Abstract
Here we describe the identification of four binding sites of secretion enhancer binding protein 2 (SEBP2) in the regulatory region of the Drosophila salivary gland secretion protein gene 4 (Sgs-4) and show that despite these sites' correspondence with previously described Broad-Complex protein binding sites, SEBP2 is a Broad-Complex-independent factor encoded by the region-specific homeotic gene fork head (fkh). Two of the Fork head/SEBP2 binding sites are located within an ecdysone response unit which controls the tissue- and stage-specific responses of Sgs-4 to the steroid hormone 20-hydroxyecdysone. We demonstrate that these binding sites are relevant to the transcriptional activation of Sgs-4 and show that Fork head also binds to the Sgs-4 ecdysone response unit in vivo. Aside from being involved in the control of decisions during embryonic development, fkh thus participates directly in the control of specialized functions of differentiated cells at later stages of development.
Full text
PDF









Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andres A. J., Thummel C. S. Hormones, puffs and flies: the molecular control of metamorphosis by ecdysone. Trends Genet. 1992 Apr;8(4):132–138. doi: 10.1016/0168-9525(92)90371-A. [DOI] [PubMed] [Google Scholar]
- Ashburner M., Chihara C., Meltzer P., Richards G. Temporal control of puffing activity in polytene chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:655–662. doi: 10.1101/sqb.1974.038.01.070. [DOI] [PubMed] [Google Scholar]
- Bardwell V. J., Treisman R. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994 Jul 15;8(14):1664–1677. doi: 10.1101/gad.8.14.1664. [DOI] [PubMed] [Google Scholar]
- Belyaeva E. S., Aizenzon M. G., Semeshin V. F., Kiss I. I., Koczka K., Baritcheva E. M., Gorelova T. D., Zhimulev I. F. Cytogenetic analysis of the 2B3-4--2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma. 1980;81(2):281–306. doi: 10.1007/BF00285954. [DOI] [PubMed] [Google Scholar]
- Clark K. L., Halay E. D., Lai E., Burley S. K. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature. 1993 Jul 29;364(6436):412–420. doi: 10.1038/364412a0. [DOI] [PubMed] [Google Scholar]
- DiBello P. R., Withers D. A., Bayer C. A., Fristrom J. W., Guild G. M. The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics. 1991 Oct;129(2):385–397. doi: 10.1093/genetics/129.2.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Emery I. F., Bedian V., Guild G. M. Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development. 1994 Nov;120(11):3275–3287. doi: 10.1242/dev.120.11.3275. [DOI] [PubMed] [Google Scholar]
- Fletcher J. C., Thummel C. S. The Drosophila E74 gene is required for the proper stage- and tissue-specific transcription of ecdysone-regulated genes at the onset of metamorphosis. Development. 1995 May;121(5):1411–1421. doi: 10.1242/dev.121.5.1411. [DOI] [PubMed] [Google Scholar]
- Fletcher J. C., Thummel C. S. The ecdysone-inducible Broad-complex and E74 early genes interact to regulate target gene transcription and Drosophila metamorphosis. Genetics. 1995 Nov;141(3):1025–1035. doi: 10.1093/genetics/141.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guay P. S., Guild G. M. The ecdysone-induced puffing cascade in Drosophila salivary glands: a Broad-Complex early gene regulates intermolt and late gene transcription. Genetics. 1991 Sep;129(1):169–175. doi: 10.1093/genetics/129.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huet F., Ruiz C., Richards G. Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development. 1993 Jun;118(2):613–627. doi: 10.1242/dev.118.2.613. [DOI] [PubMed] [Google Scholar]
- Karim F. D., Guild G. M., Thummel C. S. The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development. 1993 Jul;118(3):977–988. doi: 10.1242/dev.118.3.977. [DOI] [PubMed] [Google Scholar]
- Karim F. D., Thummel C. S. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J. 1992 Nov;11(11):4083–4093. doi: 10.1002/j.1460-2075.1992.tb05501.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaufmann E., Hoch M., Jäckle H. The interaction of DNA with the DNA-binding domain encoded by the Drosophila gene fork head. Eur J Biochem. 1994 Jul 15;223(2):329–337. doi: 10.1111/j.1432-1033.1994.tb18998.x. [DOI] [PubMed] [Google Scholar]
- Kiss I., Beaton A. H., Tardiff J., Fristrom D., Fristrom J. W. Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics. 1988 Feb;118(2):247–259. doi: 10.1093/genetics/118.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koelle M. R., Talbot W. S., Segraves W. A., Bender M. T., Cherbas P., Hogness D. S. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 1991 Oct 4;67(1):59–77. doi: 10.1016/0092-8674(91)90572-g. [DOI] [PubMed] [Google Scholar]
- Krumm A., Roth G. E., Korge G. Transformation of salivary gland secretion protein gene Sgs-4 in Drosophila: stage- and tissue-specific regulation, dosage compensation, and position effect. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5055–5059. doi: 10.1073/pnas.82.15.5055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
- Kuzin B., Tillib S., Sedkov Y., Mizrokhi L., Mazo A. The Drosophila trithorax gene encodes a chromosomal protein and directly regulates the region-specific homeotic gene fork head. Genes Dev. 1994 Oct 15;8(20):2478–2490. doi: 10.1101/gad.8.20.2478. [DOI] [PubMed] [Google Scholar]
- Lai E., Clark K. L., Burley S. K., Darnell J. E., Jr Hepatocyte nuclear factor 3/fork head or "winged helix" proteins: a family of transcription factors of diverse biologic function. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10421–10423. doi: 10.1073/pnas.90.22.10421. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai E., Prezioso V. R., Smith E., Litvin O., Costa R. H., Darnell J. E., Jr HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev. 1990 Aug;4(8):1427–1436. doi: 10.1101/gad.4.8.1427. [DOI] [PubMed] [Google Scholar]
- Lai E., Prezioso V. R., Tao W. F., Chen W. S., Darnell J. E., Jr Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 1991 Mar;5(3):416–427. doi: 10.1101/gad.5.3.416. [DOI] [PubMed] [Google Scholar]
- Lehmann M. Drosophila Sgs genes: stage and tissue specificity of hormone responsiveness. Bioessays. 1996 Jan;18(1):47–54. doi: 10.1002/bies.950180110. [DOI] [PubMed] [Google Scholar]
- Lehmann M., Korge G. Ecdysone regulation of the Drosophila Sgs-4 gene is mediated by the synergistic action of ecdysone receptor and SEBP 3. EMBO J. 1995 Feb 15;14(4):716–726. doi: 10.1002/j.1460-2075.1995.tb07050.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mangelsdorf D. J., Thummel C., Beato M., Herrlich P., Schütz G., Umesono K., Blumberg B., Kastner P., Mark M., Chambon P. The nuclear receptor superfamily: the second decade. Cell. 1995 Dec 15;83(6):835–839. doi: 10.1016/0092-8674(95)90199-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morata G. Homeotic genes of Drosophila. Curr Opin Genet Dev. 1993 Aug;3(4):606–614. doi: 10.1016/0959-437x(93)90096-8. [DOI] [PubMed] [Google Scholar]
- Mougneau E., von Seggern D., Fowler T., Rosenblatt J., Jongens T., Rogers B., Gietzen D., Beckendorf S. K. A transcriptional switch between the Pig-1 and Sgs-4 genes of Drosophila melanogaster. Mol Cell Biol. 1993 Jan;13(1):184–195. doi: 10.1128/mcb.13.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pardue M. L., Gall J. G. Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol. 1975;10:1–16. doi: 10.1016/s0091-679x(08)60727-x. [DOI] [PubMed] [Google Scholar]
- Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saumweber H., Frasch M., Korge G. Two puff-specific proteins bind within the 2.5 kb upstream region of the Drosophila melanogaster Sgs-4 gene. Chromosoma. 1990 Apr;99(1):52–60. doi: 10.1007/BF01737289. [DOI] [PubMed] [Google Scholar]
- Talbot W. S., Swyryd E. A., Hogness D. S. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell. 1993 Jul 2;73(7):1323–1337. doi: 10.1016/0092-8674(93)90359-x. [DOI] [PubMed] [Google Scholar]
- Thomas H. E., Stunnenberg H. G., Stewart A. F. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature. 1993 Apr 1;362(6419):471–475. doi: 10.1038/362471a0. [DOI] [PubMed] [Google Scholar]
- Thummel C. S. Puffs and gene regulation--molecular insights into the Drosophila ecdysone regulatory hierarchy. Bioessays. 1990 Dec;12(12):561–568. doi: 10.1002/bies.950121202. [DOI] [PubMed] [Google Scholar]
- Tsai M. J., O'Malley B. W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem. 1994;63:451–486. doi: 10.1146/annurev.bi.63.070194.002315. [DOI] [PubMed] [Google Scholar]
- Weigel D., Jäckle H. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell. 1990 Nov 2;63(3):455–456. doi: 10.1016/0092-8674(90)90439-l. [DOI] [PubMed] [Google Scholar]
- Weigel D., Jürgens G., Küttner F., Seifert E., Jäckle H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell. 1989 May 19;57(4):645–658. doi: 10.1016/0092-8674(89)90133-5. [DOI] [PubMed] [Google Scholar]
- Yao T. P., Forman B. M., Jiang Z., Cherbas L., Chen J. D., McKeown M., Cherbas P., Evans R. M. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature. 1993 Dec 2;366(6454):476–479. doi: 10.1038/366476a0. [DOI] [PubMed] [Google Scholar]
- Yao T. P., Segraves W. A., Oro A. E., McKeown M., Evans R. M. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell. 1992 Oct 2;71(1):63–72. doi: 10.1016/0092-8674(92)90266-f. [DOI] [PubMed] [Google Scholar]
- von Kalm L., Crossgrove K., Von Seggern D., Guild G. M., Beckendorf S. K. The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J. 1994 Aug 1;13(15):3505–3516. doi: 10.1002/j.1460-2075.1994.tb06657.x. [DOI] [PMC free article] [PubMed] [Google Scholar]







