Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions

Genome Biology

Volumn 10, Issue 7, 2009, Pages

  MacArthur, Stewart ^a,c   Li, Xiao Yong ^a,b   Li, Jingyi ^a   Brown, James B ^b   Cheng, Hou Cheng ^a   Zeng, Lucy ^a   Grondona, Brandi P ^a   Hechmer, Aaron ^a   Simirenko, Lisa ^a   Keränen, Soile V E ^a   Knowles, David W ^a   Stapleton, Mark ^a   Bickel, Peter ^b   Biggin, Mark D ^a   Eisen, Michael B ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BICOID PROTEIN; CAUDAL PROTEIN; DAUGHTERLESS PROTEIN; DICHAETE PROTEIN; DORSAL PROTEIN; GIANT PROTEIN; HAIRY PROTEIN; HUCKEBEIN PROTEIN; HUNCHBACK PROTEIN; KNIRPS PROTEIN; KRUPPEL LIKE FACTOR; MEDEA PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; PROTEIN FTZ; SCHNURRI PROTEIN; SLOPPY PAIRED 1 PROTEIN; SMAD PROTEIN; TAILLESS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; EVE PROTEIN, DROSOPHILA; HOMEODOMAIN PROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BLASTODERM; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; GENE MAPPING; IN VIVO STUDY; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BINDING SITE; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MORPHOGENESIS; PRENATAL DEVELOPMENT; TRANSCRIPTION INITIATION SITE;

ANIMALIA;

ANIMALS; BINDING SITES; BLASTODERM; BODY PATTERNING; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME, INSECT; HOMEODOMAIN PROTEINS; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

EID: 68849103482     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-7-r80     Document Type: Article

References (110)

1. Biggin MD Tjian R Transcriptional regulation in Drosophila: The post-genome challenge. Funct Integr Genomics 2001, 1:223-234. 11793241 10.1007/s101420000021
2. Davidson EH Genomic Regulatory Systems - Development and Evolution San Diego: Academic Press; 2001.
3. Ptashne M Gann A Genes and Signals New York: Cold Spring Harbor Press; 2002.
4. Levine M Tjian R Transcription regulation and animal diversity. Nature 2003, 424:147-151. 12853946 10.1038/nature01763
5. Fiasst S Meyer S Compilation of vertebrate-encoded transcription factors. Nucleic Acids Res 1992, 20:3-26. 1738600 10.1093/nar/20.1.3 310320
6. Pabo CO Sauer RT Transcription factors: Structural families and principles of DNA recognition. Annu Rev Biochem 1992, 61:1053-1095. 1497306 10.1146/annurev.bi.61.070192.005201
7. Berman BP Nibu Y Pfeiffer BD Tomancak P Celniker SE Levine M Rubin GM Eisen MB Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci USA 2002, 99:757-762. 11805330 10.1073/pnas.231608898 117378
8. Berman BP Pfeiffer BD Laverty TR Salzberg SL Rubin GM Eisen MB Celniker SE Computational identification of developmental enhancers: Conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol 2004, 5:R61. 15345045 10.1186/gb-2004-5-9-r61 522868
9. Keranen SV Fowlkes CC Luengo Hendriks CL Sudar D Knowles DW Malik J Biggin MD Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution II: Dynamics. Genome Biol 2006, 7:R124. 17184547 10.1186/gb-2006-7-12-r124 1794437
10. Luengo Hendriks CL Keranen SV Fowlkes CC Simirenko L Weber GH DePace AH Henriquez C Kaszuba DW Hamann B Eisen MB Malik J Sudar D Biggin MD Knowles DW Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution I: Data acquisition pipeline. Genome Biol 2006, 7:R123. 17184546 10.1186/gb-2006-7-12-r123 1794436
11. Li XY MacArthur S Bourgon R Nix D Pollard DA Iyer VN Hechmer A Simirenko L Stapleton M Luengo Hendriks CL Chu HC Ogawa N Inwood W Sementchenko V Beaton A Weiszmann R Celniker SE Knowles DW Gingeras T Speed TP Eisen MB Biggin MD Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 2008, 6:e27. 18271625 10.1371/journal.pbio.0060027 2235902
12. Fowlkes CC Hendriks CL Keranen SV Weber GH Rubel 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. 18423206 10.1016/j.cell.2008.01.053
13. Lewis EB A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570. 103000 10.1038/276565a0
14. Nusslein-Volhard C Wieschaus E Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287:795-801. 6776413 10.1038/ 287795a0
15. Lawrence PA The Making of a Fly: The Genetics of Animal Design Oxford: Blackwell-Scientific; 1992.
16. St Johnston D Nusslein-Volhard C The origin of pattern and polarity in the Drosophila embryo. Cell 1992, 68:201-219. 1733499 10.1016/ 0092-8674(92)90466-P
17. Pankratz M Jackle H Blastoderm segmentation. The Development of Drosophila melanogaster New York: Cold Spring Harbor Laboratory Press Bate M, Martinez Arias A 1993:467-516.
18. Rivera-Pomar R Jackle H From gradients to stripes in Drosophila embryogenesis: Filling in the gaps. Trends Genet 1996, 12:478-483. 8973159 10.1016/0168-9525(96)10044-5
19. Stathopoulos A Levine M Genomic regulatory networks and animal development. Dev Cell 2005, 9:449-462. 16198288 10.1016/ j.devcel.2005.09.005
20. Tsai C Gergen JP Gap gene properties of the pair-rule gene runt during Drosophila segmentation. Development 1994, 120:1671-1683. 8050373
21. Anderson KV Lengyel JA Changing rates of DNA and RNA synthesis in Drosophila embryos. Dev Biol 1981, 82:127-138. 6164584 10.1016/ 0012-1606(81)90434-6
22. Liang Z Biggin MD Eve and ftz regulate a wide array of genes in blastoderm embryos: The selector homeoproteins directly or indirectly regulate most genes in Drosophila. Development 1998, 125:4471-4482. 9778506
23. 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. 17645804 10.1186/ gb-2007-8-7-r145 2323238
24. Harding K Hoey T Warrior R Levine M Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. EMBO J 1989, 8:1205-1212. 400935 2743979
25. Schroeder MD Pearce M Fak J Fan H Unnerstall U Emberly E Rajewsky N Siggia ED Gaul U Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol 2004, 2:E271. 15340490 10.1371/ journal.pbio.0020271 514885
26. Halfon MS Gallo SM Bergman CM REDfly 2.0: An integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila. Nucleic Acids Res 2008, 36:D594-598. 18039705 10.1093/nar/ gkm876 2238825
27. Arnosti DN Barolo S Levine M Small S The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 1996, 122:205-214. 8565831
28. Fujioka M Emi-Sarker Y Yusibova GL Goto T Jaynes JB 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 1999, 126:2527-2538. 10226011
29. Fujioka M Miskiewicz P Raj L Gulledge AA Weir M Goto T Drosophila Paired regulates late even-skipped expression through a composite binding site for the paired domain and the homeodomain. Development 1996, 122:2697-2707. 8787744
30. Walter J Dever CA Biggin MD Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev 1994, 8:1678-1692. 7958848 10.1101/gad.8.14.1678
31. Carr A Biggin MD A comparison of in vivo and in vitro DNA-binding specificities suggests a new model for homeoprotein DNA binding in Drosophila embryos. EMBO J 1999, 18:1598-1608. 10075930 10.1093/emboj/ 18.6.1598 1171247
32. Zeitlinger J Zinzen RP Stark A Kellis M Zhang H Young RA Levine M Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 2007, 21:385-390. 17322397 10.1101/gad.1509607 1804326
33. Blais A Tsikitis M Acosta-Alvear D Sharan R Kluger Y Dynlacht BD An initial blueprint for myogenic differentiation. Genes Dev 2005, 19:553-569. 15706034 10.1101/gad.1281105 551576
34. Boyer LA Lee TI Cole MF Johnstone SE Levine SS Zucker JP Guenther MG Kumar RM Murray HL Jenner RG Gifford DK Melton DA Jaenisch R Young RA Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956. 16153702 10.1016/j.cell.2005.08.020
35. Johnson DS Mortazavi A Myers RM Wold B Genome-wide mapping of in vivo protein-DNA interactions. Science 2007, 316:1497-1502. 17540862 10.1126/ science.1141319
36. Yang A Zhu Z Kapranov P McKeon F Church GM Gingeras TR Struhl K Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006, 24:593-602. 17188034 10.1016/j.molcel.2006.10.018
37. Sandmann T Girardot C Brehme M Tongprasit W Stolc V Furlong EEM A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev 2007, 21:436-449. 17322403 10.1101/gad.1509007 1804332
38. Cawley S Bekiranov S Ng HH Kapranov P Sekinger EA Kampa D Piccolboni A Sementchenko V Cheng J Williams AJ Wheeler R Wong B Drenkow J Yamanaka M Patel S Brubaker S Tammana H Helt G Struhl K Gingeras TR Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004, 116:499-509. 14980218 10.1016/S0092-8674(04)00127-8
39. Rada-Iglesias A Wallerman O Koch C Ameur A Enroth S Clelland G Wester K Wilcox S Dovey OM Ellis PD Wraight VL James K Andrews R Langford C Dhami P Carter N Vetrie D Ponten F Komorowski J Dunham I Wadelius C Binding sites for metabolic disease related transcription factors inferred at base pair resolution by chromatin immunoprecipitation and genomic microarrays. Hum Mol Genet 2005, 14:3435-3447. 16221759 10.1093/hmg/ ddi378
40. Wei CL Wu Q Vega VB Chiu KP Ng P Zhang T Shahab A Yong HC Fu Y Weng Z Liu J Zhao XD Chew JL Lee YL Kuznetsov VA Sung WK Miller LD Lim B Liu ET Yu Q Ng HH Ruan Y A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219. 16413492 10.1016/ j.cell.2005.10.043
41. Bhinge AA Kim J Euskirchen GM Snyder M Iyer VR Mapping the chromosomal targets of STAT1 by Sequence Tag Analysis of Genomic Enrichment (STAGE). Genome Res 2007, 17:910-916. 17568006 10.1101/gr.5574907 1891349
42. Bieda M Xu X Singer MA Green R Farnham PJ Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006, 16:595-605. 16606705 10.1101/gr.4887606 1457046
43. Consortium TEP Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816. 17571346 10.1038/nature05874 2212820
44. Chen X Vega VB Ng HH Transcriptional regulatory networks in embryonic stem cells. Cold Spring Harb Symp Quant Biol 2008, 73:203-209. 19022762
45. Marson A Kretschmer K Frampton GM Jacobsen ES Polansky JK MacIsaac KD Levine SS Fraenkel E von Boehmer H Young RA Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007, 445:931-935. 17237765 10.1038/nature05478
46. Georlette D Ahn S MacAlpine DM Cheung E Lewis PW Beall EL Bell SP Speed T Manak JR Botchan MR Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 2007, 21:2880-2896. 17978103 10.1101/gad.1600107 2049191
47. Moorman C Sun LV Wang J de Wit E Talhout W Ward LD Greil F Lu XJ White KP Bussemaker HJ van Steensel B Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci USA 2006, 103:12027-12032. 16880385 10.1073/pnas.0605003103 1567692
48. Ip YT Park RE Kosman D Yazdanbakhsh K Levine M dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 1992, 6:1518-1530. 1644293 10.1101/gad.6.8.1518
49. Small S Blair A Levine M Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Dev Biol 1996, 175:314-324. 8626035 10.1006/dbio.1996.0117
50. Lin S Riggs AD The general affinity of lac repressor for E. coli DNA: Implications for gene regulation in procaryotes and eukaryotes. Cell 1975, 4:107-111. 1092468 10.1016/0092-8674(75)90116-6
51. Walter J Biggin MD DNA binding specificity of two homeodomain proteins in vitro and in Drosophila embryos. Proc Natl Acad Sci USA 1996, 93:2680-2685. 8610101 10.1073/pnas.93.7.2680 39690
52. von Hippel PH Revzin A Gross CA Wang AC Nonspecific DNA binding of genome regulating proteins as a biological control mechanism: 1. The lac operon: Equilibrium aspects. Proc Natl Acad Sci USA 1974, 71:4808-4812. 4612528 10.1073/pnas.71.12.4808 433986
53. Beato M Eisfeld K Transcription factor access to chromatin. Nucleic Acids Res 1997, 25:3559-3563. 9278473 10.1093/nar/25.18.3559 146956
54. Almer A Rudolph H Hinnen A Horz W Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J 1986, 5:2689-2696. 1167170 3536481
55. Carr A Biggin MD Accesibility of transcriptionanlly inactive genes in speciffically reduced at homeoprotein-DNA binding sites in Drosophila. Nucleic Acids Res 2000, 28:2839-2846. 10908343 10.1093/nar/28.14.2839 102649
56. Wallrath LL Unfolding the mysteries of heterochromatin. Curr Opin Genet Dev 1998, 8:147-153. 9610404 10.1016/S0959-437X(98)80135-4
57. Loo S Rine J Silencers and domains of generalized repression. Science 1994, 264:1768-1771. 8209257 10.1126/science.8209257
58. Kladde MP Simpson RT Chromatin structure mapping in vivo using methyltransferases. Methods Enzymol 1996, 274:214-233. 8902807 full_text
59. Sabo PJ Kuehn MS Thurman R Johnson BE Johnson EM Cao H Yu M Rosenzweig E Goldy J Haydock A Weaver M Shafer A Lee K Neri F Humbert R Singer MA Richmond TA Dorschner MO McArthur M Hawrylycz M Green RD Navas PA Noble WS Stamatoyannopoulos JA Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 2006, 3:511-518. 16791208 10.1038/nmeth890
60. Thomas GH Elgin SC Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J 1988, 7:2191-2201. 454544 2901349
61. Krause HM Klemenz R Gehring WJ Expression, modification, and localization of the fushi tarazu protein in Drosophila embryos. Genes Dev 1988, 2:1021-1036. 3049237 10.1101/gad.2.8.1021
62. Hahn MW Stajich JE Wray GA The effects of selection against spurious transcription factor binding sites. Mol Biol Evol 2003, 20:901-906. 12716998 10.1093/molbev/msg096
63. Sutherland DJ Li M Liu XQ Stefancsik R Raftery LA Stepwise formation of a SMAD activity gradient during dorsal-ventral patterning of the Drosophila embryo. Development 2003, 130:5705-5716. 14534137 10.1242/ dev.00801
64. Array Express Web Site http://www.ebi.ac.uk/microarray-as/ae/
65. BDTNP ChIP/chip Database http://bdtnp.lbl.gov/Fly-Net/chipchip.jsp?w= summary
66. BDTNP TiMAT ChIP/chip Analysis Package http://bdtnp.lbl.gov/Fly-Net/ chipchip.jsp?w=timat
67. Crooks GE Hon G Chandonia JM Brenner SE WebLogo: A sequence logo generator. Genome Res 2004, 14:1188-1190. 15173120 10.1101/gr.849004 419797
68. Ashburner M Ball CA Blake JA Botstein D Butler H Cherry JM Davis AP Dolinski K Dwight SS Eppig JT Harris MA Hill DP Issel-Tarver L Kasarskis A Lewis S Matese JC Richardson JE Ringwald M Rubin GM Sherlock G Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 2000, 25:25-29. 10802651 10.1038/75556
69. Rübel O Weber GH SVE K Fowlkes CC Luengo Hendriks CL Simirenko L Shah NY Eisen MB Biggin MD Hagen H Sudar D Malik J Knowles DW Hamann B PointCloudXplore: Visual analysis of 3D gene expression data using physical views and parallel coordinates. Data Visualization 2006 (Proceedings of the Eurographics/IEEE-VGTC Symposium on Visualization): May 8-10, 2006; Lisbon, Portugal Wellesley, Massachusetts: AK Peters Ltd Santos BC, Ertl T, Joy K 2006:203-210.
70. BDTNP Gene Expression Database http://bdtnp.lbl.gov/Fly-Net/ bioimaging.jsp
71. Driever W Nusslein-Volhard C A gradient of bicoid protein in Drosophila embryos. Cell 1988, 54:83-93. 3383244 10.1016/0092-8674(88)90182-1
72. Macdonald PM Struhl G A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 1986, 324:537-545. 2878369 10.1038/324537a0
73. Ma Y Niemitz EL Nambu PA Shan X Sackerson C Fujioka M Goto T Nambu JR Gene regulatory functions of Drosophila fish-hook, a high mobility group domain Sox protein. Mech Dev 1998, 73:169-182. 9622621 10.1016/ S0925-4773(98)00050-1
74. Nambu PA Nambu JR The Drosophila fish-hook gene encodes a HMG domain protein essential for segmentation and CNS development. Development 1996, 122:3467-3475. 8951062
75. Russell SR Sanchez-Soriano N Wright CR Ashburner M The Dichaete gene of Drosophila melanogaster encodes a SOX-domain protein required for embryonic segmentation. Development 1996, 122:3669-3676. 8951082
76. 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. 8217842 10.1016/ 0925-4773(93)90005-I
77. Vaessin H Brand M Jan LY Jan YN daughterless is essential for neuronal precursor differentiation but not for initiation of neuronal precursor formation in Drosophila embryo. Development 1994, 120:935-945. 7600969
78. Rushlow CA Han K Manley JL Levine M The graded distribution of the dorsal morphogen is initiated by selective nuclear transport in Drosophila. Cell 1989, 59:1165-1177. 2598265 10.1016/0092-8674(89)90772-1
79. Steward R Relocalization of the dorsal protein from the cytoplasm to the nucleus correlates with its function. Cell 1989, 59:1179-1188. 2598266 10.1016/0092-8674(89)90773-3
80. Carroll SB Scott MP Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell 1985, 43:47-57. 3000605 10.1016/ 0092-8674(85)90011-X
81. Carroll SB DiNardo S O'Farrell PH White RA Scott MP Temporal and spatial relationships between segmentation and homeotic gene expression in Drosophila embryos: Distributions of the fushi tarazu, engrailed, Sex combs reduced, Antennapedia, and Ultrabithorax proteins. Genes Dev 1988, 2:350-360. 2897943 10.1101/gad.2.3.350
82. Eldon ED Pirrotta V Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development 1991, 111:367-378. 1716553
83. Kraut R Levine M Spatial regulation of the gap gene giant during Drosophila development. Development 1991, 111:601-609. 1893877
84. Mohler J Eldon ED Pirrotta V A novel spatial transcription pattern associated with the segmentation gene, giant, of Drosophila. EMBO J 1989, 8:1539-1548. 400985 2504582
85. Langeland JA Attai SF Vorwerk K Carroll SB Positioning adjacent pair-rule stripes in the posterior Drosophila embryo. Development 1994, 120:2945-2955. 7607084
86. Bronner G Jackle H Control and function of terminal gap gene activity in the posterior pole region of the Drosophila embryo. Mech Dev 1991, 35:205-211. 1768621 10.1016/0925-4773(91)90019-3
87. Bronner G Jackle H Regulation and function of the terminal gap gene huckebein in the Drosophila blastoderm. Int J Dev Biol 1996, 40:157-165. 8735925
88. McDonald JA Doe CQ Establishing neuroblast-specific gene expression in the Drosophila CNS: Huckebein is activated by Wingless and Hedgehog and repressed by Engrailed and Gooseberry. Development 1997, 124:1079-1087. 9056782
89. Carroll SB Laughon A Thalley BS Expression, function, and regulation of the hairy segmentation protein in the Drosophila embryo. Genes Dev 1988, 2:883-890. 3209072 10.1101/gad.2.3.350
90. Ingham PW Howard KR Ish-Horowicz D Transcription pattern of the Drosophila segmentation gene hairy. Nature 1985, 318:439-445. 10.1038/ 318439a0
91. Pankratz MJ Hoch M Seifert E Jackle H Kruppel requirement for knirps enhancement reflects overlapping gap gene activities in the Drosophila embryo. Nature 1989, 341:337-340. 2797151 10.1038/341337a0
92. Pankratz MJ Seifert E Gerwin N Billi B Nauber U Jackle H Gradients of Kruppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the Drosophila embryo. Cell 1990, 61:309-317. 2331752 10.1016/0092-8674(90)90811-R
93. Gaul U Seifert E Schuh R Jackle H Analysis of Kruppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell 1987, 50:639-647. 3111719 10.1016/ 0092-8674(87)90037-7
94. Hoch M Schroder C Seifert E Jackle H cis-acting control elements for Kruppel expression in the Drosophila embryo. EMBO J 1990, 9:2587-2595. 552291 2114978
95. Das P Maduzia LL Wang H Finelli AL Cho SH Smith MM Padgett RW The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development 1998, 125:1519-1528. 9502733
96. Wisotzkey RG Mehra A Sutherland DJ Dobens LL Liu X Dohrmann C Attisano L Raftery LA Medea is a Drosophila Smad4 homolog that is differentially required to potentiate DPP responses. Development 1998, 125:1433-1445. 9502724
97. Bertuccioli C Fasano L Jun S Wang S Sheng G Desplan C In vivo requirement for the paired domain and homeodomain of the paired segmentation gene product. Development 1996, 122:2673-2685. 8787742
98. Butler BA Soong J Gergen JP The Drosophila segmentation gene runt has an extended cis-regulatory region that is required for vital expression at other stages of development. Mech Dev 1992, 39:17-28. 1336975 10.1016/ 0925-4773(92)90022-C
99. Kania MA Bonner AS Duffy JB Gergen JP The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev 1990, 4:1701-1713. 2249771 10.1101/gad.4.10.1701
100. Arora K Dai H Kazuko SG Jamal J O'Connor MB Letsou A Warrior R The Drosophila schnurri gene acts in the Dpp/TGF beta signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 1995, 81:781-790. 7774017 10.1016/0092-8674(95)90539-1
101. Grieder NC Nellen D Burke R Basler K Affolter M Schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 1995, 81:791-800. 7774018 10.1016/0092-8674(95)90540-5
102. Staehling-Hampton K Laughon AS Hoffmann FM A Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development 1995, 121:3393-3403. 7588072
103. Grossniklaus U Cadigan KM Gehring WJ Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 1994, 120:3155-3171. 7720559
104. Grossniklaus U Pearson RK Gehring WJ The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 1992, 6:1030-1051. 1317319 10.1101/gad.6.6.1030
105. Bhat KM van Beers EH Bhat P Sloppy paired acts as the downstream target of wingless in the Drosophila CNS and interaction between sloppy paired and gooseberry inhibits sloppy paired during neurogenesis. Development 2000, 127:655-665. 10631185
106. Reuter R Leptin M Interacting functions of snail, twist and huckebein during the early development of germ layers in Drosophila. Development 1994, 120:1137-1150. 8026325
107. Alberga A Boulay JL Kempe E Dennefeld C Haenlin M The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers. Development 1991, 111:983-992. 1879366
108. Ray RP Arora K Nusslein-Volhard C Gelbart WM The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 1991, 113:35-54. 1765005
109. Pignoni F Baldarelli RM Steingrimsson E Diaz RJ Patapoutian A Merriam JR Lengyel JA The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 1990, 62:151-163. 2364433 10.1016/0092-8674(90)90249-E
110. Thisse B Stoetzel C Gorostiza-Thisse C Perrin-Schmitt F Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 1988, 7:2175-2183. 454534 3416836