Efficient and Specific Targeting of Polycomb Group Proteins Requires Cooperative Interaction between Grainyhead and Pleiohomeotic

REFERENCES

• Americo, J., M. Whiteley, J. L. Brown, M. Fujioka, J. B. Jaynes, and J. A. Kassis. 2002. A complex array of DNA-binding proteins required for pairing-sensitive silencing by a polycomb group response element from the Drosophila engrailed gene. Genetics 160:1561–1571.
   PubMedGoogle Scholar
• Armstrong, J. A., O. Papoulas, G. Daubresse, A. S. Sperling, J. T. Lis, M. P. Scott, and J. W. Tamkun. 2002. The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J. 21:5245–5254.
   PubMed Web of Science ®Google Scholar
• Atchison, L., A. Ghias, F. Wilkinson, N. Bonini, and M. L. Atchison. 2003. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J. 22:1347–1358.
   PubMed Web of Science ®Google Scholar
• Attardi, L. D., and R. Tjian. 1993. Drosophila tissue-specific transcription factor NTF-1 contains a novel isoleucine-rich activation motif. Genes Dev. 7:1341–1353.
   PubMed Web of Science ®Google Scholar
• Bray, S. J., B. Burke, N. H. Brown, and J. Hirsh. 1989. Embryonic expression pattern of a family of Drosophila proteins that interact with a central nervous system regulatory element. Genes Dev. 3:1130–1145.
   PubMed Web of Science ®Google Scholar
• Bray, S. J., and F. C. Kafatos. 1991. Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev. 5:1672–1683.
   PubMed Web of Science ®Google Scholar
• Brown, J. L., D. Mucci, M. Whiteley, M. L. Dirksen, and J. A. Kassis. 1998. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol. Cell 1:1057–1064.
   PubMed Web of Science ®Google Scholar
• Campbell, R. B., D. A. Sinclair, M. Couling, and H. W. Brock. 1995. Genetic interactions and dosage effects of Polycomb group genes of Drosophila. Mol. Gen. Genet. 246:291–300.
   PubMedGoogle Scholar
• Carey, M. 1998. The enhanceosome and transcriptional synergy. Cell 92:5–8.
   PubMed Web of Science ®Google Scholar
• Cavalli, G., and R. Paro. 1999. Epigenetic inheritance of active chromatin after removal of the main transactivator. Science 286:955–958.
   PubMed Web of Science ®Google Scholar
• Chen, J. L., L. D. Attardi, C. P. Verrijzer, K. Yokomori, and R. Tjian. 1994. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell 79:93–105.
   PubMed Web of Science ®Google Scholar
• Chiang, A., M. B. O'Connor, R. Paro, J. Simon, and W. Bender. 1995. Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development 121:1681–1689.
   PubMedGoogle Scholar
• Czermin, B., R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185–196.
   PubMed Web of Science ®Google Scholar
• Dejardin, J., and G. Cavalli. 2004. Chromatin inheritance upon Zeste-mediated Brahma recruitment at a minimal cellular memory module. EMBO J. 23:857–868.
   PubMedGoogle Scholar
• Dejardin, J., A. Rappailles, O. Cuvier, C. Grimaud, M. Decoville, D. Locker, and G. Cavalli. 2005. Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature 434:533–538.
   PubMed Web of Science ®Google Scholar
• del Mar Lorente, M., C. Marcos-Gutierrez, C. Perez, J. Schoorlemmer, A. Ramirez, T. Magin, and M. Vidal. 2000. Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice. Development 127:5093–5100.
   PubMedGoogle Scholar
• Dynlacht, B. D., L. D. Attardi, A. Admon, M. Freeman, and R. Tjian. 1989. Functional analysis of NTF-1, a developmentally regulated Drosophila transcription factor that binds neuronal cis elements. Genes Dev. 3:1677–1688.
   PubMed Web of Science ®Google Scholar
• Francis, N. J., A. J. Saurin, Z. Shao, and R. E. Kingston. 2001. Reconstitution of a functional core polycomb repressive complex. Mol. Cell 8:545–556.
   PubMed Web of Science ®Google Scholar
• Fritsch, C., D. Beuchle, and J. Muller. 2003. Molecular and genetic analysis of the Polycomb group gene Sex combs extra/Ring in Drosophila. Mech. Dev. 120:949–954.
   PubMedGoogle Scholar
• Furuyama, T., F. Tie, and P. J. Harte. 2003. Polycomb group proteins ESC and E(Z) are present in multiple distinct complexes that undergo dynamic changes during development. Genesis 35:114–124.
   PubMedGoogle Scholar
• Garcia, E., C. Marcos-Gutierrez, M. del Mar Lorente, J. C. Moreno, and M. Vidal. 1999. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1. EMBO J. 18:3404–3418.
   PubMed Web of Science ®Google Scholar
• Gorfinkiel, N., L. Fanti, T. Melgar, E. Garcia, S. Pimpinelli, I. Guerrero, and M. Vidal. 2004. The Drosophila Polycomb group gene Sex combs extra encodes the ortholog of mammalian Ring1 proteins. Mech. Dev. 121:449–462.
   PubMedGoogle Scholar
• Hagstrom, K., M. Muller, and P. Schedl. 1997. A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. Genetics 146:1365–1380.
   PubMedGoogle Scholar
• Hochschild, A., and M. Ptashne. 1986. Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix. Cell 44:681–687.
   PubMed Web of Science ®Google Scholar
• Hodgson, J. W., B. Argiropoulos, and H. W. Brock. 2001. Site-specific recognition of a 70-base-pair element containing d(GA)(n) repeats mediates bithoraxoid polycomb group response element-dependent silencing. Mol. Cell. Biol. 21:4528–4543.
   PubMedGoogle Scholar
• Hogga, I., and F. Karch. 2002. Transcription through the iab-7 cis-regulatory domain of the bithorax complex interferes with maintenance of Polycomb-mediated silencing. Development 129:4915–4922.
   PubMed Web of Science ®Google Scholar
• Horard, B., C. Tatout, S. Poux, and V. Pirrotta. 2000. Structure of a polycomb response element and in vitro binding of polycomb group complexes containing GAGA factor. Mol. Cell. Biol. 20:3187–3197.
   PubMedGoogle Scholar
• Huang, D.-H., Y.-L. Chang, C.-C. Yang, I.-C. Pan, and B. King. 2002. pipsqueak encodes a factor essential for sequence-specific targeting of a Polycomb group protein complex. Mol. Cell. Biol. 22:6261–6271.
   PubMedGoogle Scholar
• Kal, A. J., T. Mahmoudi, N. B. Zak, and C. P. Verrijzer. 2000. The Drosophila brahma complex is an essential coactivator for the trithorax group protein zeste. Genes Dev. 14:1058–1071.
   PubMedGoogle Scholar
• Kassis, J. A. 2002. Pairing-sensitive silencing, polycomb group response elements, and transposon homing in Drosophila. Adv. Genet. 46:421–438.
   PubMed Web of Science ®Google Scholar
• Kennison, J. A. 1995. The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29:289–303.
   PubMed Web of Science ®Google 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
• Lehmann, M., T. Siegmund, K. G. Lintermann, and G. Korge. 1998. The pipsqueak protein of Drosophila melanogaster binds to GAGA sequences through a novel DNA-binding domain. J. Biol. Chem. 273:28504–28509.
   PubMedGoogle Scholar
• Levine, S. S., A. Weiss, H. Erdjument-Bromage, Z. Shao, P. Tempst, and R. E. Kingston. 2002. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol. Cell. Biol. 22:6070–6078.
   PubMedGoogle Scholar
• Mahmoudi, T., L. M. Zuijderduijn, A. Mohd-Sarip, and C. P. Verrijzer. 2003. GAGA facilitates binding of Pleiohomeotic to a chromatinized Polycomb response element. Nucleic Acids Res. 31:4147–4156.
   PubMedGoogle Scholar
• Maniatis, T., J. V. Falvo, T. H. Kim, T. K. Kim, C. H. Lin, B. S. Parekh, and M. G. Wathelet. 1998. Structure and function of the interferon-beta enhanceosome. Cold Spring Harbor Symp. Quant. Biol. 63:609–620.
   PubMedGoogle Scholar
• Mihaly, J., I. Hogga, J. Gausz, H. Gyurkovics, and F. Karch. 1997. In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. Development 124:1809–1820.
   PubMedGoogle Scholar
• Mishra, K., V. S. Chopra, A. Srinivasan, and R. K. Mishra. 2003. Trl-GAGA directly interacts with lola like and both are part of the repressive complex of Polycomb group of genes. Mech. Dev. 120:681–689.
   PubMedGoogle Scholar
• Mishra, R. K., J. Mihaly, S. Barges, A. Spierer, F. Karch, K. Hagstrom, S. E. Schweinsberg, and P. Schedl. 2001. The iab-7 Polycomb response element maps to a nucleosome-free region of chromatin and requires both GAGA and Pleiohomeotic for silencing activity. Mol. Cell. Biol. 21:1311–1318.
   PubMedGoogle Scholar
• Mohd-Sarip, A., F. Venturini, G. E. Chalkley, and C. P. Verrijzer. 2002. Pleiohomeotic can link Polycomb to DNA and mediate transcriptional repression. Mol. Cell. Biol. 22:7473–7483.
   PubMedGoogle Scholar
• Mohrmann, L., K. Langenberg, J. Krijgsveld, A. J. Kal, A. J. Heck, and C. P. Verrijzer. 2004. Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol. Cell. Biol. 24:3077–3088.
   PubMedGoogle Scholar
• Mulholland, N. M., I. F. King, and R. E. Kingston. 2003. Regulation of Polycomb group complexes by the sequence-specific DNA binding proteins Zeste and GAGA. Genes Dev. 17:2741–2746.
   PubMed Web of Science ®Google Scholar
• Muller, J., C. M. Hart, N. J. Francis, M. L. Vargas, A. Sengupta, B. Wild, E. L. Miller, M. B. O'Connor, R. E. Kingston, and J. A. Simon. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197–208.
   PubMed Web of Science ®Google Scholar
• O'Brien, T., R. C. Wilkins, C. Giardina, and J. T. Lis. 1995. Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev. 9:1098–1110.
   PubMed Web of Science ®Google Scholar
• Orlando, V., E. P. Jane, V. Chinwalla, P. J. Harte, and R. Paro. 1998. Binding of trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis. EMBO J. 17:5141–5150.
   PubMed Web of Science ®Google Scholar
• Ringrose, L., M. Rehmsmeier, J. M. Dura, and R. Paro. 2003. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 5:759–771.
   PubMed Web of Science ®Google Scholar
• Romerio, F., M. N. Gabriel, and D. M. Margolis. 1997. Repression of human immunodeficiency virus type 1 through the novel cooperation of human factors YY1 and LSF. J. Virol. 71:9375–9382.
   PubMedGoogle Scholar
• Salvaing, J., A. Lopez, A. Boivin, J. S. Deutsch, and F. Peronnet. 2003. The Drosophila Corto protein interacts with Polycomb-group proteins and the GAGA factor. Nucleic Acids Res. 31:2873–2882.
   PubMedGoogle Scholar
• Saurin, A. J., Z. Shao, H. Erdjument-Bromage, P. Tempst, and R. E. Kingston. 2001. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412:655–660.
   PubMed Web of Science ®Google Scholar
• Schwendemann, A., and M. Lehmann. 2002. Pipsqueak and GAGA factor act in concert as partners at homeotic and many other loci. Proc. Natl. Acad. Sci. USA 99:12883–12888.
   PubMedGoogle Scholar
• Shao, Z., F. Raible, R. Mollaaghababa, J. R. Guyon, C. T. Wu, W. Bender, and R. E. Kingston. 1999. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98:37–46.
   PubMedGoogle Scholar
• Sipos, L., J. Mihaly, F. Karch, P. Schedl, J. Gausz, and H. Gyurkovics. 1998. Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. Genetics 149:1031–1050.
   PubMedGoogle Scholar
• Soto, M. C., T. B. Chou, and W. Bender. 1995. Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 140:231–243.
   PubMed Web of Science ®Google Scholar
• Srinivasan, L., and M. L. Atchison. 2004. YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev. 18:2596–2601.
   PubMedGoogle 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
• Tillib, S., S. Petruk, Y. Sedkov, A. Kuzin, M. Fujioka, T. Goto, and A. Mazo. 1999. Trithorax- and Polycomb-group response elements within an Ultrabithorax transcription maintenance unit consist of closely situated but separable sequences. Mol. Cell. Biol. 19:5189–5202.
   PubMed Web of Science ®Google Scholar
• Tuckfield, A., D. R. Clouston, T. M. Wilanowski, L. L. Zhao, J. M. Cunningham, and S. M. Jane. 2002. Binding of the RING polycomb proteins to specific target genes in complex with the grainyhead-like family of developmental transcription factors. Mol. Cell. Biol. 22:1936–1946.
   PubMed Web of Science ®Google Scholar
• Uv, A. E., E. J. Harrison, and S. J. Bray. 1997. Tissue-specific splicing and functions of the Drosophila transcription factor Grainyhead. Mol. Cell. Biol. 7:6727–6735.
   Google Scholar
• Uv, A. E., C. R. Thompson, and S. J. Bray. 1994. The Drosophila tissue-specific factor Grainyhead contains novel DNA-binding and dimerization domains which are conserved in the human protein CP2. Mol. Cell. Biol. 14:4020–4031.
   PubMedGoogle Scholar
• Volker, J. L., L. E. Rameh, Q. Zhu, J. DeCaprio, and U. Hansen. 1997. Mitogenic stimulation of resting T cells causes rapid phosphorylation of the transcription factor LSF and increased DNA-binding activity. Genes Dev. 11:1435–1446.
   PubMedGoogle Scholar
• Walter, J., C. A. Dever, and M. D. Biggin. 1994. Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev. 8:1678–1692.
   PubMedGoogle Scholar
• Wang, J. C., and G. N. Giaever. 1988. Action at a distance along a DNA. Science 240:300–304.
   PubMed Web of Science ®Google Scholar
• Wang, L., J. L. Brown, R. Cao, Y. Zhang, J. A. Kassis, and R. S. Jones. 2004. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 14:637–646.
   PubMed Web of Science ®Google Scholar