Spatial expression of transcription factors in Drosophila embryonic organ development

Genome Biology

Volumn 14, Issue 12, 2013, Pages

  Hammonds, Ann S ^a   Bristow, Christopher A ^b,c,d   Fisher, William W ^a   Weiszmann, Richard ^a   Wu, Siqi ^a,e   Hartenstein, Volker ^f   Kellis, Manolis ^b,c   Yu, Bin ^e   Frise, Erwin ^a   Celniker, Susan E ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; DROSOPHILA PROTEIN; RNA;

ADULT; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; DIGESTIVE SYSTEM; DNA BINDING DOMAIN; DNA STRUCTURE; DROSOPHILA; EMBRYO DEVELOPMENT; ENDOCRINE SYSTEM; EPIDERMIS; FOREGUT; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETIC ANALYSIS; HINDGUT; IN SITU HYBRIDIZATION; LARVA; MIDGUT; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MORPHOLOGY; MUSCULOSKELETAL SYSTEM; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ORGANOGENESIS; PERIPHERAL NERVOUS SYSTEM; PUPA (LIFE CYCLE STAGE); REFERENCE DATABASE; RNA SEQUENCE; STOMATOGASTRIC NERVOUS SYSTEM; TISSUE SPECIFICITY; ANIMAL; ANTIBODY SPECIFICITY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; EMBRYO; GENE EXPRESSION; ORGAN SYSTEMS; PROTEIN EXPRESSION;

ANIMALIA; METAZOA;

ANIMALS; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; IN SITU HYBRIDIZATION; ORGAN SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84890492742     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-12-r140     Document Type: Article

References (59)

1. Chang YC, Jang AC, Lin CH, Montell DJ. Castor is required for Hedgehog-dependent cell-fate specification and follicle stem cell maintenance in Drosophila oogenesis. Proc Natl Acad Sci USA 2013, 110:E1734-E1742. 10.1073/pnas.1300725110, 3651482, 23610413.
2. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 2011, 9:e1001046. 10.1371/journal.pbio.1001046, 3079585, 21526222.
3. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, Lin MF, Washietl S, Arshinoff BI, Ay F, Meyer PE, Robine N, Washington NL, Di Stefano L, Berezikov E, Brown CD, Candeias R, Carlson JW, Carr A, Jungreis I, Marbach D, Sealfon R, Tolstorukov MY, Will S, Alekseyenko AA, Artieri C, Booth BW, et al. modENCODE Consortium Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010, 330:1787-1797. 3192495, 21177974, modENCODE Consortium.
4. Negre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, Li Z, Ishii H, Spokony RF, Chen J, Hwang L, Cheng C, Auburn RP, Davis MB, Domanus M, Shah PK, Morrison CA, Zieba J, Suchy S, Senderowicz L, Victorsen A, Bild NA, Grundstad AJ, Hanley D, MacAlpine DM, Mannervik M, et al. A cis-regulatory map of the Drosophila genome. Nature 2011, 471:527-531. 10.1038/nature09990, 3179250, 21430782.
5. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, Alves P, Chateigner A, Perry M, Morris M, Auerbach RK, Feng X, Leng J, Vielle A, Niu W, Rhrissorrakrai K, Agarwal A, Alexander RP, Barber G, Brdlik CM, Brennan J, Brouillet JJ, Carr A, Cheung MS, Clawson H, Contrino S, et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2011, 330:1775-1787.
6. Stamatoyannopoulos JA, Snyder M, Hardison R, Ren B, Gingeras T, Gilbert DM, Groudine M, Bender M, Kaul R, Canfield T, Giste E, Johnson A, Zhang M, Balasundaram G, Byron R, Roach V, Sabo PJ, Sandstrom R, Stehling AS, Thurman RE, Weissman SM, Cayting P, Hariharan M, Lian J, Cheng Y, Landt SG, Ma Z, Wold BJ, Dekker J, Crawford GE, et al. Mouse ENCODE Consortium An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol 2012, 13:418. 3491367, 22889292, Mouse ENCODE Consortium.
7. Tabara H, Motohashi T, Kohara Y. A multi-well version of in situ hybridization on whole mount embryos of Caenorhabditis elegans. Nucleic Acids Res 1996, 24:2119-2124. 10.1093/nar/24.11.2119, 145910, 8668544.
8. Tomancak P, Beaton A, Weiszmann R, Kwan E, Shu S, Lewis SE, Richards S, Ashburner M, Hartenstein V, Celniker SE, Rubin GM. Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol 2002, 3:RESEARCH0088-0088.14.
9. Imai KS, Hino K, Yagi K, Satoh N, Satou Y. Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 2004, 131:4047-4058. 10.1242/dev.01270, 15269171.
10. Bell GW, Yatskievych TA, Antin PB. GEISHA, a whole-mount in situ hybridization gene expression screen in chicken embryos. Dev Dyn 2004, 229:677-687. 10.1002/dvdy.10503, 14991723.
11. Visel A, Thaller C, Eichele G. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 2004, 32:D552-D556. 10.1093/nar/gkh029, 308763, 14681479.
12. Pollet N, Muncke N, Verbeek B, Li Y, Fenger U, Delius H, Niehrs C. An atlas of differential gene expression during early Xenopus embryogenesis. Mech Dev 2005, 122:365-439. 10.1016/j.mod.2004.11.009, 15763213.
13. Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, Hartenstein V, Celniker SE, Rubin GM. Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 2007, 8:R145. 10.1186/gb-2007-8-7-r145, 2323238, 17645804.
14. Tassy O, Dauga D, Daian F, Sobral D, Robin F, Khoueiry P, Salgado D, Fox V, Caillol D, Schiappa R, Laporte B, Rios A, Luxardi G, Kusakabe T, Joly JS, Darras S, Christiaen L, Contensin M, Auger H, Lamy C, Hudson C, Rothbächer U, Gilchrist MJ, Makabe KW, Hotta K, Fujiwara S, Satoh N, Satou Y, Lemaire P. The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. Genome Res 2010, 20:1459-1468. 10.1101/gr.108175.110, 2945195, 20647237.
15. Zhao J, Klyne G, Benson E, Gudmannsdottir E, White-Cooper H, Shotton D. FlyTED: the Drosophila testis gene expression database. Nucleic Acids Res 2010, 38:D710-D715. 10.1093/nar/gkp1006, 2808924, 19934263.
16. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176. 10.1038/nature05453, 17151600.
17. Niehrs C, Pollet N. Synexpression groups in eukaryotes. Nature 1999, 402:483-487. 10.1038/990025, 10591207.
18. Frise E, Hammonds AS, Celniker SE. Systematic image-driven analysis of the spatial Drosophila embryonic expression landscape. Mol Syst Biol 2010, 6:345. 2824522, 20087342.
19. McQuilton P, St Pierre SE, Thurmond J. FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res 2012, 40:D706-D714. 10.1093/nar/gkr1030, 3245098, 22127867.
20. Bard JB. Anatomics: the intersection of anatomy and bioinformatics. J Anat 2005, 206:1-16. 10.1111/j.0021-8782.2005.00376.x, 1571451, 15679867.
21. Haudry Y, Berube H, Letunic I, Weeber PD, Gagneur J, Girardot C, Kapushesky M, Arendt D, Bork P, Brazma A, Furlong EE, Wittbrodt J, Henrich TL. 4DXpress: a database for cross-species expression pattern comparisons. Nucleic Acids Res 2008, 36:D847-D853. 2238840, 17916571.
22. Weiszmann R, Hammonds AS, Celniker SE. Determination of gene expression patterns using high-throughput RNA in situ hybridization to whole-mount Drosophila embryos. Nat Protoc 2009, 4:605-618. 10.1038/nprot.2009.55, 2780369, 19360017.
23. Zdobnov EM, Apweiler R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848. 10.1093/bioinformatics/17.9.847, 11590104.
24. Reece-Hoyes JS, Deplancke B, Shingles J, Grove CA, Hope IA, Walhout AJ. A compendium of Caenorhabditis elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biol 2005, 6:R110. 10.1186/gb-2005-6-13-r110, 1414109, 16420670.
25. Kummerfeld SK, Teichmann SA. DBD: a transcription factor prediction database. Nucleic Acids Res 2006, 34:D74-D81. 10.1093/nar/gkj131, 1347493, 16381970.
26. BDGP gene expression patterns resource. [http://insitu.fruitfly.org].
27. Adryan B, Teichmann SA. The developmental expression dynamics of Drosophila melanogaster transcription factors. Genome Biol 2010, 11:R40. 10.1186/gb-2010-11-4-r40, 2884543, 20384991.
28. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, et al. The developmental transcriptome of Drosophila melanogaster. Nature 2011, 471:473-479. 10.1038/nature09715, 3075879, 21179090.
29. Kohonen T. Essentials of the self-organizing map. Neural Netw 2013, 37:52-65.
30. Stuart JMS, Segal E, Koller D, Kim SK. A gene-coexpression network for global discovery of conserved genetic modules. Science 2003, 302:249-255. 10.1126/science.1087447, 12934013.
31. BDGP MapExplorer. [http://insitu.fruitfly.org/som].
32. Kispert A, Herrmann BG, Leptin M, Reuter R. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev 1994, 8:2137-2150. 10.1101/gad.8.18.2137, 7958884.
33. De Velasco B, Shen J, Go S, Hartenstein V. Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol 2004, 274:280-294. 10.1016/j.ydbio.2004.07.015, 15385159.
34. Moses K, Rubin GM. Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 1991, 5:583-593. 10.1101/gad.5.4.583, 2010085.
35. Pfreundt U, James DP, Tweedie S, Wilson D, Teichmann SA, Adryan B. FlyTF: improved annotation and enhanced functionality of the Drosophila transcription factor database. Nucleic Acids Res 2010, 38:D443-D447. 10.1093/nar/gkp910, 2808907, 19884132.
36. Zhu LJ, Christensen RG, Kazemian M, Hull CJ, Enuameh MS, Basciotta MD, Brasefield JA, Zhu C, Asriyan Y, Lapointe DS, Sinha S, Wolfe SA, Brodsky MH. FlyFactorSurvey: a database of Drosophila transcription factor binding specificities determined using the bacterial one-hybrid system. Nucleic Acids Res 2011, 39:D111-D117. 10.1093/nar/gkq858, 3013762, 21097781.
37. Fulton DL, Sundararajan S, Badis G, Hughes TR, Wasserman WW, Roach JC, Sladek R. TFCat: the curated catalog of mouse and human transcription factors. Genome Biol 2009, 10:R29. 10.1186/gb-2009-10-3-r29, 2691000, 19284633.
38. Tanaka K, Shouguchi-Miyata J, Miyamoto N, Ikeda JE. Novel nuclear shuttle proteins, HDBP1 and HDBP2, bind to neuronal cell-specific cis-regulatory element in the promoter for the human Huntington's disease gene. J Biol Chem 2004, 279:7275-7286.
39. Chang YL, King B, Lin SC, Kennison JA, Huang DH. A double-bromodomain protein, FSH-S, activates the homeotic gene ultrabithorax through a critical promoter-proximal region. Mol Cell Biol 2007, 27:5486-5498. 10.1128/MCB.00692-07, 1952094, 17526731.
40. Enuameh MS, Asriyan Y, Richards A, Christensen RG, Hall VL, Kazemian M, Zhu C, Pham H, Cheng Q, Blatti C, Brasefield JA, Basciotta MD, Ou J, McNulty JC, Zhu LJ, Celniker SE, Sinha S, Stormo GD, Brodsky MH, Wolfe SA. Global analysis of Drosophila Cys2-His2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res 2013, 23:928-940. 10.1101/gr.151472.112, 3668361, 23471540.
41. Cronmiller C, Cummings CA. The daughterless gene product in Drosophila is a nuclear protein that is broadly expressed throughout the organism during development. Mech Dev 1993, 42:159-169. 10.1016/0925-4773(93)90005-I, 8217842.
42. Wong MC, Castanon I, Baylies MK. Daughterless dictates Twist activity in a context-dependent manner during somatic myogenesis. Dev Biol 2008, 317:417-429. 10.1016/j.ydbio.2008.02.020, 2435306, 18407256.
43. Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287:795-801. 10.1038/287795a0, 6776413.
44. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570. 10.1038/276565a0, 103000.
45. Junion G, Spivakov M, Girardot C, Braun M, Gustafson EH, Birney E, Furlong EE. A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell 2012, 148:473-486. 10.1016/j.cell.2012.01.030, 22304916.
46. Fowlkes CC, Hendriks CL, Keränen SV, Weber GH, Rübel O, Huang MY, Chatoor S, DePace AH, Simirenko L, Henriquez C, Beaton A, Weiszmann R, Celniker S, Hamann B, Knowles DW, Biggin MD, Eisen MB, Malik J. A quantitative spatiotemporal atlas of gene expression in the Drosophila blastoderm. Cell 2008, 133:364-374. 10.1016/j.cell.2008.01.053, 18423206.
47. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, Mungall C, Svirskas R, Kadonaga JT, Doe CQ, Eisen MB, Celniker SE, Rubin GM. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci USA 2008, 105:9715-9720. 10.1073/pnas.0803697105, 2447866, 18621688.
48. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39:W29-W37. 10.1093/nar/gkr367, 3125773, 21593126.
49. Schultz J, Milpetz F, Bork P, Ponting CP. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 1998, 95:5857-5864. 10.1073/pnas.95.11.5857, 34487, 9600884.
50. Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux PS, Pagni M, Sigrist CJ. The PROSITE database. Nucleic Acids Res 2006, 34:D227-D230. 10.1093/nar/gkj063, 1347426, 16381852.
51. Abhiman S, Iyer LM, Aravind L. BEN: a novel domain in chromatin factors and DNA viral proteins. Bioinformatics 2008, 24:458-461. 10.1093/bioinformatics/btn007, 2477736, 18203771.
52. Fassler J, Landsman D, Acharya A, Moll JR, Bonovich M, Vinson C. B-ZIP proteins encoded by the Drosophila genome: evaluation of potential dimerization partners. Genome Res 2002, 12:1190-1200. 10.1101/gr.67902, 186634, 12176927.
53. Atcha FA, Syed A, Wu B, Hoverter NP, Yokoyama NN, Ting JH, Munguia JE, Mangalam HJ, Marsh JL, Waterman ML. A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol Cell Biol 2007, 27:8352-8363. 10.1128/MCB.02132-06, 2169181, 17893322.
54. Yazdani U, Huang Z, Terman JR. The glucose transporter (GLUT4) enhancer factor is required for normal wing positioning in Drosophila. Genetics 2008, 178:919-929. 10.1534/genetics.107.078030, 2248331, 18245850.
55. Hens K, Feuz JD, Isakova A, Iagovitina A, Massouras A, Bryois J, Callaerts P, Celniker SE, Deplancke B. Automated protein-DNA interaction screening of Drosophila regulatory elements. Nat Methods 2011, 8:1065-70. 10.1038/nmeth.1763, 22037703.
56. Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, Booth BW, Weng J, Park S, Suzuki AM, Wan KH, Yu C, Zhang D, Carlson JW, Cherbas L, Eads BD, Miller D, Mockaitis K, Roberts J, Davis CA, Frise E, Hammonds AS, Olson S, Shenker S, Sturgill D, Samsonova AA, Weiszmann R, Robinson G, Hernandez J, Andrews J, et al. Diversity and dynamics of the Drosophila transcriptome. Nature 2014, In Press.
57. Matlab SOM toolbox. [http://www.cis.hut.fi/projects/somtoolbox/].
58. van der Maten L, Hinton G. Viualizing data using t-SNE. J Mach Learn Res 2008, 9:2579-2605.
59. Adryan B, Teichmann SA. FlyTF: a systematic review of site-specific transcription factors in the fruit fly Drosophila melanogaster. Bioinformatics 2006, 22:1532-1533. 10.1093/bioinformatics/btl143, 16613907.