Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1993 Aug;134(4):1135–1144. doi: 10.1093/genetics/134.4.1135

Distance-Independent Inactivation of an Enhancer by the Suppressor of Hairy-Wing DNA-Binding Protein of Drosophila

D Dorsett 1
PMCID: PMC1205581  PMID: 8375652

Abstract

When the gypsy retrotransposon of Drosophila inserts between an enhancer and promoter it prevents the enhancer from activating transcription. Enhancers are blocked because the protein (SUHW) encoded by the suppressor of Hairy-wing [su(Hw)] gene binds to gypsy. For example, gypsy insertions in an 85 kilobase region between a wing margin-specific enhancer and the promoter in the cut gene cause a cut wing phenotype that is suppressed by su(Hw) mutations. A temperature-sensitive combination of mutant su(Hw) alleles was used to investigate the mechanism by which SUHW blocks the cut wing margin enhancer. By shifting from the nonpermissive to the permissive temperature and vice versa at various stages in development it was found that active SUHW is only required around pupariation when the wing margin enhancer is active to cause a cut wing phenotype. This was true whether gypsy was in the embryonic control region near the promoter, or in the late larval control region near the wing margin enhancer. These results indicate that SUHW must be active only when an enhancer is active to block the enhancer. Furthermore, the observations also indicate that enhancer-blocking by SUHW is reversible and that it occurs soon after binding of active SUHW to gypsy DNA. These results are consistent with models in which SUHW structurally interferes with enhancer-promoter interactions.

Full Text

The Full Text of this article is available as a PDF (4.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blochlinger K., Bodmer R., Jack J., Jan L. Y., Jan Y. N. Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature. 1988 Jun 16;333(6174):629–635. doi: 10.1038/333629a0. [DOI] [PubMed] [Google Scholar]
  2. Blochlinger K., Bodmer R., Jan L. Y., Jan Y. N. Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 1990 Aug;4(8):1322–1331. doi: 10.1101/gad.4.8.1322. [DOI] [PubMed] [Google Scholar]
  3. Bodmer R., Barbel S., Sheperd S., Jack J. W., Jan L. Y., Jan Y. N. Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell. 1987 Oct 23;51(2):293–307. doi: 10.1016/0092-8674(87)90156-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Geyer P. K., Green M. M., Corces V. G. Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila. EMBO J. 1990 Jul;9(7):2247–2256. doi: 10.1002/j.1460-2075.1990.tb07395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Hoover K. K., Gerasimova T. I., Chien A. J., Corces V. G. Dominant effects of suppressor of Hairy-wing mutations on gypsy-induced alleles of forked and cut in Drosophila melanogaster. Genetics. 1992 Nov;132(3):691–697. doi: 10.1093/genetics/132.3.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jack J. W. Molecular organization of the cut locus of Drosophila melanogaster. Cell. 1985 Oct;42(3):869–876. doi: 10.1016/0092-8674(85)90283-1. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Johnson T. K., Judd B. H. Analysis of the Cut Locus of DROSOPHILA MELANOGASTER. Genetics. 1979 Jun;92(2):485–502. doi: 10.1093/genetics/92.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Klug W. S., Bodenstein D., King R. C. Oogenesis in the suppressor of hairy-wing mutant of Drosophila melanogaster. I. Phenotypic characterization and transplantation experiments. J Exp Zool. 1968 Feb;167(2):151–156. doi: 10.1002/jez.1401670203. [DOI] [PubMed] [Google Scholar]
  13. Levis R., Bingham P. M., Rubin G. M. Physical map of the white locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Jan;79(2):564–568. doi: 10.1073/pnas.79.2.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Liu S., McLeod E., Jack J. Four distinct regulatory regions of the cut locus and their effect on cell type specification in Drosophila. Genetics. 1991 Jan;127(1):151–159. doi: 10.1093/genetics/127.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Modolell J., Bender W., Meselson M. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1678–1682. doi: 10.1073/pnas.80.6.1678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Müeller-Storm H. P., Sogo J. M., Schaffner W. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell. 1989 Aug 25;58(4):767–777. doi: 10.1016/0092-8674(89)90110-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Peifer M., Bender W. Sequences of the gypsy transposon of Drosophila necessary for its effects on adjacent genes. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9650–9654. doi: 10.1073/pnas.85.24.9650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES