Su(H)-mediated repression positions gene boundaries along the dorsal-ventral axis of drosophila embryos

Developmental Cell

Volumn 31, Issue 1, 2014, Pages 100-113

  Ozdemir, Anil ^a   Ma, Lijia ^b   White, Kevin P ^b   Stathopoulos, Angelike ^a  

^a California Institute of Technology HHMI   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SUPPRESSOR OF HAIRLESS; UNCLASSIFIED DRUG; DL (DORSAL) PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; REPRESSOR PROTEIN; SUPPRESSOR OF HAIRLESS PROTEIN, DROSOPHILA; ZELDA PROTEIN, DROSOPHILA;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE REPRESSION; NONHUMAN; PHENOTYPE; PROTEIN BINDING; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS;

ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NUCLEAR PROTEINS; PHOSPHOPROTEINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84908011221     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.08.005     Document Type: Article

References (58)

1. Ajuria L., Nieva C., Winkler C., Kuo D., Samper N., Andreu M.J., Helman A., González-Crespo S., Paroush Z., Courey A.J., Jiménez G. Capicua DNA-binding sites are general response elements for RTK signaling in Drosophila. Development 2011, 138:915-924.
2. Balaskas N., Ribeiro A., Panovska J., Dessaud E., Sasai N., Page K.M., Briscoe J., Ribes V. Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 2012, 148:273-284.
3. Bardin A.J., Schweisguth F. Bearded family members inhibit Neuralized-mediated endocytosis and signaling activity of Delta in Drosophila. Dev. Cell 2006, 10:245-255.
4. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 2007, 104:3312-3317.
5. Bray S.J. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 2006, 7:678-689.
6. Castro B., Barolo S., Bailey A.M., Posakony J.W. Lateral inhibition in proneural clusters:cis-regulatory logic and default repression by Suppressor of Hairless. Development 2005, 132:3333-3344.
7. Chen H., Xu Z., Mei C., Yu D., Small S. A system of repressor gradients spatially organizes the boundaries of Bicoid-dependent target genes. Cell 2012, 149:618-629.
8. Chou T.B., Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 1996, 144:1673-1679.
9. Couturier L., Vodovar N., Schweisguth F. Endocytosis by Numb breaks Notch symmetry at cytokinesis. Nat. Cell Biol. 2012, 14:131-139.
10. Cowden J., Levine M. The Snail repressor positions Notch signaling in the Drosophila embryo. Development 2002, 129:1785-1793.
11. Cowden J., Levine M. Ventral dominance governs sequential patterns of gene expression across the dorsal-ventral axis of the neuroectoderm in the Drosophila embryo. Dev. Biol. 2003, 262:335-349.
12. Crocker J., Erives A. A Schnurri/Mad/Medea complex attenuates the dorsal-twist gradient readout at vnd. Dev. Biol. 2013, 378:64-72.
13. Crocker J., Tamori Y., Erives A. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol. 2008, 6:e263.
14. De Renzis S., Yu J., Zinzen R., Wieschaus E. Dorsal-ventral pattern of Delta trafficking is established by a Snail-Tom-Neuralized pathway. Dev. Cell 2006, 10:257-264.
15. del Álamo D., Rouault H., Schweisguth F. Mechanism and significance ofcis-inhibition in Notch signalling. Curr. Biol. 2011, 21:R40-R47.
16. Dunipace L., Ozdemir A., Stathopoulos A. Complex interactions betweencis-regulatory modules in native conformation are critical for Drosophila snail expression. Development 2011, 138:4075-4084.
17. Dunipace L., Saunders A., Ashe H.L., Stathopoulos A. Autoregulatory feedback controls sequential action ofcis-regulatory modules at the brinker locus. Dev. Cell 2013, 26:536-543.
18. Erives A., Levine M. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. USA 2004, 101:3851-3856.
19. Furriols M., Bray S. A model Notch response element detects Suppressor of Hairless-dependent molecular switch. Curr. Biol. 2001, 11:60-64.
20. Garcia M., Stathopoulos A. Lateral gene expression in Drosophila early embryos is supported by Grainyhead-mediated activation and tiers of dorsally-localized repression. PLoS ONE 2011, 6:e29172.
21. Gonzalez-Crespo S., Levine M. Interactions between dorsal and helix-loop-helix proteins initiate the differentiation of the embryonic mesoderm and neuroectoderm in Drosophila. Genes Dev. 1993, 7:1703-1713.
22. Hong J.W., Hendrix D.A., Papatsenko D., Levine M.S. How the Dorsal gradient works: insights from postgenome technologies. Proc. Natl. Acad. Sci. USA 2008, 105:20072-20076.
23. Huang A.M., Rusch J., Levine M. An anteroposterior Dorsal gradient in the Drosophila embryo. Genes Dev. 1997, 11:1963-1973.
24. Ip Y.T., Park R.E., Kosman D., Bier E., Levine M. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes Dev. 1992, 6:1728-1739.
25. Ip Y.T., Park R.E., 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.
26. Janody F., Reischl J., Dostatni N. Persistence of Hunchback in the terminal region of the Drosophila blastoderm embryo impairs anterior development. Development 2000, 127:1573-1582.
27. Jiang J., Levine M. Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 1993, 72:741-752.
28. Johnson D.S., Mortazavi A., Myers R.M., Wold B. Genome-wide mapping of invivo protein-DNA interactions. Science 2007, 316:1497-1502.
29. Kasai Y., Nambu J.R., Lieberman P.M., Crews S.T. Dorsal-ventral patterning in Drosophila: DNA binding of snail protein to the single-minded gene. Proc. Natl. Acad. Sci. USA 1992, 89:3414-3418.
30. Kosman D., Ip Y.T., Levine M., Arora K. Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science 1991, 254:118-122.
31. Leptin M. twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 1991, 5:1568-1576.
32. Liang H.L., Nien C.Y., Liu H.Y., Metzstein M.M., Kirov N., Rushlow C. The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 2008, 456:400-403.
33. Liberman L.M., Stathopoulos A. Design flexibility incis-regulatory control of gene expression: synthetic and comparative evidence. Dev. Biol. 2009, 327:578-589.
34. Löhr U., Chung H.R., Beller M., Jäckle H. Antagonistic action of Bicoid and the repressor Capicua determines the spatial limits of Drosophila head gene expression domains. Proc. Natl. Acad. Sci. USA 2009, 106:21695-21700.
35. Maeda R.K., Karch F. Making connections: boundaries and insulators in Drosophila. Curr. Opin. Genet. Dev. 2007, 17:394-399.
36. Markstein M., Zinzen R., Markstein P., Yee K.P., Erives A., Stathopoulos A., Levine M. A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 2004, 131:2387-2394.
37. Mizutani C.M., Meyer N., Roelink H., Bier E. Threshold-dependent BMP-mediated repression: a model for a conserved mechanism that patterns the neuroectoderm. PLoS Biol. 2006, 4:e313.
38. Morel V., Schweisguth F. Repression by suppressor of hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes Dev. 2000, 14:377-388.
39. Moussian B., Roth S. Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr. Biol. 2005, 15:R887-R899.
40. Oosterveen T., Kurdija S., Alekseenko Z., Uhde C.W., Bergsland M., Sandberg M., Andersson E., Dias J.M., Muhr J., Ericson J. Mechanistic differences in the transcriptional interpretation of local and long-range Shh morphogen signaling. Dev. Cell 2012, 23:1006-1019.
41. Ozdemir A., Fisher-Aylor K.I., Pepke S., Samanta M., Dunipace L., McCue K., Zeng L., Ogawa N., Wold B.J., Stathopoulos A. High resolution mapping of Twist to DNA in Drosophila embryos: Efficient functional analysis and evolutionary conservation. Genome Res. 2011, 21:566-577.
42. Payankaulam S., Li L.M., Arnosti D.N. Transcriptional repression: conserved and evolved features. Curr. Biol. 2010, 20:R764-R771.
43. Perry M.W., Boettiger A.N., Bothma J.P., Levine M. Shadow enhancers foster robustness of Drosophila gastrulation. Curr. Biol. 2010, 20:1562-1567.
44. Ransick A., Davidson E.H. cis-regulatory processing of Notch signaling input to the sea urchin glial cells missing gene during mesoderm specification. Dev. Biol. 2006, 297:587-602.
45. Reeves G.T., Stathopoulos A. Graded Dorsal and differential gene regulation in the Drosophila embryo. Perspectives on Generation and Interpretation of Morphogen Gradients 2009, Cold Spring Harbor Laboratory Press, New York. J. Briscoe, P. Lawrence, J.-P. Vincent (Eds.).
46. Reeves G.T., Trisnadi N., Truong T.V., Nahmad M., Katz S., Stathopoulos A. Dorsal-ventral gene expression in the Drosophila embryo reflects the dynamics and precision of the dorsal nuclear gradient. Dev. Cell 2012, 22:544-557.
47. 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.
48. Rogers K.W., Schier A.F. Morphogen gradients: from generation to interpretation. Annu. Rev. Cell Dev. Biol. 2011, 27:377-407.
49. Rushlow C.A., Shvartsman S.Y. Temporal dynamics, spatial range, and transcriptional interpretation of the Dorsal morphogen gradient. Curr. Opin. Genet. Dev. 2012, 22:542-546.
50. 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.
51. Stathopoulos A., Levine M. Whole-genome analysis of Drosophila gastrulation. Curr. Opin. Genet. Dev. 2004, 14:477-484.
52. Stathopoulos A., Levine M. Genomic regulatory networks and animal development. Dev. Cell 2005, 9:449-462.
53. Stathopoulos A., Levine M. Localized repressors delineate the neurogenic ectoderm in the early Drosophila embryo. Dev. Biol. 2005, 280:482-493.
54. Struffi P., Corado M., Kaplan L., Yu D., Rushlow C., Small S. Combinatorial activation and concentration-dependent repression of the Drosophila even skipped stripe 3+7 enhancer. Development 2011, 138:4291-4299.
55. Struhl G., Greenwald I. Presenilin-mediated transmembrane cleavage is required for Notch signal transduction in Drosophila. PNAS 2001, 98:229-234.
56. Tapanes-Castillo A., Baylies M.K. Notch signaling patterns Drosophila mesodermal segments by regulating the bHLH transcription factor twist. Development 2004, 131:2359-2372.
57. Zinzen R.P., Senger K., Levine M., Papatsenko D. Computational models for neurogenic gene expression in the Drosophila embryo. Curr. Biol. 2006, 16:1358-1365.
58. Zinzen R.P., Girardot C., Gagneur J., Braun M., Furlong E.E. Combinatorial binding predicts spatio-temporalcis-regulatory activity. Nature 2009, 462:65-70.