Quantitative analysis of the Drosophila segmentation regulatory network using pattern generating potentials

PLoS Biology

Volumn 8, Issue 8, 2010, Pages 51-52

  Kazemian, Majid ^a   Blatti, Charles ^a   Richards, Adam ^b   McCutchan, Michael ^c   Wakabayashi Ito, Noriko ^b   Hammonds, Ann S ^d   Celniker, Susan E ^d   Kumar, Sudhir ^c   Wolfe, Scot A ^b   Brodsky, Michael H ^b   Sinha, Saurabh ^a,e  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; INSECT PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; INSECT GENETICS; INSECT GENOME; NONHUMAN; PREDICTION; QUANTITATIVE ANALYSIS; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; COMPUTER PROGRAM; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; METHODOLOGY; MORPHOGENESIS; PRENATAL DEVELOPMENT; PROTEIN BINDING;

METAZOA;

ANIMALS; BINDING SITES; BODY PATTERNING; COMPUTATIONAL BIOLOGY; DROSOPHILA; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; INSECT PROTEINS; MODELS, GENETIC; PROTEIN BINDING; SOFTWARE; TRANSCRIPTION FACTORS;

EID: 77956830473     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000456     Document Type: Article

References (59)

1. Davidson E (2001) Genomic regulatory systems: development and evolution: Academic Press.
2. Schroeder MD, Pearce M, Fak J, Fan H, Unnerstall U, et al. (2004) Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol 2: E271. doi:10.1371/journal.pbio.0020271.
3. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, et al. (2000) Genomewide location and function of DNA binding proteins. Science 290: 2306-2309.
4. Weinmann AS, Yan PS, Oberley MJ, Huang TH, Farnham PJ (2002) Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes Dev 16: 235-244.
5. Levine M(2008) A systems view of Drosophila segmentation. Genome Biol 9: 207.
6. 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.
7. Zeitlinger J, Zinzen RP, Stark A, Kellis M, Zhang H, et al. (2007) Wholegenome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 21: 385-390.
8. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EE (2009) Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462: 65-70.
9. Frith MC, Li MC, Weng Z (2003) Cluster-Buster: finding dense clusters of motifs in DNA sequences. Nucleic Acids Res 31: 3666-3668.
10. 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.
11. Berman BP, Pfeiffer BD, Laverty TR, Salzberg SL, Rubin GM, et al. (2004) Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol 5: R61.
12. Sinha S, Schroeder MD, Unnerstall U, Gaul U, Siggia ED (2004) Cross-species comparison significantly improves genome-wide prediction of cis-regulatory modules in Drosophila. BMC Bioinformatics 5: 129.
13. Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, et al. (2007) Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232.
14. 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.
15. Bulyk ML, McGuire AM, Masuda N, Church GM (2004) A motif co-occurrence approach for genome-wide prediction of transcription-factor-binding sites in Escherichia coli. Genome Res 14: 201-208.
16. Noyes MB, Christensen RG, Wakabayashi A, Stormo GD, Brodsky MH, et al. (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133: 1277-1289.
17. Sinha S, van Nimwegen E, Siggia ED (2003) A probabilistic method to detect regulatory modules. Bioinformatics 19 Suppl 1: i292-i301.
18. Stone EA, Sidow A (2007) Constructing a meaningful evolutionary average at the phylogenetic center of mass. BMC Bioinformatics 8: 222.
19. MacArthur S, Li XY, Li J, Brown JB, Chu HC, et al. (2009) 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 10: R80.
20. 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.
21. 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.
22. Perkins TJ, Jaeger J, Reinitz J, Glass L (2006) Reverse engineering the gap gene network of Drosophila melanogaster. PLoS Comput Biol 2: e51. doi:10.1371/ journal.pcbi.0020051.
23. Lohr U, Chung HR, Beller M, Jackle H (2009) Antagonistic action of Bicoid and the repressor Capicua determines the spatial limits of Drosophila head gene expression domains. Proc Natl Acad Sci U S A.
24. Ochoa-Espinosa A, Yu D, Tsirigos A, Struffi P, Small S (2009) Anteriorposterior positional information in the absence of a strong Bicoid gradient. Proc Natl Acad Sci U S A 106: 3823-3828.
25. Zhu W, Foehr M, Jaynes JB, Hanes SD (2001) Drosophila SAP18, a member of the Sin3/Rpd3 histone deacetylase complex, interacts with Bicoid and inhibits its activity. Dev Genes Evol 211: 109-117.
26. 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.
27. Liaw GJ, Rudolph KM, Huang JD, Dubnicoff T, Courey AJ, et al. (1995) The torso response element binds GAGA and NTF-1/Elf-1, and regulates tailless by relief of repression. Genes Dev 9: 3163-3176.
28. Jimenez G, Guichet A, Ephrussi A, Casanova J (2000) Relief of gene repression by torso RTK signaling: role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev 14: 224-231.
29. Kumar S, Consortium F (2009) A knowledgebase spatiotemporal expression patterns at a genomic-scale in the fruit-fly embryogenesis (www.flyexpress.net). Arizona State University, Tempe, Arizona 85287, USA.
30. Hong JW, Hendrix DA, Levine MS (2008) Shadow enhancers as a source of evolutionary novelty. Science 321: 1314.
31. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, et al. (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105: 9715-9720.
32. Bergman CM, Carlson JW, Celniker SE (2005) Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila melanogaster. Bioinformatics 21: 1747-1749.
33. Kim Y, Coppey M, Grossman R, Ajuria L, Jimenez G, et al. (2010) MAPK substrate competition integrates patterning signals in the Drosophila embryo. Curr Biol 20: 446-451.
34. Mohler J (1993) Genetic regulation of CNC expression in the pharnygeal primordia of Drosophila blastoderm embryos. Development Genes and Evolution 202: 214-223.
35. Wu LH, Lengyel JA (1998) Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125: 2433-2442.
36. Weigel D, Jurgens G, Klingler M, Jackle H (1990) Two gap genes mediate maternal terminal pattern information in Drosophila. Science 248: 495-498.
37. Pignoni F, Steingrimsson E, Lengyel JA (1992) bicoid and the terminal system activate tailless expression in the early Drosophila embryo. Development 115: 239-251.
38. Zhou B, Bagri A, Beckendorf SK (2001) Salivary gland determination in Drosophila: a salivary-specific, fork head enhancer integrates spatial pattern and allows fork head autoregulation. Dev Biol 237: 54-67.
39. 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.
40. Manu, Surkova S, Spirov AV, Gursky VV, Janssens H, et al. (2009) Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation. PLoS Biol 7: e1000049. doi:10.1371/journal.pbio.1000049.
41. Stevens LM, Beuchle D, Jurcsak J, Tong X, Stein D (2003) The Drosophila embryonic patterning determinant torsolike is a component of the eggshell. Curr Biol 13: 1058-1063.
42. Elnitski L, Hardison RC, Li J, Yang S, Kolbe D, et al. (2003) Distinguishing regulatory DNA from neutral sites. Genome Res 13: 64-72.
43. Chen X, Blanchette M (2007) Prediction of tissue-specific cis-regulatory modules using Bayesian networks and regression trees. BMC Bioinformatics 8 Suppl 10: S2.
44. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, et al. (2009) Diversity and complexity in DNA recognition by transcription factors. Science 324: 1720-1723.
45. Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, et al. (2007) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 8: R145.
46. Fowlkes CC, Hendriks CL, Keranen SV, Weber GH, Rubel O, et al. (2008) A quantitative spatiotemporal atlas of gene expression in the Drosophila blastoderm. Cell 133: 364-374.
47. 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: D594-598.
48. Bussemaker HJ, Li H, Siggia ED (2001) Regulatory element detection using correlation with expression. Nat Genet 27: 167-171.
49. 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. Nat Genet 38: 1159-1165.
50. Ashyraliyev M, Siggens K, Janssens H, Blom J, Akam M, et al. (2009) Gene circuit analysis of the terminal gap gene huckebein. PLoS Comput Biol 5: e1000548. doi:10.1371/journal.pcbi.1000548.
51. Moses AM, Pollard DA, Nix DA, Iyer VN, Li XY, et al. (2006) Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput Biol 2: e130. doi:10.1371/journal.pcbi.0020130.
52. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
53. Liang Z, Biggin MD (1998) Eve and ftz regulate a wide array of genes in blastoderm embryos: the selector homeoproteins directly or indirectly regulate most genes in Drosophila. Development 125: 4471-4482.
54. Lin S, Riggs AD (1975) The general affinity of lac repressor for E. coli DNA: implications for gene regulation in procaryotes and eucaryotes. Cell 4: 107-111.
55. Won KJ, Agarwal S, Shen L, Shoemaker R, Ren B, et al. (2009) An integrated approach to identifying cis-regulatory modules in the human genome. PLoS One 4: e5501. doi:10.1371/journal.pone.0005501.
56. Felsenstein J (1973) Maximum-likelihood estimation of evolutionary trees from continuous characters. Am J Hum Genet 25: 471-492.
57. Ronen O, Rohlicek JR, Ostendorf M (1995) Parameter estimation of dependence tree models using the EM algorithm. IEEE SIGNAL PROCESSING LETTERS 2: 157-159.
58. R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
59. Kumar S, Jayaraman K, Panchanathan S, Gurunathan R, Marti-Subirana A, et al. (2002) BEST: a novel computational approach for comparing gene expression patterns from early stages of Drosophila melanogaster development. Genetics 162: 2037-2047.