cis-Regulatory Logic of Short-Range Transcriptional Repression in Drosophila melanogaster

REFERENCES

• Arnosti, D. N. 2002. Design and function of transcriptional switches in Drosophila. Insect Biochem. Mol. Biol. 32:1257–1273.
   PubMedGoogle Scholar
• Arnosti, D. N. 2004. Multiple mechanisms of transcriptional repression in eukaryotes, p. 33–67. In M. Gossen, J. Kaufmann, and S. J. Triezenberg (ed.), Handbook of experimental pharmacology: transcription factors, vol. 166. Springer, Berlin, Germany.
   Google Scholar
• Arnosti, D. N., S. Barolo, M. Levine, and S. Small. 1996. The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 122:205–214.
   PubMedGoogle Scholar
• Arnosti, D. N., S. Gray, S. Barolo, J. Zhou, and M. Levine. 1996. The gap protein knirps mediates both quenching and direct repression in the Drosophila embryo. EMBO J. 15:3659–3666.
   PubMedGoogle Scholar
• Banerji, J., S. Rusconi, and W. Schaffner. 1981. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 2:299–308.
   Google Scholar
• Barolo, S., L. A. Carver, and J. W. Posakony. 2000. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. BioTechniques 29:726, 728, 730, 732.
   PubMed Web of Science ®Google Scholar
• Barolo, S., and M. Levine. 1997. hairy mediates dominant repression in the Drosophila embryo. EMBO J. 16:2883–2891.
   PubMed Web of Science ®Google Scholar
• Barolo, S., and J. W. Posakony. 2002. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev. 16:1167–1181.
   PubMedGoogle Scholar
• Beer, M. A., and S. Tavazoie. 2004. Predicting gene expression from sequence. Cell 117:185–198.
   PubMed Web of Science ®Google Scholar
• Bergman, C. M., and M. Kreitman. 2001. Analysis of conserved noncoding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences. Genome Res. 11:1335–1345.
   PubMedGoogle Scholar
• Berman, B. P., Y. Nibu, B. D. Pfeiffer, P. Tomancak, S. E. Celniker, M. Levine, G. M. Rubin, and M. B. Eisen. 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.
   PubMed Web of Science ®Google Scholar
• Brand, A. H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415.
   PubMed Web of Science ®Google Scholar
• Burns, L. G., and C. L. Peterson. 1997. The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo. Mol. Cell. Biol. 17:4811–4819.
   PubMedGoogle Scholar
• Capovilla, M., E. D. Eldon, and V. Pirrotta. 1992. The giant gene of Drosophila encodes a b-ZIP DNA-binding protein that regulates the expression of other segmentation gap genes. Development 114:99–112.
   PubMedGoogle Scholar
• Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2001. From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell Science, Malden, Mass.
   Google Scholar
• Chen, G., and A. J. Courey. 2000. Groucho/TLE family proteins and transcriptional repression. Gene 249:1–16.
   PubMed Web of Science ®Google Scholar
• Chen, G., J. Fernandez, S. Mische, and A. J. Courey. 1999. A functional interaction between the histone deacetylase Rpd3 and the corepressor Groucho in Drosophila development. Genes Dev. 13:2218–2230.
   PubMed Web of Science ®Google Scholar
• Chinnadurai, G. 2002. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol. Cell 2:213–224.
   Google Scholar
• Chinnadurai, G. 2003. CtBP family proteins: more than transcriptional corepressors. BioEssays 25:9–12.
   PubMed Web of Science ®Google Scholar
• Clyde, D. E., M. S. Corado, X. Wu, A. Paré, D. Papatsenko, and S. Small. 2003. A self-organizing system of repressor gradients establishes segmental complexity in Drosophila. Nature 426:849–853.
   PubMedGoogle Scholar
• Courey, A. J., and J. D. Huang. 1995. The establishment and interpretation of transcription factor gradients in the Drosophila embryo. Biochim. Biophys. Acta 1261:1–18.
   PubMedGoogle Scholar
• Davidson, E. H. 2001. Genomic regulatory systems: development and evolution. Academic Press, San Diego, Calif.
   Google Scholar
• Deckert, J., and K. Struhl. 2001. Histone acetylation at promoters is differentially affected by specific activators and repressors. Mol. Cell. Biol. 21:2726–2735.
   PubMed Web of Science ®Google Scholar
• Driever, W., and C. Nusslein-Volhard. 1988. A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93.
   PubMed Web of Science ®Google Scholar
• Driever, W., G. Thoma, and C. Nusslein-Volhard. 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.
   PubMed Web of Science ®Google Scholar
• Emberly, E., N. Rajewsky, and E. D. Siggia. 2003. Conservation of regulatory elements between two species of Drosophila. BMC Bioinformatics 4:57.
   PubMedGoogle Scholar
• Erives, A., and M. Levine. 2004. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. USA 101:3851–3856.
   PubMedGoogle Scholar
• Flores-Saaib, R. D., and A. J. Courey. 2000. Analysis of Groucho-histone interactions suggests mechanistic similarities between Groucho- and Tup1-mediated repression. Nucleic Acids Res. 28:4189–4196.
   PubMedGoogle Scholar
• Fujioka, M., Y. Emi-Sarker, G. L. Yusibova, T. Goto, and J. B. Jaynes. 1999. 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 126:2527–2538.
   PubMedGoogle Scholar
• Gaston, K., and P. S. Jayaraman. 2003. Transcriptional repression in eukaryotes: repressors and repression mechanisms. Cell Mol. Life Sci. 60:721–741.
   PubMedGoogle Scholar
• Gray, S., and M. Levine. 1996. Transcriptional repression in development. Curr. Opin. Cell Biol. 8:358–364.
   PubMedGoogle Scholar
• Gray, S., P. Szymanski, and M. Levine. 1994. Short-range repression permits multiple enhancers to function autonomously within a complex promoter. Genes Dev. 8:1829–1838.
   PubMedGoogle Scholar
• Hanes, S. D., G. Riddihough, D. Ish-Horowicz, and R. Brent. 1994. Specific DNA recognition and intersite spacing are critical for action of the Bicoid morphogen. Mol. Cell. Biol. 14:3364–3375.
   PubMedGoogle Scholar
• Hewitt, G. F., B. S. Strunk, C. Margulies, T. Priputin, X.-D. Wang, R. Amey, B. A. Pabst, D. Kosman, J. Reinitz, and D. N. Arnosti. 1999. Transcriptional repression by the Drosophila Giant protein: cis element positioning provides an alternative means of interpreting an effector gradient. Development 126:1201–1210.
   PubMedGoogle Scholar
• Janody, F., R. Sturny, V. Schaeffer, Y. Azou, and N. Dostatni. 2001. Two distinct domains of Bicoid mediate its transcriptional downregulation by the Torso pathway. Development 128:2281–2290.
   PubMedGoogle Scholar
• Jiang, J., and M. Levine. 1993. Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72:741–752.
   PubMedGoogle Scholar
• Johnston, M., and R. W. Davis. 1984. Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:1440–1448.
   PubMed Web of Science ®Google Scholar
• Keller, S. A., Y. Mao, P. Struffi, C. Margulies, C. E. Yurk, A. R. Anderson, R. L. Amey, S. Moore, J. M. Ebels, K. Foley, M. Corado, and D. N. Arnosti. 2000. dCtBP-dependent and -independent repression activities of the Drosophila Knirps protein. Mol. Cell. Biol. 20:7247–7258.
   PubMedGoogle Scholar
• Kim, T. K., and T. Maniatis. 1997. The mechanism of transcriptional synergy of an in vitro assembled interferon-beta enhanceosome. Mol. Cell 1:119–129.
   PubMed Web of Science ®Google Scholar
• Koh, S. S., A. Z. Ansari, M. Ptashne, and R. A. Young. 1998. An activator target in the RNA polymerase II holoenzyme. Mol. Cell 1:895–904.
   PubMed Web of Science ®Google Scholar
• Kosman, D., and S. Small. 1997. Concentration-dependent patterning by an ectopic expression domain of the Drosophila gap gene knirps. Development 124:1343–1354.
   PubMedGoogle Scholar
• Kulkarni, M. M., and D. N. Arnosti. 2005. Transcriptional enhancers: intelligent enhanceosomes or flexible billboards. J. Cell. Biochem. 94:890–898.
   PubMedGoogle Scholar
• Kulkarni, M. M., and D. N. Arnosti. 2003. Information display by transcriptional enhancers. Development 130:6569–6575.
   PubMedGoogle Scholar
• La Rosée A., T. Häder, H. Taubert, R. Rivera-Pomar, and H. Jäckle. 1997. Mechanism and Bicoid-dependent control of hairy stripe 7 expression in the posterior region of the Drosophila embryo. EMBO J. 16:4403–4411.
   PubMedGoogle Scholar
• Lenhard, B., A. Sandelin, L. Mendoza, P. Engstrom, N. Jareborg, and W. W. Wasserman. 2003. Identification of conserved regulatory elements by comparative genome analysis. J. Biol. 2:13.
   PubMedGoogle Scholar
• Loots, G. G., R. M. Locksley, C. M. Blankespoor, Z. E. Wang, W. Miller, E. M. Rubin, and K. A. Frazer. 2000. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 288:136–140.
   PubMed Web of Science ®Google Scholar
• Ludwig, M. Z., C. Bergman, N. H. Patel, and M. Kreitman. 2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403:564–567.
   PubMedGoogle Scholar
• Ludwig, M. Z., and M. Kreitman. 1995. Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol. Biol. Evol. 12:1002–1011.
   PubMedGoogle Scholar
• Ludwig, M. Z., N. H. Patel, and M. Kreitman. 1998. Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125:949–958.
   PubMedGoogle Scholar
• Majello, B., G. Napolitano, P. De Luca, and L. Lania. 1998. Recruitment of human TBP selectively activates RNA polymerase II TATA-dependent promoters. J. Biol. Chem. 273:16509–16516.
   PubMedGoogle Scholar
• Makeev, V. J., A. P. Lifanov, A. G. Nazina, and D. A. Papatsenko. 2003. Distance preferences in the arrangement of binding motifs and hierarchical levels in organization of transcription regulatory information. Nucleic Acids Res. 31:6016–6026.
   PubMedGoogle Scholar
• Markstein, M., and M. Levine. 2002. Decoding cis-regulatory DNAs in the Drosophila genome. Curr. Opin. Genet. Dev. 12:601–606.
   PubMedGoogle Scholar
• Markstein, M., P. Markstein, V. Markstein, and M. S. Levine. 2002. Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 99:763–768.
   PubMedGoogle Scholar
• Merika, M., and D. Thanos. 2001. Enhanceosomes. Curr. Opin. Genet. Dev. 11:205–208.
   PubMed Web of Science ®Google Scholar
• Munshi, N., T. Agalioti, S. Lomvardas, M. Merika, G. Chen, and D. Thanos. 2001. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 293:1133–1136.
   PubMed Web of Science ®Google Scholar
• Nibu, Y., K. Senger, and M. Levine. 2003. CtBP-independent repression in the Drosophila embryo. Mol. Cell. Biol. 23:3990–3999.
   PubMedGoogle Scholar
• Nibu, Y., H. Zhang, and M. Levine. 2001. Local action of long-range repressors in the Drosophila embryo. EMBO J. 20:2246–2253.
   PubMed Web of Science ®Google Scholar
• Pham, A. D., S. Muller, and F. Sauer. 1999. Mesoderm-determining transcription in Drosophila is alleviated by mutations in TAF(II)60 and TAF(II)110. Mech. Dev. 84:3–16.
   PubMedGoogle Scholar
• Piano, F., M. J. Parisi, R. Karess, and M. P. Kambysellis. 1999. Evidence for redundancy but not trans factor-cis element coevolution in the regulation of Drosophila Yp genes. Genetics 152:605–616.
   PubMedGoogle Scholar
• Rajewsky, N., M. Vergassola, U. Gaul, and E. D. Siggia. 2002. Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 3:30.
   PubMedGoogle Scholar
• Rebeiz, M., N. L. Reeves, and J. W. Posakony. 2002. SCORE: a computational approach to the identification of cis-regulatory modules and target genes in whole-genome sequence data. Site clustering over random expectation. Proc. Natl. Acad. Sci. USA 99:9888–9893.
   PubMedGoogle Scholar
• Rivera-Pomar, R., and H. Jãckle. 1996. From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends Genet. 12:478–483.
   PubMed Web of Science ®Google Scholar
• Ryu, J. R., and D. N. Arnosti. 2003. Functional similarity of Knirps CtBP-dependent and CtBP-independent transcriptional repressor activities. Nucleic Acids Res. 31:4654–4662.
   PubMedGoogle Scholar
• Ryu, J. R., L. K. Olson, and D. N. Arnosti. 2001. Cell-type specificity of short-range transcriptional repressors. Proc. Natl. Acad. Sci. USA 98:12960–12965.
   PubMedGoogle Scholar
• Sackerson, C., M. Fujioka, and T. Goto. 1999. The even-skipped locus is contained in a 16-kb chromatin domain. Dev. Biol. 211:39–52.
   PubMedGoogle Scholar
• Schroeder, M. D., M. Pearce, J. Fak, H. Fan, U. Unnerstall, E. Emberly, N. Rajewsky, E. D. Siggia, and U. Gaul. 2004. Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol. 2:E271.
   PubMedGoogle Scholar
• Seipel, K., O. Georgiev, and W. Schaffner. 1992. Different activation domains stimulate transcription from remote (′enhancer') and proximal (′promoter') positions. EMBO J. 11:4961–4968.
   PubMedGoogle Scholar
• Senger, K., G. W. Armstrong, W. J. Rowell, J. M. Kwan, M. Markstein, and M. Levine. 2004. Immunity regulatory DNAs share common organizational features in Drosophila. Mol. Cell 13:19–32.
   PubMed Web of Science ®Google Scholar
• Shi, Y., J.-I. Sawada, G. Sui, E. B. Affar, J. R. Whetstine, F. Lan, H. Ogawa, M. P.-S. Luke, Y. Nakatani, and Y. Shi. 2003. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422:735–738.
   PubMed Web of Science ®Google Scholar
• Small, S. 1997. Mechanisms of segmental pattern formation in Drosophila melanogaster, p. 137–178. In J. R. Collier (ed.), Reproductive biology of invertebrates, vol. 7. Progress in developmental biology. John Wiley & Sons, Hoboken, N.J.
   Google Scholar
• Small, S., D. N. Arnosti, and M. Levine. 1993. Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 119:762–772.
   PubMedGoogle Scholar
• Small, S., A. Blair, and M. Levine. 1992. Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. 11:4047–4057.
   PubMed Web of Science ®Google Scholar
• Small, S., A. Blair, and M. Levine. 1996. Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Dev. Biol. 175:314–324.
   PubMedGoogle Scholar
• Song, H., P. Hasson, Z. Paroush, and A. J. Courey. 2004. Groucho oligomerization is required for repression in vivo. Mol. Cell. Biol. 24:4341–4350.
   PubMedGoogle Scholar
• Struffi, P., M. Corado, M. Kulkarni, and D. N. Arnosti. 2004. Quantitative contributions of CtBP-dependent and -independent repression activities of Knirps. Development 131:2419–2429.
   PubMed Web of Science ®Google Scholar
• Struhl, G. 1989. Morphogen gradients and the control of body pattern in insect embryos. Ciba Found. Symp. 144:65–98.
   PubMedGoogle Scholar
• Strunk, B., P. Struffi, K. Wright, B. Pabst, J. Thomas, L. Qin, and D. N. Arnosti. 2001. Role of CtBP in transcriptional repression by the Drosophila giant protein. Dev. Biol. 239:229–240.
   PubMedGoogle Scholar
• Subramanian, T., and G. Chinnadurai. 2003. Association of class I histone deacetylases with transcriptional corepressor CtBP. FEBS Lett. 540:255–258.
   PubMed Web of Science ®Google Scholar
• Sutrias-Grau, M., and D. N. Arnosti. 2004. CtBP contributes quantitatively to Knirps repression activity in an NAD binding-dependent manner. Mol. Cell. Biol. 24:5953–5966.
   PubMed Web of Science ®Google Scholar
• Thanos, D., and T. Maniatis. 1995. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83:1091–1100.
   PubMed Web of Science ®Google Scholar
• Zhou, J., J. Zwicker, P. Szymanski, M. Levine, and R. Tjian. 1998. TAFII mutations disrupt Dorsal activation in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 95:13483–13488.
   PubMedGoogle Scholar