Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 33, 2011, Pages 13570-13575

  Perry, Michael W ^a   Boettiger, Alistair N ^a   Levine, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cis regulation; Development; Robustness

Indexed keywords

ARTICLE; DROSOPHILA; EMBRYO; ENHANCER REGION; GAP GENE; GENE; GENE EXPRESSION; HUNCHBACK GENE; KNIRPS GENE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BODY PATTERNING; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; EMBRYONIC INDUCTION; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTPASE-ACTIVATING PROTEINS; TRANSCRIPTION FACTORS;

EID: 80052007879     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109873108     Document Type: Article

References (45)

1. Hong J-W, Hendrix D.A., Levine M.S. (2008) Shadow enhancers as a source of evolutionary novelty. Science 321:1314.
2. Frankel N., et al. (2010) Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466:490-493.
3. Perry M.W., Boettiger A.N., Bothma J.P., Levine M. (2010) Shadow enhancers foster robustness of Drosophila gastrulation. Curr Biol 20:1562-1567.
4. Waddington C.H. (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
5. Clyde D.E., et al. (2003) A self-organizing system of repressor gradients establishes segmental complexity in Drosophila. Nature 426:849-853. (Pubitemid 38056871)
6. Jaeger J., et al. (2004) Dynamic control of positional information in the early Drosophila embryo. Nature 430:368-371. (Pubitemid 38937746)
7. Small S., Blair A., Levine M. (1996) Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Dev Biol 175:314-324. (Pubitemid 26160759)
8. Small S., Blair A., Levine M. (1992) Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J 11:4047-4057.
9. Fujioka M., Emi-Sarker Y., Yusibova G.L., Goto T., Jaynes J.B. (1999) Analysis of an evenskipped rescue transgene reveals both composite and discrete neuronal and early blastoderm enhancers, and multi-stripe positioning by gap gene repressor gradients. Development 126:2527-2538. (Pubitemid 29299021)
10. Stathopoulos A., Levine M. (2005) Localized repressors delineate the neurogenic ectoderm in the early Drosophila embryo. Dev Biol 280:482-493. (Pubitemid 40692146)
11. Li X.Y., et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6:e27.
12. Schroeder M.D., et al. (2004) Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol 2:E271.
13. Driever W., Thoma G., Nüsslein-Volhard C. (1989) Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340:363-367. (Pubitemid 19191601)
14. Hoch M., Schröder C., Seifert E., Jäckle H. (1990) cis-acting control elements for Krüppel expression in the Drosophila embryo. EMBO J 9:2587-2595.
15. Rivera-Pomar R., Lu X., Perrimon N., Taubert H., Jäckle H. (1995) Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376:253-256.
16. Berman B.P., et al. (2002) Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci USA 99:757-762. (Pubitemid 34106583)
17. Ochoa-Espinosa A., et al. (2005) The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc Natl Acad Sci USA 102:4960-4965.
18. Margolis J.S., et al. (1995) Posterior stripe expression of hunchback is driven from two promoters by a common enhancer element. Development 121:3067-3077.
19. Struhl G. (1989) Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338:741-744.
20. Pankratz M.J., Busch M., Hoch M., Seifert E., Jäckle H. (1992) Spatial control of the gap gene knirps in the Drosophila embryo by posterior morphogen system. Science 255:986-989.
21. Hartmann B., Reichert H., Walldorf U. (2001) Interaction of gap genes in the Drosophila head: Tailless regulates expression of empty spiracles in early embryonic patterning and brain development. Mech Dev 109:161-172. (Pubitemid 33112029)
22. Häder T., et al. (2000) Receptor tyrosine kinase signaling regulates different modes of Groucho-dependent control of Dorsal. Curr Biol 10:51-54. (Pubitemid 30057416)
23. Venken K.J., He Y., Hoskins R.A., Bellen H.J. (2006) P[acman]: A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747-1751. (Pubitemid 44969080)
24. Venken K.J., et al. (2009) Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods 6:431-434.
25. Groth A.C., Fish M., Nusse R., Calos M.P. (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166:1775-1782. (Pubitemid 38621059)
26. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 104:3312-3317. (Pubitemid 46364156)
27. Boettiger A.N., Levine M.(2009) Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325:471-473.
28. Kim Y., et al. (2010) MAPK substrate competition integrates patterning signals in the Drosophila embryo. Curr Biol 20:446-451.
29. Struhl G., Johnston P., Lawrence P.A. (1992) Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 69:237-249.
30. Courey A.J., Jia S. (2001) Transcriptional repression: The long and the short of it. Genes Dev 15:2786-2796. (Pubitemid 33042049)
31. Goldstein R.E., Jiménez G., Cook O., Gur D., Paroush Z. (1999) Huckebein repressor activity in Drosophila terminal patterning is mediated by Groucho. Development 126:3747-3755. (Pubitemid 29440474)
32. Gray S., Levine M. (1996) Short-range transcriptional repressors mediate both quenching and direct repression within complex loci in Drosophila. Genes Dev 10:700-710.
33. Janody F., Reischl J., Dostatni N. (2000) Persistence of Hunchback in the terminal region of the Drosophila blastoderm embryo impairs anterior development. Development 127:1573-1582. (Pubitemid 30234915)
34. Kraut R., Levine M. (1991) Mutually repressive interactions between the gap genes giant and Krüppel define middle body regions of the Drosophila embryo. Development 111:611-621. (Pubitemid 21920442)
35. Manu, et al. (2009) Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation. PLoS Biol 7:e1000049.
36. Manu, et al. (2009) Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLOS Comput Biol 5:e1000303.
37. Yu D., Small S. (2008) Precise registration of gene expression boundaries by a repressive morphogen in Drosophila. Curr Biol 18:868-876.
38. Barolo S., Levine M. (1997) Hairy mediates dominant repression in the Drosophila embryo. EMBO J 16:2883-2891. (Pubitemid 27226224)
39. Winkler C.J., Ponce A., Courey A.J. (2010) Groucho-mediated repression may result from a histone deacetylase-dependent increase in nucleosome density. PLoS ONE 5:e10166.
40. Li L.M., Arnosti D.N. (2011) Long- and short-range transcriptional repressors induce distinct chromatin states on repressed genes. Curr Biol 21:406-412.
41. Papatsenko D. (2007) ClusterDraw web server: A tool to identify and visualize clusters of binding motifs for transcription factors. Bioinformatics 23:1032-1034.
42. Markstein M., et al. (2004) A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 131:2387-2394. (Pubitemid 38877646)
43. Lee E.C., et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
44. Liu P., Jenkins N.A., Copeland N.G. (2003) A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13:476-484. (Pubitemid 36395405)
45. Kosman D., et al. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305:846. (Pubitemid 39038414)