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. 1995 Jan;139(1):215–228. doi: 10.1093/genetics/139.1.215

The Suppressor of Hairy-Wing Protein Regulates the Tissue-Specific Expression of the Drosophila Gypsy Retrotransposon

P A Smith 1, V G Corces 1
PMCID: PMC1206320  PMID: 7705625

Abstract

The gypsy retrotransposon of Drosophila melanogaster causes mutations that show temporal and tissue-specific phenotypes. These mutant phenotypes can be reversed by mutations in su(Hw), a gene that also regulates the transcription of the gypsy element. Gypsy encodes a full-length 7.0-kb RNA that is expressed in the salivary gland precursors and fat body of the embryo, imaginal discs and fat body of larvae, and fat body and ovaries of adult females. The su(Hw)-binding region inserted upstream of the promoter of a lacZ reporter gene can induce β-galactosidase expression in a subset of the embryonic and larval tissues where gypsy is normally transcribed. This expression is dependent on the presence of a functional su(Hw) product, suggesting that this protein is a positive activator of gypsy transcription. Flies transformed with a construct in which the 5' LTR and leader sequences of gypsy are fused to lacZ show β-galactosidase expression in all tissues where gypsy is normally expressed, indicating that sequences other than the su(Hw)-binding site are required for proper spatial and temporal expression of gypsy. Mutations in the zinc fingers of su(Hw) affect its ability to bind DNA and to induce transcription of the lacZ reporter gene. Two other structural domains of su(Hw) also play an important role in transcriptional regulation of gypsy. Deletion of the amino-terminal acidic domain results in the loss of lacZ expression in larval fat body and adult ovaries, whereas mutations in the leucine zipper region result in an increase of lacZ expression in larval fat body and a decrease in adult ovaries. These effects might be the result of interactions of su(Hw) with activator and repressor proteins through the acidic and leucine zipper domains to produce the final pattern of tissue-specific expression of gypsy.

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Selected References

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  1. Abel T., Michelson A. M., Maniatis T. A Drosophila GATA family member that binds to Adh regulatory sequences is expressed in the developing fat body. Development. 1993 Nov;119(3):623–633. doi: 10.1242/dev.119.3.623. [DOI] [PubMed] [Google Scholar]
  2. Berger S. L., Cress W. D., Cress A., Triezenberg S. J., Guarente L. Selective inhibition of activated but not basal transcription by the acidic activation domain of VP16: evidence for transcriptional adaptors. Cell. 1990 Jun 29;61(7):1199–1208. doi: 10.1016/0092-8674(90)90684-7. [DOI] [PubMed] [Google Scholar]
  3. Corces V. G., Geyer P. K. Interactions of retrotransposons with the host genome: the case of the gypsy element of Drosophila. Trends Genet. 1991 Mar;7(3):86–90. doi: 10.1016/0168-9525(91)90277-W. [DOI] [PubMed] [Google Scholar]
  4. Dorsett D. Potentiation of a polyadenylylation site by a downstream protein-DNA interaction. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4373–4377. doi: 10.1073/pnas.87.11.4373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dorsett D., Viglianti G. A., Rutledge B. J., Meselson M. Alteration of hsp82 gene expression by the gypsy transposon and suppressor genes in Drosophila melanogaster. Genes Dev. 1989 Apr;3(4):454–468. doi: 10.1101/gad.3.4.454. [DOI] [PubMed] [Google Scholar]
  6. Ephrussi A., Dickinson L. K., Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 1991 Jul 12;66(1):37–50. doi: 10.1016/0092-8674(91)90137-n. [DOI] [PubMed] [Google Scholar]
  7. Geyer P. K., Corces V. G. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 1992 Oct;6(10):1865–1873. doi: 10.1101/gad.6.10.1865. [DOI] [PubMed] [Google Scholar]
  8. Geyer P. K., Green M. M., Corces V. G. Mutant gene phenotypes mediated by a Drosophila melanogaster retrotransposon require sequences homologous to mammalian enhancers. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8593–8597. doi: 10.1073/pnas.85.22.8593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Geyer P. K., Spana C., Corces V. G. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 1986 Oct;5(10):2657–2662. doi: 10.1002/j.1460-2075.1986.tb04548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gill G., Ptashne M. Negative effect of the transcriptional activator GAL4. Nature. 1988 Aug 25;334(6184):721–724. doi: 10.1038/334721a0. [DOI] [PubMed] [Google Scholar]
  11. Glaser R. L., Wolfner M. F., Lis J. T. Spatial and temporal pattern of hsp26 expression during normal development. EMBO J. 1986 Apr;5(4):747–754. doi: 10.1002/j.1460-2075.1986.tb04277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hardy C. F., Sussel L., Shore D. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 1992 May;6(5):801–814. doi: 10.1101/gad.6.5.801. [DOI] [PubMed] [Google Scholar]
  13. Harrison D. A., Gdula D. A., Coyne R. S., Corces V. G. A leucine zipper domain of the suppressor of Hairy-wing protein mediates its repressive effect on enhancer function. Genes Dev. 1993 Oct;7(10):1966–1978. doi: 10.1101/gad.7.10.1966. [DOI] [PubMed] [Google Scholar]
  14. Harrison D. A., Mortin M. A., Corces V. G. The RNA polymerase II 15-kilodalton subunit is essential for viability in Drosophila melanogaster. Mol Cell Biol. 1992 Mar;12(3):928–935. doi: 10.1128/mcb.12.3.928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Holdridge C., Dorsett D. Repression of hsp70 heat shock gene transcription by the suppressor of hairy-wing protein of Drosophila melanogaster. Mol Cell Biol. 1991 Apr;11(4):1894–1900. doi: 10.1128/mcb.11.4.1894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hope I. A., Mahadevan S., Struhl K. Structural and functional characterization of the short acidic transcriptional activation region of yeast GCN4 protein. Nature. 1988 Jun 16;333(6174):635–640. doi: 10.1038/333635a0. [DOI] [PubMed] [Google Scholar]
  18. Jack J., Dorsett D., Delotto Y., Liu S. Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer. Development. 1991 Nov;113(3):735–747. doi: 10.1242/dev.113.3.735. [DOI] [PubMed] [Google Scholar]
  19. Jarrell K. A., Meselson M. Drosophila retrotransposon promoter includes an essential sequence at the initiation site and requires a downstream sequence for full activity. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):102–104. doi: 10.1073/pnas.88.1.102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jiang J., Cai H., Zhou Q., Levine M. Conversion of a dorsal-dependent silencer into an enhancer: evidence for dorsal corepressors. EMBO J. 1993 Aug;12(8):3201–3209. doi: 10.1002/j.1460-2075.1993.tb05989.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jiang Y. W., Stillman D. J. Involvement of the SIN4 global transcriptional regulator in the chromatin structure of Saccharomyces cerevisiae. Mol Cell Biol. 1992 Oct;12(10):4503–4514. doi: 10.1128/mcb.12.10.4503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Keleher C. A., Goutte C., Johnson A. D. The yeast cell-type-specific repressor alpha 2 acts cooperatively with a non-cell-type-specific protein. Cell. 1988 Jun 17;53(6):927–936. doi: 10.1016/s0092-8674(88)90449-7. [DOI] [PubMed] [Google Scholar]
  24. Keleher C. A., Passmore S., Johnson A. D. Yeast repressor alpha 2 binds to its operator cooperatively with yeast protein Mcm1. Mol Cell Biol. 1989 Nov;9(11):5228–5230. doi: 10.1128/mcb.9.11.5228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kirov N., Zhelnin L., Shah J., Rushlow C. Conversion of a silencer into an enhancer: evidence for a co-repressor in dorsal-mediated repression in Drosophila. EMBO J. 1993 Aug;12(8):3193–3199. doi: 10.1002/j.1460-2075.1993.tb05988.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  28. Lankenau S., Corces V. G., Lankenau D. H. The Drosophila micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase. Mol Cell Biol. 1994 Mar;14(3):1764–1775. doi: 10.1128/mcb.14.3.1764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ma J., Ptashne M. Deletion analysis of GAL4 defines two transcriptional activating segments. Cell. 1987 Mar 13;48(5):847–853. doi: 10.1016/0092-8674(87)90081-x. [DOI] [PubMed] [Google Scholar]
  30. Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mazo A. M., Mizrokhi L. J., Karavanov A. A., Sedkov Y. A., Krichevskaja A. A., Ilyin Y. V. Suppression in Drosophila: su(Hw) and su(f) gene products interact with a region of gypsy (mdg4) regulating its transcriptional activity. EMBO J. 1989 Mar;8(3):903–911. doi: 10.1002/j.1460-2075.1989.tb03451.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mismer D., Rubin G. M. Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. Genetics. 1987 Aug;116(4):565–578. doi: 10.1093/genetics/116.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. O'Neil K. T., Hoess R. H., DeGrado W. F. Design of DNA-binding peptides based on the leucine zipper motif. Science. 1990 Aug 17;249(4970):774–778. doi: 10.1126/science.2389143. [DOI] [PubMed] [Google Scholar]
  34. Parkhurst S. M., Corces V. G. Forked, gypsys, and suppressors in Drosophila. Cell. 1985 Jun;41(2):429–437. doi: 10.1016/s0092-8674(85)80016-7. [DOI] [PubMed] [Google Scholar]
  35. Parkhurst S. M., Corces V. G. Interactions among the gypsy transposable element and the yellow and the suppressor of hairy-wing loci in Drosophila melanogaster. Mol Cell Biol. 1986 Jan;6(1):47–53. doi: 10.1128/mcb.6.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Parkhurst S. M., Harrison D. A., Remington M. P., Spana C., Kelley R. L., Coyne R. S., Corces V. G. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev. 1988 Oct;2(10):1205–1215. doi: 10.1101/gad.2.10.1205. [DOI] [PubMed] [Google Scholar]
  37. Peifer M., Bender W. The anterobithorax and bithorax mutations of the bithorax complex. EMBO J. 1986 Sep;5(9):2293–2303. doi: 10.1002/j.1460-2075.1986.tb04497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pirrotta V., Steller H., Bozzetti M. P. Multiple upstream regulatory elements control the expression of the Drosophila white gene. EMBO J. 1985 Dec 16;4(13A):3501–3508. doi: 10.1002/j.1460-2075.1985.tb04109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Roseman R. R., Pirrotta V., Geyer P. K. The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects. EMBO J. 1993 Feb;12(2):435–442. doi: 10.1002/j.1460-2075.1993.tb05675.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rosen B., Beddington R. S. Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions. Trends Genet. 1993 May;9(5):162–167. doi: 10.1016/0168-9525(93)90162-b. [DOI] [PubMed] [Google Scholar]
  41. Rutledge B. J., Mortin M. A., Schwarz E., Thierry-Mieg D., Meselson M. Genetic interactions of modifier genes and modifiable alleles in Drosophila melanogaster. Genetics. 1988 Jun;119(2):391–397. doi: 10.1093/genetics/119.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Smith P. A., Corces V. G. The suppressor of Hairy-wing binding region is required for gypsy mutagenesis. Mol Gen Genet. 1992 May;233(1-2):65–70. doi: 10.1007/BF00587562. [DOI] [PubMed] [Google Scholar]
  43. Spana C., Corces V. G. DNA bending is a determinant of binding specificity for a Drosophila zinc finger protein. Genes Dev. 1990 Sep;4(9):1505–1515. doi: 10.1101/gad.4.9.1505. [DOI] [PubMed] [Google Scholar]
  44. Spana C., Harrison D. A., Corces V. G. The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 1988 Nov;2(11):1414–1423. doi: 10.1101/gad.2.11.1414. [DOI] [PubMed] [Google Scholar]
  45. 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]

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