High resolution mapping of Twist to DNA in Drosophila embryos: Efficient functional analysis and evolutionary conservation

Genome Research

Volumn 21, Issue 4, 2011, Pages 566-577

  Ozdemir, Anil ^a   Fisher Aylor, Katherine I ^a   Pepke, Shirley ^a   Samanta, Manoj ^b   Dunipace, Leslie ^a   McCue, Kenneth ^a   Zeng, Lucy ^c   Ogawa, Nobuo ^c   Wold, Barbara J ^a   Stathopoulos, Angelike ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Systemix Institute   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SU(H); TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; DROSOPHILA; E BOX ELEMENT; EMBRYO; GENE MAPPING; GENETIC ASSOCIATION; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; TRANSGENICS;

ANIMALS; BASE COMPOSITION; BASE SEQUENCE; BINDING SITES; COMPUTATIONAL BIOLOGY; CONSENSUS SEQUENCE; CONSERVED SEQUENCE; DNA; DROSOPHILA; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TWIST TRANSCRIPTION FACTOR;

DROSOPHILA MELANOGASTER;

EID: 79953311672     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.104018.109     Document Type: Article

References (52)

1. Arnosti DN, Kulkarni MM. 2005. Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards? J Cell Biochem 94: 890-898.
2. Auerbach RK, Euskirchen G, Rozowsky J, Lamarre-Vincent N, Moqtaderi Z, Lefrancois P, Struhl K, Gerstein M, Snyder M. 2009. Mapping accessible chromatin regions using Sono-Seq. Proc Natl Acad Sci 106: 14926-14931.
3. Bailey TL, Williams N, Misleh C, Li WW. 2006. MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34: W369-373 (Web Server issue).
4. Bergman CM, Pfeiffer BD, Rincon-Limas DE, Hoskins RA, Gnirke A, Mungall CJ, Wang AM, Kronmiller B, Pacleb J, Park S, et al. 2002. Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome. Genome Biol 3: RESEARCH0086. doi: 10.1186/gb-2002-3-12- research0086.
5. Berman BP, Nibu Y, Pfeiffer BD, Tomancak P, Celniker SE, Levine M, Rubin GM, Eisen MB. 2002. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci 99: 757-762. (Pubitemid 34106583)
6. Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, et al. 2010. Genome-wide MyoD binding in skeletal muscle cells: A potential for broad cellular reprogramming. Dev Cell 18: 662-674.
7. Castanon I, Von Stetina S, Kass J, Baylies MK. 2001. Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128: 3145-3159. (Pubitemid 32825758)
8. Chopra VS, Levine M. 2009. Combinatorial patterning mechanisms in the Drosophila embryo. Brief Funct Genomics Proteomics 8: 243-249.
9. Crocker J, Tamori Y, Erives A. 2008. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6: e263. doi: 10.1371/journal.pbio.0060263.
10. Davidson EH. 2006. The regulatory genome: Gene regulatory networks in development and evolution. Academic, Burlington, MA.
11. Erives A, Levine M. 2004. Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci 101: 3851-3856. (Pubitemid 38381066)
12. Fullwood MJ, Ruan Y. 2009. ChIP-based methods for the identification of long-range chromatin interactions. J Cell Biochem 107: 30-39.
13. Gonzalez-Crespo S, Levine M. 1993. Interactions between dorsal and helixloop- helix proteins initiate the differentiation of the embryonic mesoderm and neuroectoderm in Drosophila. Genes Dev 7: 1703-1713. (Pubitemid 23269317)
14. Grove CA, De Masi F, Barrasa MI, Newburger DE, Alkema MJ, Bulyk ML, Walhout AJ. 2009. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 138: 314-327.
15. Gurudatta BV, Corces VG. 2009. Chromatin insulators: Lessons from the fly. Brief Funct Genomics Proteomics 8: 276-282.
16. Ho MC, Johnsen H, Goetz SE, Schiller BJ, Bae E, Tran DA, Shur AS, Allen JM, Rau C, Bender W, et al. 2009. Functional evolution of cis-regulatory modules at a homeotic gene in Drosophila. PLoS Genet 5: e1000709. doi: 10.1371/journal.pgen.1000709.
17. Ip YT, Levine M, Small SJ. 1992a. The bicoid and dorsal morphogens use a similar strategy to make stripes in the Drosophila embryo. J Cell Sci Suppl 16: 33-38. (Pubitemid 23097468)
18. Ip YT, Park RE, Kosman D, Bier E, Levine M. 1992b. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes Dev 6: 1728-1739.
19. Ip YT, Park RE, Kosman D, Yazdanbakhsh K, Levine M. 1992c. dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 6: 1518-1530.
20. Iyer V, Struhl K. 1995. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J 14: 2570-2579.
21. Jiang J, Rushlow CA, Zhou Q, Small S, Levine M. 1992. Individual dorsal morphogen binding sites mediate activation and repression in the Drosophila embryo. EMBO J 11: 3147-3154.
22. Johnson DS, Mortazavi A, Myers RM, Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502. (Pubitemid 46906620)
23. Landolin JM, Johnson DS, Trinklein ND, Aldred SF, Medina C, Shulha H, Weng Z, Myers RM. 2010. Sequence features that drive human promoter function and tissue specificity. Genome Res 20: 890-898.
24. Lehmann M. 2004. Anything else but GAGA: A nonhistone protein complex reshapes chromatin structure. Trends Genet 20: 15-22. (Pubitemid 38032816)
25. Levine M, Tjian R. 2003. Transcription regulation and animal diversity. Nature 424: 147-151. (Pubitemid 36858677)
26. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA, Iyer VN, Hechmer A, Simirenko L, Stapleton M, Luengo Hendriks CL, 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.
27. Liberman LM, Stathopoulos A. 2009. Design flexibility in cis-regulatory control of gene expression: Synthetic and comparative evidence. Dev Biol 327: 578-589.
28. 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.
29. MacArthur S, Li XY, Li J, Brown JB, Chu HC, Zeng L, Grondona BP, Hechmer A, Simirenko L, Keranen SV, 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. doi: 10.1186/gb-2009-10-7-r80.
30. Markstein M, Markstein P, Markstein V, Levine MS. 2002. Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc Natl Acad Sci 99: 763-768. (Pubitemid 34106584)
31. MarksteinM, Zinzen R, Markstein P, Yee KP, Erives A, Stathopoulos A, Levine M. 2004. A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 131: 2387-2394. (Pubitemid 38877646)
32. Massari ME, Murre C. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429-440. (Pubitemid 30023084)
33. Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB, et al. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58: 537-544. (Pubitemid 19203538)
34. Nam J, Dong P, Tarpine R, Istrail S, Davidson EH. 2010. Functional cis-regulatory genomics for systems biology. Proc Natl Acad Sci 107: 3930-3935.
35. Ogawa N, Biggin MD. 2011. High-throughput SELEX determination of DNA sequences bound by transcription factors in vitro. In Methods inmolecular biology (ed. B Deplanke), Humana Press, Clifton, New Jersey (in press).
36. Peckham HE, Thurman RE, Fu Y, Stamatoyannopoulos JA, Noble WS, Struhl K, Weng Z. 2007. Nucleosome positioning signals in genomic DNA. Genome Res 17: 1170-1177. (Pubitemid 47204860)
37. Pepke S, Wold B, Mortazavi A. 2009. Computation for ChIP-seq and RNAseq studies. Nat Methods 6 (11 Suppl): S22-S32.
38. Reeves GT, Stathopoulos A. 2009. Graded dorsal and differential gene regulation in the Drosophila embryo. Cold Spring Harb Perspect Biol 1: a000836. doi: 10.1101/cshperspect.a000836.
39. Sandmann T, Jakobsen JS, Furlong EE. 2006. ChIP-on-chip protocol for genome-wide analysis of transcription factor binding in Drosophila melanogaster embryos. Nat Protoc 1: 2839-2855.
40. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, Furlong EE. 2007. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev 21: 436-449.
41. Schuettengruber B, Cavalli G. 2009. Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136: 3531-3542.
42. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)
43. Small S, Blair A, Levine M. 1992. Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J 11: 4047-4057.
44. Sosinsky A, Honig B, Mann RS, Califano A. 2007. Discovering transcriptional regulatory regions in Drosophila by a nonalignment method for phylogenetic footprinting. Proc Natl Acad Sci 104: 6305-6310. (Pubitemid 47186090)
45. Stathopoulos A, Levine M. 2002. Linear signaling in the Toll-Dorsal pathway of Drosophila: Activated Pelle kinase specifies all threshold outputs of gene expression while the bHLH protein Twist specifies a subset. Development 129: 3411-3419.
46. Stathopoulos A, Levine M. 2005. Genomic regulatory networks and animal development. Dev Cell 9: 449-462. (Pubitemid 41430729)
47. 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. (Pubitemid 35441250)
48. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, Millburn G, Osumi-Sutherland D, Schroeder A, Seal R, et al. 2009. FlyBase: Enhancing Drosophila gene ontology annotations. Nucleic Acids Res 37: D555-D559.
49. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E, Batzoglou S, Myers RM, Sidow A. 2008. Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat Methods 5: 829-834.
50. Zeitlinger J, Zinzen RP, Stark A, Kellis M, Zhang H, Young RA, Levine M. 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.
51. Zinzen R, Senger K, Levine M, Papatsenko D. 2006. Computational models for neurogenic gene expression in the Drosophila embryo. Curr Biol 16: 1358-1365. (Pubitemid 43975367)
52. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EE. 2009. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462: 65-70.