Abstract
During late embryogenesis, the expression domains of homeotic genes are maintained by two groups of ubiquitously expressed regulators: the Polycomb repressors and the Trithorax activators. It is not known how the activities of the two maintenance systems are initially targeted to the correct genes. Zeste and GAGA are sequence-specific DNA-binding proteins previously shown to be Trithorax group activators of the homeotic gene Ultrabithorax (Ubx). We demonstrate that Zeste and GAGA DNA-binding sites at the proximal promoter are also required to maintain, but not to initiate, repression of Ubx. Furthermore, the repression mediated by Zeste DNA-binding site is abolished in zeste null embryos. These data imply that Zeste and probably GAGA mediate Polycomb repression. We present a model in which the dual transcriptional activities of Zeste and GAGA are an essential component of the mechanism that chooses which maintenance system is to be targeted to a given promoter.
References
31
Referenced
46
-
Bhat, K. M., Farkas, G., Karch, F., Gyurkovics, H., Gausz, J. and Schedl, P. (1996). The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development122, 1113-1124.
(
10.1242/dev.122.4.1113
) -
Bienz, M. and Muller, J. (1995). Transcriptional silencing of homeotic genes in Drosophila. BioEssays17, 775-784.
(
10.1002/bies.950170907
) -
Biggin, M. D. and Tjian, R. (1988). Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell53, 699-711.
(
10.1016/0092-8674(88)90088-8
) -
Cavalli, G. and Paro, R. (1999). Epigentic inheritance of active chromatin after removal of the main transactivator. Science286, 955-958.
(
10.1126/science.286.5441.955
) -
Chan, C. S., Rastelli, L. and Pirrotta, V. (1994). A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J.13, 2553-2564.
(
10.1002/j.1460-2075.1994.tb06545.x
) -
Farkas, G., Gausz, J., Galloni, M., Reuter, G., Gyurkovics, H. and Karch, F. (1994). The Trithorax-like gene encodes the Drosophila GAGA factor. Nature371, 806-808.
(
10.1038/371806a0
) -
Gildea, J. J., Lopez, R. and Shearn, A. (2000). A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics156, 645-663.
(
10.1093/genetics/156.2.645
) -
Goldberg, M. L., Colvin, R. A. and Mellin, A. F. (1989). The Drosophila zeste locus is nonessential. Genetics123, 145-155.
(
10.1093/genetics/123.1.145
) -
Hagstrom, K., Muller, M. and Schedl, P. (1997). A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. Genetics146, 1365-1380.
(
10.1093/genetics/146.4.1365
) -
Hashimoto, N., Brock, H. W., Nomura, M., Kyba, M., Hodgson, J., Fujita, Y., Takihara, Y., Shimada, K. and Higashinakagawa, T. (1998). RAE28, BMI1, and M33 are members of heterogeneous multimeric mammalian Polycomb group complexes. Biochem. Biophys. Res. Commun.245, 356-365.
(
10.1006/bbrc.1998.8438
) -
Horad, B., Tatout, C., Poux, S. and Pirrotta, V. (2000). Structure of a polycomb response element and in vitro binding of polycomb group complexes containing GAGA factor. Mol. Cell. Biol.20, 3187-3197.
(
10.1128/MCB.20.9.3187-3197.2000
) -
Irvine, K. D., Helfand, S. L. and Hogness, D. S. (1991). The large upstream control region of the Drosophila homeotic gene Ultrabithorax. Development111, 407-424.
(
10.1242/dev.111.2.407
) -
Kennison, J. A. (1995). The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet.29, 289-303.
(
10.1146/annurev.ge.29.120195.001445
) -
LaJeunesse, D. and Shearn, A. (1996). E(z): a polycomb group gene or a trithorax group gene? Development122, 2189-2197.
(
10.1242/dev.122.7.2189
) -
Laney, J. D. and Biggin, M. D. (1992). zeste, a nonessential gene, potently activates Ultrabithorax transcription in the Drosophila embryo. Genes Dev.6, 1531-1541.
(
10.1101/gad.6.8.1531
) -
Laney, J. D. and Biggin, M. D. (1996). Redundant control of Ultrabithorax by zeste involves functional levels of zeste protein binding at the Ultrabithorax promoter. Development122, 2303-2311.
(
10.1242/dev.122.7.2303
) -
Laney, J. D. and Biggin, M. D. (1997). Zeste-mediated activation by an enhancer is independent of cooperative DNA binding in vivo. Proc. Natl. Acad. Sci. USA94, 3602-3604.
(
10.1073/pnas.94.8.3602
) -
Orlando, V., Jane, E. P., Chinwalla, V., Harte, P. J. and Paro, R. (1998). Binding of Trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis. EMBO J.17, 5141-5150.
(
10.1093/emboj/17.17.5141
) -
Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. In Drosophila melanogaster: Practical Uses in Cell and Molecular Biology (ed. L. S. B. Goldstein and E. A. Friberg), pp. 445-487. San Diego, CA: Academic Press.
(
10.1016/S0091-679X(08)60927-9
) -
Pirrotta, V. (1998). Polycombing the genome: PcG, trxG and chromatin silencing. Cell93, 333-336.
(
10.1016/S0092-8674(00)81162-9
) -
Pirrotta, V., Bickel, S. and Mariani, C. (1988). Developmental expression of the Drosophila zeste gene and localization of zeste protein on polytene chromosomes. Genes Dev.2, 1839-1850.
(
10.1101/gad.2.12b.1839
) -
Poux, S., Kostic, C. and Pirrotta, V. (1996). Hunchback-independent silencing of late Ubx enhancers by a Polycomb Group Response Element. EMBO J.15, 4713-4722.
(
10.1002/j.1460-2075.1996.tb00848.x
) -
Saurin, A. J., Shao, Z., Erdjument-Bromage, H., Tempst, P. and Kingston, R. E. (2001). A Drosophila Polycomb complex includes Zeste and dTAFII proteins. Nature412, 655-660.
(
10.1038/35088096
) -
Simon, J., Chiang, A., Bender, W., Shimell, M. J. and O’Connor, M. (1993). Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol.158, 131-144.
(
10.1006/dbio.1993.1174
) -
Sinclair, D. A., Milne, T. A., Hodgson, J. W., Shellard, J., Salinas, C. A., Kyba, M., Randazzo, F. and Brock, H. W. (1998). The Additional sex combs gene of Drosophila encodes a chromatin protein that binds to shared and unique Polycomb group sites on polytene chromosomes. Development125, 1207-1216.
(
10.1242/dev.125.7.1207
) - Spradling, A. C. (1986). P element-mediated transformation. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 175-197. Washington, DC: IRL Press.
-
Strouboulis, J., Damjanovski, S., Vermaak, D., Meric, F. and Wolffe, A. P. (1999). Transcriptional repression be XPc1, a new polycomb homolog in Xenopus laevis embryos, is independent of histone deacetylase. Mol. Cell. Biol.19, 3958-3968.
(
10.1128/MCB.19.6.3958
) -
Strutt, H. and Paro, R. (1997). The polycomb protein complex of Drosophila melanogaster has different compositions at different target genes. Mol. Cell. Biol.17, 6773-6783.
(
10.1128/MCB.17.12.6773
) -
Tillib, S., Petruk, S., Sedkov, Y., Kuzin, A., Fujioka, M., Goto, T. and Mazo, A. (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.
(
10.1128/MCB.19.7.5189
) -
Wu, C. T., Jones, R. S., Lasko, P. F. and Gelbart, W. M. (1989). Homeosis and the interaction of zeste and white in Drosophila. Mol. Gen. Genet.218, 559-564.
(
10.1007/BF00332424
) -
Zhang, C. C. and Bienz, M. (1992). Segmental determination in Drosophila conferred by hunchback (hb), a repressor of the homeotic gene Ultrabithorax (Ubx). Proc. Natl. Acad. Sci. USA89, 7511-7515.
(
10.1073/pnas.89.16.7511
)
Dates
Type | When |
---|---|
Created | 4 years, 4 months ago (April 26, 2021, 1:03 a.m.) |
Deposited | 2 years, 8 months ago (Dec. 25, 2022, 6:59 a.m.) |
Indexed | 1 year, 2 months ago (June 9, 2024, 12:52 p.m.) |
Issued | 23 years, 5 months ago (March 15, 2002) |
Published | 23 years, 5 months ago (March 15, 2002) |
Published Print | 23 years, 5 months ago (March 15, 2002) |
@article{Hur_2002, title={Zeste maintains repression ofUbxtransgenes: support for a new model of Polycomb repression}, volume={129}, ISSN={0950-1991}, url={http://dx.doi.org/10.1242/dev.129.6.1339}, DOI={10.1242/dev.129.6.1339}, number={6}, journal={Development}, publisher={The Company of Biologists}, author={Hur, Man-Wook and Laney, Jeffrey D. and Jeon, Sang-Hack and Ali, Janann and Biggin, Mark D.}, year={2002}, month=mar, pages={1339–1343} }