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. 1987 Jan;6(1):207–214. doi: 10.1002/j.1460-2075.1987.tb04740.x

Developmental regulation by an enhancer from the Sgs-4 gene of Drosophila

Antony W Shermoen 1, Jill Jongens 1,1, Susan W Barnett 1, Kathleen Flynn 1, Steven K Beckendorf 1
PMCID: PMC553378  PMID: 16453749

Abstract

A cis acting regulatory region has previously been identified 300-500 bp upstream of the Drosophila glue protein gene, Sgs-4. The functional capabilities of this region have now been examined by fusing it to the Drosophila Adh gene and determining the pattern of expression from the fused construct after transformation. The results show that the Sgs-4 sequences between −150 and −568 are able to direct Adh expression in late third-instar salivary glands, the appropriate tissue and timing for Sgs-4 expression. In addition, the Sgs-4 sequence elevates Adh expression in the anterior midgut and fat body, despite the fact that Sgs-4 is not normally expressed there. All three regulatory activities, tissue specificity, timing and enhancement, show the positional flexibility of enhancer elements. In addition, the Sgs-4 and Adh regulatory elements combine to direct expression in novel spatial/temporal combinations in which neither would normally be expressed.

Keywords: tissue specific expression, P-element transformation, Adh regulation

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Selected References

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  1. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  2. Benyajati C., Place A. R., Wang N., Pentz E., Sofer W. Deletions at intervening sequence splice sites in the alcohol dehydrogenase gene of Drosophila. Nucleic Acids Res. 1982 Nov 25;10(22):7261–7272. doi: 10.1093/nar/10.22.7261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benyajati C., Spoerel N., Haymerle H., Ashburner M. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5' end in different developmental stages. Cell. 1983 May;33(1):125–133. doi: 10.1016/0092-8674(83)90341-0. [DOI] [PubMed] [Google Scholar]
  4. Boshart M., Weber F., Jahn G., Dorsch-Häsler K., Fleckenstein B., Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell. 1985 Jun;41(2):521–530. doi: 10.1016/s0092-8674(85)80025-8. [DOI] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  6. Burch J. B., Weintraub H. Temporal order of chromatin structural changes associated with activation of the major chicken vitellogenin gene. Cell. 1983 May;33(1):65–76. doi: 10.1016/0092-8674(83)90335-5. [DOI] [PubMed] [Google Scholar]
  7. Coté B., Bender W., Curtis D., Chovnick A. Molecular mapping of the rosy locus in Drosophila melanogaster. Genetics. 1986 Apr;112(4):769–783. doi: 10.1093/genetics/112.4.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dworniczak B., Seidel R., Pongs O. Puffing activities and binding of ecdysteroid to polytene chromosomes of Drosophila melanogaster. EMBO J. 1983;2(8):1323–1330. doi: 10.1002/j.1460-2075.1983.tb01587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garabedian M. J., Shepherd B. M., Wensink P. C. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell. 1986 Jun 20;45(6):859–867. doi: 10.1016/0092-8674(86)90560-x. [DOI] [PubMed] [Google Scholar]
  10. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  11. Goldberg D. A., Posakony J. W., Maniatis T. Correct developmental expression of a cloned alcohol dehydrogenase gene transduced into the Drosophila germ line. Cell. 1983 Aug;34(1):59–73. doi: 10.1016/0092-8674(83)90136-8. [DOI] [PubMed] [Google Scholar]
  12. Heberlein U., England B., Tjian R. Characterization of Drosophila transcription factors that activate the tandem promoters of the alcohol dehydrogenase gene. Cell. 1985 Jul;41(3):965–977. doi: 10.1016/s0092-8674(85)80077-5. [DOI] [PubMed] [Google Scholar]
  13. Herbomel P., Saragosti S., Blangy D., Yaniv M. Fine structure of the origin-proximal DNAase I-hypersensitive region in wild-type and EC mutant polyoma. Cell. 1981 Sep;25(3):651–658. doi: 10.1016/0092-8674(81)90172-0. [DOI] [PubMed] [Google Scholar]
  14. Herr W., Clarke J. The SV40 enhancer is composed of multiple functional elements that can compensate for one another. Cell. 1986 May 9;45(3):461–470. doi: 10.1016/0092-8674(86)90332-6. [DOI] [PubMed] [Google Scholar]
  15. Karess R. E., Rubin G. M. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. doi: 10.1016/0092-8674(84)90534-8. [DOI] [PubMed] [Google Scholar]
  16. Lewis N., Gibson J. Variation in amount of enzyme protein in natural populations. Biochem Genet. 1978 Apr;16(3-4):159–170. doi: 10.1007/BF00484075. [DOI] [PubMed] [Google Scholar]
  17. McGinnis W., Shermoen A. W., Beckendorf S. K. A transposable element inserted just 5' to a Drosophila glue protein gene alters gene expression and chromatin structure. Cell. 1983 Aug;34(1):75–84. doi: 10.1016/0092-8674(83)90137-x. [DOI] [PubMed] [Google Scholar]
  18. McGinnis W., Shermoen A. W., Heemskerk J., Beckendorf S. K. DNA sequence changes in an upstream DNase I-hypersensitive region are correlated with reduced gene expression. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1063–1067. doi: 10.1073/pnas.80.4.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McNabb S. L., Beckendorf S. K. Cis-acting sequences which regulate expression of the Sgs-4 glue protein gene of Drosophila. EMBO J. 1986 Sep;5(9):2331–2340. doi: 10.1002/j.1460-2075.1986.tb04501.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Muskavitch M. A., Hogness D. S. An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell. 1982 Jul;29(3):1041–1051. doi: 10.1016/0092-8674(82)90467-6. [DOI] [PubMed] [Google Scholar]
  21. Posakony J. W., Fischer J. A., Maniatis T. Identification of DNA sequences required for the regulation of Drosophila alcohol dehydrogenase gene expression. Cold Spring Harb Symp Quant Biol. 1985;50:515–520. doi: 10.1101/sqb.1985.050.01.063. [DOI] [PubMed] [Google Scholar]
  22. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  23. Saragosti S., Moyne G., Yaniv M. Absence of nucleosomes in a fraction of SV40 chromatin between the origin of replication and the region coding for the late leader RNA. Cell. 1980 May;20(1):65–73. doi: 10.1016/0092-8674(80)90235-4. [DOI] [PubMed] [Google Scholar]
  24. Shermoen A. W., Beckendorf S. K. A complex of interacting DNAase I-hypersensitive sites near the Drosophila glue protein gene, Sgs4. Cell. 1982 Jun;29(2):601–607. doi: 10.1016/0092-8674(82)90176-3. [DOI] [PubMed] [Google Scholar]
  25. Spradling A. C. The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell. 1981 Nov;27(1 Pt 2):193–201. doi: 10.1016/0092-8674(81)90373-1. [DOI] [PubMed] [Google Scholar]
  26. Wildeman A. G., Zenke M., Schatz C., Wintzerith M., Grundström T., Matthes H., Takahashi K., Chambon P. Specific protein binding to the simian virus 40 enhancer in vitro. Mol Cell Biol. 1986 Jun;6(6):2098–2105. doi: 10.1128/mcb.6.6.2098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wu C., Gilbert W. Tissue-specific exposure of chromatin structure at the 5' terminus of the rat preproinsulin II gene. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1577–1580. doi: 10.1073/pnas.78.3.1577. [DOI] [PMC free article] [PubMed] [Google Scholar]

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