Rearrangements of 2.5 Kilobases of Noncoding DNA from the Drosophila even-skipped Locus Define Predictive Rules of Genomic cis-Regulatory Logic

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Kim, Ah Ram ^a,b   Martinez, Carlos ^a   Ionides, John ^c   Ramos, Alexandre F ^d   Ludwig, Michael Z ^a   Ogawa, Nobuo ^e   Sharp, David H ^f   Reinitz, John ^a,g  

^a UNIVERSITY OF CHICAGO   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^f LOS ALAMOS NATIONAL LABORATORY   (United States)

^g UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NONCODING DNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; DROSOPHILA EVEN SKIPPED GENE; ENHANCER MSE2; ENHANCER MSE3; ENHANCER REGION; FUSION GENE; GENE; GENE CONSTRUCT; GENE EXPRESSION; GENE LOCUS; GENE REARRANGEMENT; GENOMICS; MATHEMATICAL MODEL; NONHUMAN; PREDICTION; PROTEIN DNA INTERACTION; QUANTITATIVE ANALYSIS; THERMODYNAMICS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REARRANGEMENT; GENOME; HOMEODOMAIN PROTEINS; RNA, UNTRANSLATED; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

EID: 84874772813     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003243     Document Type: Article

References (87)

1. Hong JW, Hendrix D, Levine M, (2008) Shadow enhancers as a source of evolutionary novelty. Science 321: 1314.
2. Perry M, Boettiger AN, Bothma JP, Levine M, (2010) Shadow enhancers foster robustness of Drosophila gastrulation. Current Biology 20: 1562-1567.
3. Perry M, Boettiger AN, Levine M, (2011) Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo. Proceedings of the National Academy of Sciences of the United States of America 108: 13570-13575.
4. Reinitz J, Hou S, Sharp DH, (2003) Transcriptional control in Drosophila. Com Plex Us 1: 54-64.
5. Poustelnikova E, Pisarev A, Blagov M, Samsonova M, Reinitz J, (2004) A database for management of gene expression data in situ. Bioinformatics 20: 2212-2221.
6. Surkova S, Kosman D, Kozlov K, Manu Myasnikova E, et al. (2008) Characterization of the Drosophila segment determination morphome. Developmental Biology 313: 844-862.
7. Pisarev A, Poustelnikova E, Samsonova M, Reinitz J, (2008) FlyEx, the quantitative atlas on segmentation gene expression at cellular resolution. Nucleic Acids Research 37: D560-D566.
8. Janssens H, Hou S, Jaeger J, Kim AR, Myasnikova E, et al. (2006) Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nature Genetics 38: 1159-1165.
9. Louis M, Holm L, Sanchez L, Kaufman M, (2003) Theoretical model for the regulation of Sex-lethal, a gene that controls sex determination and dosage compensation in Drosophila melanogaster. Genetics 165: 1355-1384.
10. Zinzen RP, Senger K, Levine M, Papatsenko D, (2006) Computational models for neurogenic gene expression in the Drosophila embryo. Current Biology 16: 1358-1365.
11. Zinzen RP, Papatsenko D, (2007) Enhancer responses to similarly distributed antagonistic gradients in development. PLoS Comput Biol 3: e84 doi:10.1371/journal.pcbi.0030084.
12. Papatsenko D, Levine M, (2008) Dual regulation by the hunchback gradient in the Drosophila embryo. Proceedings of the National Academy of Sciences of the United States of America 105: 2901-2906.
13. Fakhouri WD, Ay A, Sayal R, Dresch J, Dayringer E, et al. (2010) Deciphering a transcriptional regulatory code: modeling short-range repression in the Drosophila embryo. Molecular Systems Biology 6: 341.
14. Segal E, Raveh-Sadka T, Schroeder M, Unnerstall U, Gaul U, (2008) Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451: 535-540.
15. He X, Samee MAH, Blatti C, Sinha S, (2010) Thermodynamics-based models of transcriptional regulation by enhancers: The roles of synergistic activation, cooperative binding and short-range repression. PLoS Comput Biol 6: e1000935 doi:10.1371/journal.pcbi.1000935.
16. Janssens H, Kosman D, Vanario-Alonso CE, Jaeger J, Samsonova M, et al. (2005) A highthroughput method for quantifying gene expression data from early Drosophila embryos. Development, Genes and Evolution 215: 374-381.
17. Stanojevic D, Hoey T, Levine M, (1989) Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature 341: 331-335.
18. Small S, Kraut R, Hoey T, Warrior R, Levine M, (1991) Transcriptional regulation of a pair-rule stripe in Drosophila. Genes and Development 5: 827-839.
19. Small S, Blair A, Levine M, (1996) Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Developmental Biology 175: 314-324.
20. Small S, Arnosti DN, Levine M, (1993) Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 119: 767-772.
21. Oberstein A, Pare A, Kaplan L, Small S, (2005) Site-specific transgenesis by cre-mediated recombination in Drosophila. Nature Methods 2: 583-585.
22. Myasnikova E, Samsonova M, Kosman D, Reinitz J, (2005) Removal of background signal from in situ data on the expression of segmentation genes in Drosophila. Development, Genes and Evolution 215: 320-326.
23. Surkova S, Myasnikova E, Janssens H, Kozlov KN, Samsonova A, et al. (2008) Pipeline for acquisition of quantitative data on segmentation gene expression from confocal images. Fly 2: 58-66.
24. Small S, Blair A, Levine M, (1992) Regulation of even-skipped stripe 2 in the Drosophila embryo. The EMBO Journal 11: 4047-4057.
25. Lusk RW, Eisen MB, (2010) Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet 6: e1000829 doi:10.1371/journal.pgen.1000829.
26. Erives A, Levine M, (2004) Coordinate enhancers share common organizational features in the Drosophila genome. Proceedings of the National Academy of Sciences USA 101: 3851-3856.
27. Berg OG, Hippel PH, (1988) Selection of DNA binding sites by regulatory proteins. II. The binding specificity of cyclic AMP receptor protein to recognition sites. Journal of Molecular Biology 200: 709-723.
28. Johnson AD, Meyer BJ, Ptashne M, (1979) Interactions between DNA-bound repressors govern regulation by the λ phage repressor. Proceedings of the National Academy of Sciences USA 76: 5061-5065.
29. Ackers GK, Johnson AD, Shea MA, (1982) Quantitative model for gene-regulation by lambda-phage repressor. Proceedings of the National Academy of Sciences USA 79: 1129-1133.
30. Ma X, Yuan D, Diepold K, Scarborough T, Ma J, (1996) The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 112: 1195-1206.
31. Burz DS, Rivera-Pomar R, Jaeckle H, Hanes SD, (1998) Cooperative DNA-binding by Bicoid provides a mechanism for threshold-dependent gene activation in the Drosophila embryo. The EMBO journal 17: 5998-6009.
32. Kim AR (2012) Breaking the genomic cis-regulatory code by an experimental and theoretical analysis of eve enhancer fusions. PhD Thesis, Department of Biochemistry and Cell Biology, Stony Brook University.
33. Louis M (2003) Sex determination in Drosophila melanogaster: a theoretical model for the regulation of the Sex-lethal gene. Ph.D. thesis, University of Cambridge.
34. Reinitz J, Vaisnys JR, (1990) Theoretical and experimental analysis of the phage lambda genetic switch implies missing levels of cooperativity. The Journal of Theoretical Biology 145: 295-318.
35. Simpson-Brose M, Treisman J, Desplan C, (1994) Synergy between the Hunchback and Bicoid morphogens is required for anterior patterning in Drosophila. Cell 78: 855-865.
36. Arnosti DN, Gray S, Barolo S, Zhou J, Levine M, (1996) The gap protein Knirps mediates both quenching and direct repression in the Drosophila embryo. The EMBO Journal 15: 3659-3666.
37. Nibu Y, Zhang H, Bajor E, Barolo S, Small S, et al. (1998) dCtBP mediates transcriptional repression by Knirps, Krüppel and Snail in the Drosophila embryo. The EMBO Journal 17: 7009-7020.
38. Hewitt GF, Strunk B, Margulies C, Priputin T, Wang XD, et al. (1999) Transcriptional repression by the Drosophila Giant protein: Cis element positioning provides an alternative means of interpreting an effector gradient. Development 126: 1201-1210.
39. Gray S, Levine M, (1996) Short-range transcriptional repressors mediate both quenching and direct repression within complex loci in Drosophila. Genes and Development 10: 700-710.
40. Chopra VS, Kong N, Levine M, (2012) Transcriptional repression via antilooping in the Drosophila embryo. Proceedings of the National Academy of Sciences USA 109: 9460-9464.
41. Ptashne M, Gann A, (1997) Transcriptional activation by recruitment. Nature 386: 569-577.
42. Naar AM, Lemon BD, Tjian R, (2001) Transcriptional coactivator complexes. Annual Reviews of Biochemistry 70: 475-501.
43. Park JM, Gim BS, Kim JM, Yoon JH, Kim HS, et al. (2001) Drosophila mediator complex is broadly utilized by diverse gene-specific transcription factors at different types of core promoters. Molecular and Cellular Biology 21: 2312-2323.
44. Berger SL, Triezenberg WDCACSJ, Guarente L, (1990) Selective inhibition of activated but not basal transcription by the acidic activation domain of VP16: Evidence for transcriptional adaptors. Cell 61: 1199-1208.
45. Berger SL, Pina B, Silverman N, Marcus GA, Agapite J, et al. (1990) Genetic isolation of ADA2: A potential transcriptional adaptor required for function of certain acidic activation domains. Cell 70: 251-265.
46. Lemon B, Tijian R, (2000) Orchestrated response: a symphony of transcription factors for gene control. Genes and Development 14: 2551-2569.
47. Tamkun JW, Deuring R, Scott MP, Kissinger M, Pattatucci AM, et al. (1992) Brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcription activator SNF2/SWI2. Cell 68: 561-572.
48. Saurin AJ, Shao Z, Erdjument-Bromage H, Tempst P, Kingston RE, (2001) A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412: 655-660.
49. Han K, Levine M, Manley JL, (1989) Synergistic activation and repression of transcription by Drosophila homeobox proteins. Cell 56: 573-583.
50. Yan R, Small S, Desplan C, Dearolf CR, Jr JED (1996) Identification of a stat gene that functions in Drosophila development. Cell 84: 421-430.
51. Ludwig MZ, Patel NH, Kreitman M, (1998) Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125: 949-958.
52. Fujioka M, Emi-Sarker Y, Yusibova GL, Goto T, Jaynes JB, (1999) Analysis of an even-skipped rescue transgene reveals both composite and discrete neuronal and early blastoderm enhancers, and multi-stripe positioning by gap gene repressor gradients. Development 126: 2527-2538.
53. Ludwig MZ, Bergman CM, Patel NH, Kreitman M, (2000) Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564-567.
54. Hare EE, Peterson BK, Iyer VN, Meier R, Eisen MB, (2008) Sepsid even-skipped enhancers are functionally conserved in Drosopila despite lack of sequence conservation. PLoS Genet 4: e1000106 doi:10.1371/journal.pgen.1000106.
55. Driever W, Thoma G, Nüsslein-Volhard C, (1989) Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the Bicoid morphogen. Nature 340: 363-367.
56. Hoch M, Schröder C, Seifert E, Jäckle H, (1990) Cis-acting control elements for Krüppel expression in the Drosophila embryo. The EMBO Journal 9: 2587-2595.
57. Klingler M, Soong J, Butler B, Gergen JP, (1996) Disperse versus compact elements for the regulation of runt stripes in Drosophila. Developmental Biology 177: 73-84.
58. Howard KR, Struhl G, (1990) Decoding positional information: regulation of the pair-rule gene hairy. Development 110: 1223-1231.
59. Fujioka M, Jaynes JB, Goto T, (1995) Early even-skipped stripes act as morphogenetic gradients at the single cell level to establish engrailed expression. Development 121: 4371-4382.
60. Sackerson C, Fujioka M, Goto T, (1999) The even-skipped locus is contained in a 16-kb chromatin domain. Developmental Biology 211: 39-52.
61. Stanojevic D, Small S, Levine M, (1991) Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 254: 1385-1387.
62. Ludwig MZ, Manu Kittler R, White KP, Kreitman M, (2011) Consequences of eukaryotic enhancer architecture for gene expression dynamics, development, and fitness. PLoS Genet 7: e1002364. doi:10.1371/journal.pgen.1002364.
63. Jaeger J, Blagov M, Kosman D, Kozlov KN, Manu, et al. (2004) Dynamical analysis of regulatory interactions in the gap gene system of Drosophila melanogaster. Genetics 167: 1721-1737.
64. Frasch M, Levine M, (1987) Complementary patterns of even-skipped and fushi-tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila. Genes and Development 1: 981-995.
65. Reinitz J, Sharp DH, (1995) Mechanism of eve stripe formation. Mechanisms of Development 49: 133-158.
66. Ma Y, Niemitz EL, Nambu PA, Shan X, Sackerson C, et al. (1998) Gene regulatory functions of Drosophila Fish-hook, a high mobility group domain Sox protein. Mechanisms of Development 73: 169-182.
67. Kirov N, Zhelnin L, Shah J, Rushlow C, (1993) Conversion of a silencer into an enhancer: evidence for a co-repressor in dorsal-mediated repression in Drosophila. The EMBO Journal 12: 3193-3199.
68. Kirov N, Lieberman P, Rushlow C, (1996) The transcriptional corepressor DSP1 inhibits activated transcription by disrupting TFIIA-TBP complex formation. The EMBO Journal 15: 7079-7087.
69. Kerppola TK, Curran T, (1991) Fos-Jun heterodimers and Jun homodimers bend DNA in opposite orientations: Implications for transcription factor cooperativity. Cell 66: 317-326.
70. Maerkl SJ, Quake SR, (2007) A systems approach to measuring the binding energy landscapes of transcription factors. Science 315: 233-237.
71. Barolo S, Levine M, (1997) Hairy mediates dominant repression in the Drosophila embryo. The EMBO Journal 16: 2883-2891.
72. Sedighi M, Sengupta AM, (2007) Epigenetic chromatin silencing: bistability and front propagation. Physical Biology 4: 246-255.
73. Gottesfeld JM, Melton DA, (1978) The length of nucleosome-associated DNA is the same in both transcribed and nontranscribed regions of chromatin. Nature 273: 317-319.
74. Rubel O, Weber GH, Keranen SVE, Fowlkes CC, Hendriks LCL,et al. (2006) PointCloudXplore: Visual Analysis of 3D Gene Expression Data Using Physical Views and Parallel Coordinates. In: Eurographics/IEEE-VGTC Symposium on Visualization. pp. 203-210.
75. Abramoff MD, Magalhaes P, Ram S, (2004) Image Processing with Image J. Biophotonics International 11: 36-42.
76. Roulet E, Busso S, Camargo AA, Simpson AJG, Mermod N, et al. (2002) High-throughput SELEX SAGE method for quantitative modeling of transcription-factor binding sites. Nature Biotechnology 20: 831-835.
77. Orgawa N, Biggin MD, (2012) High-Throughput SELEX Determination of DNA Sequences Bound by Transcription Factors In Vitro. Methods in Molecular Biology 786: 51-63.
78. Bailey TL, Williams N, Misleh C, Li WW, (2006) MEME: discovering and analyzing dna and protein sequence motifs. Nucleic acids research 34: 369-373.
79. Rajewsky N, Vergassola M, Gaul U, Siggia ED, (2002) Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 3: 30.
80. Berman BP, Nibu Y, Pfeiffer BD, Tomancak P, Celniker SE, et al. (2002) Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proceedings of the National Academy of Sciences USA 99: 757-762.
81. 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 Research pp. 1-14.
82. Li X, 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.
83. Gilbert DG (2005). DroSpeGe, a public database of Drosophila species genomes. Http://insects.eugenes.org/DroSpeGe/.
84. Gilbert DG, (2007) DroSpeGe: rapid access database for new Drosophila species genomes. Nucleic Acids Research 35: D480-D485.
85. Lam J, Delosme JM (1988) An efficient simulated annealing schedule: Derivation. Technical Report 8816, Yale Electrical Engineering Department, New Haven, CT.
86. Lam J, Delosme JM (1988) An efficient simulated annealing schedule: Implementation and evaluation. Technical Report 8817, Yale Electrical Engineering Department, New Haven, CT.
87. Hawley DK, McClure WR, (1982) Mechanism of activation of transcription initiation from the lambda-PRM promoter. The Journal of Molecular Biology 157: 493-525.