Abstract
The Drosophila melanogaster decapentaplegic (dpp) gene encodes a transforming growth factor beta-related cell signaling molecule that plays a critical role in dorsal/ventral pattern formation. The dpp expression pattern in the Drosophila embryo is dynamic, consisting of three phases. Phase I, in which dpp is expressed in a broad dorsal domain, depends on elements in the dpp second intron that interact with the Dorsal transcription factor to repress transcription ventrally. In contrast, phases II and III, in which dpp is expressed first in broad longitudinal stripes (phase II) and subsequently in narrow longitudinal stripes (phase III), depend on multiple independent elements in the dpp 5'-flanking region. Several aspects of the normal dpp expression pattern appear to depend on the unique properties of the dpp core promoter. For example, this core promoter (extending from -22 to +6) is able to direct a phase II expression pattern in the absence of additional upstream or downstream regulatory elements. In addition, a ventral-specific enhancer in the dpp 5'-flanking region that binds the Dorsal factor activates the heterologous hsp70 core promoter but not the dpp core promoter. Thus, the dpp core promoter region may contribute to spatially regulated transcription both by interacting directly with spatially restricted activators and by modifying the activity of proteins bound to enhancer elements.
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- Barton M. C., Madani N., Emerson B. M. The erythroid protein cGATA-1 functions with a stage-specific factor to activate transcription of chromatin-assembled beta-globin genes. Genes Dev. 1993 Sep;7(9):1796–1809. doi: 10.1101/gad.7.9.1796. [DOI] [PubMed] [Google Scholar]
- Biggin M. D., Tjian R. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell. 1988 Jun 3;53(5):699–711. doi: 10.1016/0092-8674(88)90088-8. [DOI] [PubMed] [Google Scholar]
- Courey A. J., Huang J. D. The establishment and interpretation of transcription factor gradients in the Drosophila embryo. Biochim Biophys Acta. 1995 Mar 14;1261(1):1–18. doi: 10.1016/0167-4781(94)00234-t. [DOI] [PubMed] [Google Scholar]
- Eichbaum Q. G., Iyer R., Raveh D. P., Mathieu C., Ezekowitz R. A. Restriction of interferon gamma responsiveness and basal expression of the myeloid human Fc gamma R1b gene is mediated by a functional PU.1 site and a transcription initiator consensus. J Exp Med. 1994 Jun 1;179(6):1985–1996. doi: 10.1084/jem.179.6.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- England B. P., Admon A., Tjian R. Cloning of Drosophila transcription factor Adf-1 reveals homology to Myb oncoproteins. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):683–687. doi: 10.1073/pnas.89.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- England B. P., Heberlein U., Tjian R. Purified Drosophila transcription factor, Adh distal factor-1 (Adf-1), binds to sites in several Drosophila promoters and activates transcription. J Biol Chem. 1990 Mar 25;265(9):5086–5094. [PubMed] [Google Scholar]
- Ferguson E. L., Anderson K. V. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell. 1992 Oct 30;71(3):451–461. doi: 10.1016/0092-8674(92)90514-d. [DOI] [PubMed] [Google Scholar]
- Heberlein U., Tjian R. Temporal pattern of alcohol dehydrogenase gene transcription reproduced by Drosophila stage-specific embryonic extracts. Nature. 1988 Feb 4;331(6155):410–415. doi: 10.1038/331410a0. [DOI] [PubMed] [Google Scholar]
- Hiromi Y., Gehring W. J. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell. 1987 Sep 11;50(6):963–974. doi: 10.1016/0092-8674(87)90523-x. [DOI] [PubMed] [Google Scholar]
- Hoey T., Weinzierl R. O., Gill G., Chen J. L., Dynlacht B. D., Tjian R. Molecular cloning and functional analysis of Drosophila TAF110 reveal properties expected of coactivators. Cell. 1993 Jan 29;72(2):247–260. doi: 10.1016/0092-8674(93)90664-c. [DOI] [PubMed] [Google Scholar]
- Hoppler S., Bienz M. Specification of a single cell type by a Drosophila homeotic gene. Cell. 1994 Feb 25;76(4):689–702. doi: 10.1016/0092-8674(94)90508-8. [DOI] [PubMed] [Google Scholar]
- Huang J. D., Schwyter D. H., Shirokawa J. M., Courey A. J. The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression. Genes Dev. 1993 Apr;7(4):694–704. doi: 10.1101/gad.7.4.694. [DOI] [PubMed] [Google Scholar]
- Irish V. F., Gelbart W. M. The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1987 Oct;1(8):868–879. doi: 10.1101/gad.1.8.868. [DOI] [PubMed] [Google Scholar]
- Jackson P. D., Hoffmann F. M. Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression. Dev Dyn. 1994 Jan;199(1):28–44. doi: 10.1002/aja.1001990104. [DOI] [PubMed] [Google Scholar]
- Jiang J., Kosman D., Ip Y. T., Levine M. The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes Dev. 1991 Oct;5(10):1881–1891. doi: 10.1101/gad.5.10.1881. [DOI] [PubMed] [Google Scholar]
- Kaufmann J., Smale S. T. Direct recognition of initiator elements by a component of the transcription factor IID complex. Genes Dev. 1994 Apr 1;8(7):821–829. doi: 10.1101/gad.8.7.821. [DOI] [PubMed] [Google Scholar]
- Kwok R. P., Lundblad J. R., Chrivia J. C., Richards J. P., Bächinger H. P., Brennan R. G., Roberts S. G., Green M. R., Goodman R. H. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature. 1994 Jul 21;370(6486):223–226. doi: 10.1038/370223a0. [DOI] [PubMed] [Google Scholar]
- Liaw G. J. Improved protocol for directional multimerization of a DNA fragment. Biotechniques. 1994 Oct;17(4):668–670. [PubMed] [Google Scholar]
- Liaw G. J., Lengyel J. A. Control of tailless expression by bicoid, dorsal and synergistically interacting terminal system regulatory elements. Mech Dev. 1993 Jan;40(1-2):47–61. doi: 10.1016/0925-4773(93)90087-e. [DOI] [PubMed] [Google Scholar]
- Massagué J. Receptors for the TGF-beta family. Cell. 1992 Jun 26;69(7):1067–1070. doi: 10.1016/0092-8674(92)90627-o. [DOI] [PubMed] [Google Scholar]
- Massagué J. The transforming growth factor-beta family. Annu Rev Cell Biol. 1990;6:597–641. doi: 10.1146/annurev.cb.06.110190.003121. [DOI] [PubMed] [Google Scholar]
- Padgett R. W., St Johnston R. D., Gelbart W. M. A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature. 1987 Jan 1;325(6099):81–84. doi: 10.1038/325081a0. [DOI] [PubMed] [Google Scholar]
- Pan D. J., Huang J. D., Courey A. J. Functional analysis of the Drosophila twist promoter reveals a dorsal-binding ventral activator region. Genes Dev. 1991 Oct;5(10):1892–1901. doi: 10.1101/gad.5.10.1892. [DOI] [PubMed] [Google Scholar]
- Parvin J. D., Timmers H. T., Sharp P. A. Promoter specificity of basal transcription factors. Cell. 1992 Mar 20;68(6):1135–1144. doi: 10.1016/0092-8674(92)90084-p. [DOI] [PubMed] [Google Scholar]
- Pugh B. F., Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell. 1990 Jun 29;61(7):1187–1197. doi: 10.1016/0092-8674(90)90683-6. [DOI] [PubMed] [Google Scholar]
- Ray R. P., Arora K., Nüsslein-Volhard C., Gelbart W. M. The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development. 1991 Sep;113(1):35–54. doi: 10.1242/dev.113.1.35. [DOI] [PubMed] [Google Scholar]
- Soeller W. C., Poole S. J., Kornberg T. In vitro transcription of the Drosophila engrailed gene. Genes Dev. 1988 Jan;2(1):68–81. doi: 10.1101/gad.2.1.68. [DOI] [PubMed] [Google Scholar]
- St Johnston R. D., Gelbart W. M. Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 1987 Sep;6(9):2785–2791. doi: 10.1002/j.1460-2075.1987.tb02574.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- St Johnston R. D., Hoffmann F. M., Blackman R. K., Segal D., Grimaila R., Padgett R. W., Irick H. A., Gelbart W. M. Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 1990 Jul;4(7):1114–1127. doi: 10.1101/gad.4.7.1114. [DOI] [PubMed] [Google Scholar]
- Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
- Verrijzer C. P., Yokomori K., Chen J. L., Tjian R. Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science. 1994 May 13;264(5161):933–941. doi: 10.1126/science.8178153. [DOI] [PubMed] [Google Scholar]
- Wefald F. C., Devlin B. H., Williams R. S. Functional heterogeneity of mammalian TATA-box sequences revealed by interaction with a cell-specific enhancer. Nature. 1990 Mar 15;344(6263):260–262. doi: 10.1038/344260a0. [DOI] [PubMed] [Google Scholar]
- Zawel L., Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. doi: 10.1016/s0079-6603(08)60217-2. [DOI] [PubMed] [Google Scholar]
- Zenzie-Gregory B., Sheridan P., Jones K. A., Smale S. T. HIV-1 core promoter lacks a simple initiator element but contains a bipartite activator at the transcription start site. J Biol Chem. 1993 Jul 25;268(21):15823–15832. [PubMed] [Google Scholar]