Identification of Genomic Sites That Bind the Drosophila Suppressor of Hairy-wing Insulator Protein

REFERENCES

• Bell, A. C., A. G. West, and G. Felsenfeld. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387–396.
   PubMed Web of Science ®Google 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
• Berman, B. P., B. D. Pfeiffer, T. R. Laverty, S. L. Salzberg, G. M. Rubin, M. B. Eisen, and S. E. Celniker. 2004. Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol. 5:R61.
   PubMedGoogle Scholar
• Biessmann, H. 1985. Molecular analysis of the yellow gene (y) region of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 82:7369–7373.
   PubMedGoogle Scholar
• Boutanaev, A. M., A. I. Kalmykova, Y. Y. Shevelyov, and D. I. Nurminsky. 2002. Large clusters of co-expressed genes in the Drosophila genome. Nature 420:666–669.
   PubMedGoogle Scholar
• Brasset, E., and C. Vaury. 2005. Insulators are fundamental components of the eukaryotic genomes. Heredity 94:571–576.
   PubMedGoogle Scholar
• Brown, R. S. 2005. Zinc finger proteins: getting a grip on RNA. Curr. Opin. Struct. Biol. 15:94–98.
   PubMed Web of Science ®Google Scholar
• Burcin, M., R. Arnold, M. Lutz, B. Kaiser, D. Runge, F. Lottspeich, G. N. Filippova, V. V. Lobanenkov, and R. Renkawitz. 1997. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol. Cell Biol. 17:1281–1288.
   PubMed Web of Science ®Google Scholar
• Byrd, K., and V. G. Corces. 2003. Visualization of chromatin domains created by the gypsy insulator of Drosophila. J. Cell Biol. 162:565–574.
   PubMedGoogle Scholar
• Cai, H., and M. Levine. 1995. Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature 376:533–536.
   PubMedGoogle Scholar
• Cai, H. N., and M. Levine. 1997. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J. 16:1732–1741.
   PubMed Web of Science ®Google Scholar
• Cantor, A. B., and S. H. Orkin. 2005. Coregulation of GATA factors by the friend of GATA (FOG) family of multitype zinc finger proteins. Semin. Cell Dev. Biol. 16:117–128.
   PubMed Web of Science ®Google Scholar
• Capelson, M., and V. G. Corces. 2004. Boundary elements and nuclear organization. Biol. Cell 96:617–629.
   PubMedGoogle Scholar
• Chen, J. L., K. L. Huisinga, M. M. Viering, S. A. Ou, C. T. Wu, and P. K. Geyer. 2002. Enhancer action in trans is permitted throughout the Drosophila genome. Proc. Natl. Acad. Sci. USA 99:3723–3728.
   PubMed Web of Science ®Google Scholar
• Chia, W., G. Howes, M. Martin, Y. B. Meng, K. Moses, and S. Tsubota. 1986. Molecular analysis of the yellow locus of Drosophila. EMBO J. 5:3597–3605.
   PubMedGoogle Scholar
• Cuvier, O., C. M. Hart, and U. K. Laemmli. 1998. Identification of a class of chromatin boundary elements. Mol. Cell. Biol. 18:7478–7486.
   PubMedGoogle Scholar
• Engel, N., and M. S. Bartolomei. 2003. Mechanisms of insulator function in gene regulation and genomic imprinting. Int. Rev. Cytol. 232:89–127.
   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
• Gaszner, M., J. Vazquez, and P. Schedl. 1999. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev. 13:2098–2107.
   PubMedGoogle Scholar
• Gause, M., P. Morcillo, and D. Dorsett. 2001. Insulation of enhancer-promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol. Cell. Biol. 21:4807–4817.
   PubMed Web of Science ®Google Scholar
• Georgiev, P., and M. Kozycina. 1996. Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations. Genetics 142:425–436.
   PubMedGoogle Scholar
• Georgiev, P. G., and T. I. Gerasimova. 1989. Novel genes influencing the expression of the yellow locus and mdg4 (gypsy) in Drosophila melanogaster. Mol. Gen. Genet. 220:121–126.
   PubMedGoogle Scholar
• Gerasimova, T. I., and V. G. Corces. 2001. Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu. Rev. Genet. 35:193–208.
   PubMedGoogle Scholar
• Geyer, P. K., and V. G. Corces. 1992. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 6:1865–1873.
   PubMedGoogle Scholar
• Geyer, P. K., and V. G. Corces. 1987. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1:996–1004.
   PubMedGoogle Scholar
• Geyer, P. K., C. Spana, and V. G. Corces. 1986. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 5:2657–2662.
   PubMed Web of Science ®Google Scholar
• Ghosh, D., T. I. Gerasimova, and V. G. Corces. 2001. Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function. EMBO J. 20:2518–2527.
   PubMedGoogle Scholar
• Golovnin, A., I. Birukova, O. Romanova, M. Silicheva, A. Parshikov, E. Savitskaya, V. Pirrotta, and P. Georgiev. 2003. An endogenous Su(Hw) insulator separates the yellow gene from the Achaete-scute gene complex in Drosophila. Development 130:3249–3258.
   PubMed Web of Science ®Google Scholar
• Golovnin, A., M. Gause, S. Georgieva, E. Gracheva, and P. Georgiev. 1999. The su(Hw) insulator can disrupt enhancer-promoter interactions when located more than 20 kilobases away from the Drosophila achaete-scute complex. Mol. Cell. Biol. 19:3443–3456.
   PubMedGoogle Scholar
• Granok, H., B. A. Leibovitch, C. D. Shaffer, and S. C. Elgin. 1995. Chromatin. Ga-ga over GAGA factor. Curr. Biol. 5:238–241.
   PubMed Web of Science ®Google Scholar
• Hagstrom, K., M. Muller, and P. Schedl. 1996. Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev. 10:3202–3215.
   PubMedGoogle Scholar
• Harrison, D. A., D. A. Gdula, R. S. Coyne, and V. G. Corces. 1993. A leucine zipper domain of the suppressor of Hairy-wing protein mediates its repressive effect on enhancer function. Genes Dev. 7:1966–1978.
   PubMedGoogle Scholar
• Harrison, D. A., P. K. Geyer, C. Spana, and V. G. Corces. 1989. The gypsy retrotransposon of Drosophila melanogaster: mechanisms of mutagenesis and interaction with the suppressor of Hairy-wing locus. Dev. Genet. 10:239–248.
   PubMedGoogle Scholar
• Harrison, D. A., M. A. Mortin, and V. G. Corces. 1992. The RNA polymerase II 15-kilodalton subunit is essential for viability in Drosophila melanogaster. Mol. Cell. Biol. 12:928–935.
   PubMedGoogle Scholar
• Hart, C. M., K. Zhao, and U. K. Laemmli. 1997. The scs′ boundary element: characterization of boundary element-associated factors. Mol. Cell. Biol. 17:999–1009.
   PubMedGoogle Scholar
• Holdridge, C., and D. Dorsett. 1991. Repression of hsp70 heat shock gene transcription by the suppressor of hairy-wing protein of Drosophila melanogaster. Mol. Cell. Biol. 11:1894–1900.
   PubMedGoogle Scholar
• Hoover, K. K., T. I. Gerasimova, A. J. Chien, and V. G. Corces. 1992. Dominant effects of suppressor of Hairy-wing mutations on gypsy-induced alleles of forked and cut in Drosophila melanogaster. Genetics 132:691–697.
   PubMedGoogle Scholar
• Hurst, L. D., C. Pal, and M. J. Lercher. 2004. The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5:299–310.
   PubMed Web of Science ®Google Scholar
• Kalmykova, A. I., D. I. Nurminsky, D. V. Ryzhov, and Y. Y. Shevelyov. 2005. Regulated chromatin domain comprising cluster of co-expressed genes in Drosophila melanogaster. Nucleic Acids Res. 33:1435–1444.
   PubMedGoogle Scholar
• Kim, C., B. F. Paulus, and M. S. Wold. 1994. Interactions of human replication protein A with oligonucleotides. Biochemistry 33:14197–14206.
   PubMed Web of Science ®Google Scholar
• Kuhn, E. J., and P. K. Geyer. 2003. Genomic insulators: connecting properties to mechanism. Curr. Opin. Cell Biol. 15:259–265.
   PubMedGoogle Scholar
• Kuhn, E. J., M. M. Viering, K. M. Rhodes, and P. K. Geyer. 2003. A test of insulator interactions in Drosophila. EMBO J. 22:2463–2471.
   PubMed Web of Science ®Google Scholar
• Lercher, M. J., A. O. Urrutia, and L. D. Hurst. 2002. Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat. Genet. 31:180–183.
   PubMedGoogle Scholar
• Lobanenkov, V. V., R. H. Nicolas, V. V. Adler, H. Paterson, E. M. Klenova, A. V. Polotskaja, and G. H. Goodwin. 1990. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5′-flanking sequence of the chicken c-myc gene. Oncogene 5:1743–1753.
   PubMed Web of Science ®Google Scholar
• Mallin, D. R., J. S. Myung, J. S. Patton, and P. K. Geyer. 1998. Polycomb group repression is blocked by the Drosophila suppressor of Hairy-wing [su(Hw)] insulator. Genetics 148:331–339.
   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
• Modolell, J., W. Bender, and M. Meselson. 1983. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. Proc. Natl. Acad. Sci. USA 80:1678–1682.
   PubMedGoogle Scholar
• Morris, J. R., J. L. Chen, P. K. Geyer, and C. T. Wu. 1998. Two modes of transvection: enhancer action in trans and bypass of a chromatin insulator in cis. Proc. Natl. Acad. Sci. USA 95:10740–10745.
   PubMedGoogle Scholar
• Mozer, B., R. Marlor, S. Parkhurst, and V. Corces. 1985. Characterization and developmental expression of a Drosophila ras oncogene. Mol. Cell. Biol. 5:885–889.
   PubMedGoogle Scholar
• Muravyova, E., A. Golovnin, E. Gracheva, A. Parshikov, T. Belenkaya, V. Pirrotta, and P. Georgiev. 2001. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 291:495–498.
   PubMedGoogle Scholar
• Nabirochkin, S., M. Ossokina, and T. Heidmann. 1998. A nuclear matrix/scaffold attachment region co-localizes with the gypsy retrotransposon insulator sequence. J. Biol. Chem. 273:2473–2479.
   PubMedGoogle Scholar
• Pai, C. Y., E. P. Lei, D. Ghosh, and V. G. Corces. 2004. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell 16:737–748.
   PubMedGoogle Scholar
• Parnell, T. J., M. M. Viering, A. Skjesol, C. Helou, E. J. Kuhn, and P. K. Geyer. 2003. An endogenous Suppressor of Hairy-wing insulator separates regulatory domains in Drosophila. Proc. Natl. Acad. Sci. USA 100:13436–13441.
   PubMedGoogle Scholar
• Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
   PubMed Web of Science ®Google Scholar
• Quitschke, W. W., M. J. Taheny, L. J. Fochtmann, and A. A. Vostrov. 2000. Differential effect of zinc finger deletions on the binding of CTCF to the promoter of the amyloid precursor protein gene. Nucleic Acids Res. 28:3370–3378.
   PubMed Web of Science ®Google Scholar
• Ramos, E., D. Ghosh, E. Baxter, and V. Corces. 2006. Genomic organization of gypsy chromatin insulators in Drosophila melanogaster. Genetics 172:2337–2349.
   PubMedGoogle Scholar
• Rebeiz, M., and J. W. Posakony. 2004. GenePalette: a universal software tool for genome sequence visualization and analysis. Dev. Biol. 271:431–438.
   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.
   PubMed Web of Science ®Google Scholar
• Recillas-Targa, F., M. J. Pikaart, B. Burgess-Beusse, A. C. Bell, M. D. Litt, A. G. West, M. Gaszner, and G. Felsenfeld. 2002. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc. Natl. Acad. Sci. USA 99:6883–6888.
   PubMed Web of Science ®Google Scholar
• Ren, X. Y., M. W. Fiers, W. J. Stiekema, and J. P. Nap. 2005. Local coexpression domains of two to four genes in the genome of Arabidopsis. Plant Physiol. 138:923–934.
   PubMedGoogle Scholar
• Roseman, R. R., E. A. Johnson, C. K. Rodesch, M. Bjerke, R. N. Nagoshi, and P. K. Geyer. 1995. A P element containing suppressor of hairy-wing binding regions has novel properties for mutagenesis in Drosophila melanogaster. Genetics 141:1061–1074.
   PubMedGoogle Scholar
• Savitskaya, E., L. Melnikova, M. Kostuchenko, E. Kravchenko, E. Pomerantseva, T. Boikova, D. Chetverina, A. Parshikov, P. Zobacheva, E. Gracheva, A. Galkin, and P. Georgiev. 2006. Study of long-distance functional interactions between Su(Hw) insulators that can regulate enhancer-promoter communication in Drosophila melanogaster. Mol. Cell. Biol. 26:754–761.
   PubMedGoogle Scholar
• Schweinsberg, S., K. Hagstrom, D. Gohl, P. Schedl, R. P. Kumar, R. Mishra, and F. Karch. 2004. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 168:1371–1384.
   PubMedGoogle Scholar
• Scott, K. C., A. D. Taubman, and P. K. Geyer. 1999. Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength. Genetics 153:787–798.
   PubMedGoogle Scholar
• Scott, K. S., and P. K. Geyer. 1995. Effects of the su(Hw) insulator protein on the expression of the divergently transcribed Drosophila yolk protein genes. EMBO J. 14:6258–6267.
   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
• Shen, B., J. Kim, and D. Dorsett. 1994. The enhancer-blocking suppressor of Hairy-wing zinc finger protein of Drosophila melanogaster alters DNA structure. Mol. Cell. Biol. 14:5645–5652.
   PubMedGoogle Scholar
• Sigrist, C. J., and V. Pirrotta. 1997. Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes. Genetics 147:209–221.
   PubMedGoogle Scholar
• Singh, G. B., J. A. Kramer, and S. A. Krawetz. 1997. Mathematical model to predict regions of chromatin attachment to the nuclear matrix. Nucleic Acids Res. 25:1419–1425.
   PubMedGoogle Scholar
• Spana, C., and V. G. Corces. 1990. DNA bending is a determinant of binding specificity for a Drosophila zinc finger protein. Genes Dev. 4:1505–1515.
   PubMedGoogle Scholar
• Spana, C., D. A. Harrison, and V. G. Corces. 1988. The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 2:1414–1423.
   PubMedGoogle Scholar
• Spellman, P. T., and G. M. Rubin. 2002. Evidence for large domains of similarly expressed genes in the Drosophila genome. J. Biol. 1:5.
   PubMedGoogle Scholar
• Vostrov, A. A., and W. W. Quitschke. 1997. The zinc finger protein CTCF binds to the APBbeta domain of the amyloid beta-protein precursor promoter. Evidence for a role in transcriptional activation. J. Biol. Chem. 272:33353–33359.
   PubMedGoogle Scholar
• West, A. G., M. Gaszner, and G. Felsenfeld. 2002. Insulators: many functions, many mechanisms. Genes Dev. 16:271–288.
   PubMed Web of Science ®Google Scholar
• West, A. G., S. Huang, M. Gaszner, M. D. Litt, and G. Felsenfeld. 2004. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16:453–463.
   PubMed Web of Science ®Google Scholar
• Yusufzai, T. M., and G. Felsenfeld. 2004. The 5′-HS4 chicken beta-globin insulator is a CTCF-dependent nuclear matrix-associated element. Proc. Natl. Acad. Sci. USA 101:8620–8624.
   PubMed Web of Science ®Google Scholar
• Yusufzai, T. M., H. Tagami, Y. Nakatani, and G. Felsenfeld. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13:291–298.
   PubMed Web of Science ®Google Scholar
• Zhao, H., and A. Dean. 2005. Organizing the genome: enhancers and insulators. Biochem. Cell Biol. 83:516–524.
   PubMedGoogle Scholar