-7.
54. Lis J. Promoter-associated pausing in promoter architecture and postinitiation transcriptional regulation. ColdSpringHarb Symp Quant Biol 1998;63:347-56.
55. Ohler U, Liao GC, Niemann H, et al. Computational analysis of core promoters in the Drosophila genome. Genome Biol 2002;3:RESEARCH0087.
56. Rach EA, Yuan HY, Majoros WH, et al. Motif composition, conservation and condition-specificity of single and alternative transcription start sites in the Drosophila genome. Genome Biol 2009;10:R73.
57. Hendrix DA, Hong JW, Zeitlinger J, et al. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. ProcNatl Acad SciUSA 2008;105:7762-7.
58. Lee C, Li X, Hechmer A, et al. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol Cell Biol 2008;28:3290-300.
59. Ohler U, Wassarman DA. Promoting developmental transcription. Development 2010;137:15-26.
60. Li J, Gilmour DS. Promoter proximal pausing and the control of gene expression. Curr Opin Genet Dev 2011;21: 231-5.
61. Zeitlinger J, Stark A. Developmental gene regulation in the era of genomics. Dev Biol 2010;339:230-9.
62. MacArthur S, Li XY, Li J, et al. 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.
63. Li XY, MacArthur S, Bourgon R, et al. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 2008;6:e27.
64. Roy S, Ernst J, Kharchenko PV, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010;330:1787-97.
65. Negre N, Brown CD, Ma L, et al. A cis-regulatory map of the Drosophila genome. Nature 2011;471:527-31.
66. Farnham PJ. Insights from genomic profiling of transcription factors. Nat Rev Genet 2009;10:605-16.
67. MacQuarrie KL, Fong AP, Morse RH, et al. Genome-wide transcription factor binding: beyond direct target regulation. TrendsGenet 2011;27:141-8.
68. Orian A, Van Steensel B, Delrow J, et al. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. GenesDev 2003;17:1101-14.
69. Moorman C, Sun LV, Wang J, et al. Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci USA 2006;103:12027-32.
70. Kvon EZ, Stampfel G, Yanez-Cuna JO, et al. HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature. GenesDev 2012;26:908-13.
71. Wunderlich Z, Mirny LA. Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 2009;25:434-40.
72. Edelman LB, Fraser P. Transcription factories: genetic programming in three dimensions. Curr Opin Genet Dev 2012; 22:110-4.
73. Bantignies F, Roure V, Comet I, et al. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 2011;144:214-26.
74. Satija R, Bradley RK. The TAG team motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo. Genome Res 2012;22:656-65.
75. Tsukiyama T, Becker PB, Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 1994;367: 525-32.
76. Tsukiyama T, Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 1995; 83:1011-20.
77. Adkins NL, Hagerman TA, Georgel P. GAGA protein: a multi-faceted transcription factor. BiochemCell Biol 2006;84: 559-67.
78. ten Bosch JR, Benavides JA, Cline TW. The TAGteam DNA motif controls the timing of Drosophila preblastoderm transcription. Development 2006;133:1967-77.
79. De Renzis S, Elemento O, Tavazoie S, et al. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 2007;5:e117.
80. Satija R, Bradley RK. The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo. Genome Res 2012;22:656-65.
81. Nien CY, Liang HL, Butcher S, et al. Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLoS Genet 2011;7:e1002339.
82. Harrison MM, Li XY, Kaplan T, et al. Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet 2011;7:e1002266.
83. Ciglar L, Furlong EE. Conservation and divergence in developmental networks: a view from Drosophila myogenesis. Curr Opin Cell Biol 2009;21:754-60.
84. Zinzen RP, Girardot C, Gagneur J, et al. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009;462:65-70.
85. Junion G, Spivakov M, Girardot C, et al. A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell 2012;148:473-86.
86. He Q, Bardet AF, Patton B, et al. High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species. Nat Genet 2011;43: 414-20.
87. Hong JW, Hendrix DA, Levine MS. Shadow enhancers as a source of evolutionary novelty. Science 2008;321:1314.
88. Barolo S. Shadow enhancers: frequently asked questions about distributed cis-regulatory information and enhancer redundancy. Bioessays 2012;34:135-41.
89. Allada R, Emery P, Takahashi JS, et al. Stopping time: the genetics of fly and mouse circadian clocks. Annu Rev Neurosci 2001;24:1091-119.
90. Menet JS, Abruzzi KC, Desrochers J, et al. Dynamic PER repression mechanisms in the Drosophila circadian clock: from on-DNA to off-DNA. GenesDev 2010;24:358-67.
91. Abruzzi KC, Rodriguez J, Menet JS, et al. Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression. Genes Dev 2011;25: 2374-86.
92. Choo SW, White R, Russell S. Genome-wide analysis of the binding of the Hox protein Ultrabithorax and the Hox cofactor Homothorax in Drosophila. PLoS One 2011;6: e14778.
93. Slattery M, Ma L, Negre N, et al. Genome-wide tissuespecific occupancy of the Hox protein Ultrabithorax and Hox cofactor Homothorax in Drosophila. PLoS One 2011;6:e14686.
94. Agrawal P, Habib F, Yelagandula R, et al. Genome-level identification of targets of Hox protein Ultrabithorax in Drosophila: novel mechanisms for target selection. Sci Rep 2011;1:205.
95. Choo SW, Russell S. Genomic approaches to understanding Hox gene function. Adv Genet 2011;76:55-91.
96. Hueber SD, Bezdan D, Henz SR, et al. Comparative analysis of Hox downstream genes in Drosophila. Development 2007;134:381-92.
97. Slattery M, Riley T, Liu P, et al. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 2011;147:1270-82.
98. Siggers T, Duyzend MH, Reddy J, et al. Non-DNAbinding cofactors enhance DNA-binding specificity of a transcriptional regulatory complex. Mol Syst Biol 2011;7: 555.
99. Carlson CD, Warren CL, Hauschild KE, et al. Specificity landscapes of DNA binding molecules elucidate biological function. Proc Natl Acad Sci USA 2010;107:4544-9.
100. Ideker T, Krogan NJ. Differential network biology. Mol Syst Biol 2012;8:565.