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. 1998 Jul;149(3):1393–1405. doi: 10.1093/genetics/149.3.1393

hobo Induced rearrangements in the yellow locus influence the insulation effect of the gypsy su(Hw)-binding region in Drosophila melanogaster.

M Gause 1, H Hovhannisyan 1, T Kan 1, S Kuhfittig 1, V Mogila 1, P Georgiev 1
PMCID: PMC1460218  PMID: 9649529

Abstract

The su(Hw) protein is responsible for the insulation mediated by the su(Hw)-binding region present in the gypsy retrotransposon. In the y2 mutant, su(Hw) protein partially inhibits yellow transcription by repressing the function of transcriptional enhancers located distally from the yellow promoter with respect to gypsy. y2 mutation derivatives have been induced by the insertion of two hobo copies on the both sides of gypsy: into the yellow intron and into the 5' regulatory region upstream of the wing and body enhancers. The hobo elements have the same structure and orientation, opposite to the direction of yellow transcription. In the sequence context, where two copies of hobo are separated by the su(Hw)-binding region, hobo-dependent rearrangements are frequently associated with duplications of the region between the hobo elements. Duplication of the su(Hw)-binding region strongly inhibits the insulation of the yellow promoter separated from the body and wing enhancers by gypsy. These results provide a better insight into mechanisms by which the su(Hw)-binding region affects the enhancer function.

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Selected References

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  1. Blackman R. K., Koehler M. M., Grimaila R., Gelbart W. M. Identification of a fully-functional hobo transposable element and its use for germ-line transformation of Drosophila. EMBO J. 1989 Jan;8(1):211–217. doi: 10.1002/j.1460-2075.1989.tb03366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cai H. N., Levine M. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J. 1997 Apr 1;16(7):1732–1741. doi: 10.1093/emboj/16.7.1732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cai H., Levine M. Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature. 1995 Aug 10;376(6540):533–536. doi: 10.1038/376533a0. [DOI] [PubMed] [Google Scholar]
  4. Calvi B. R., Hong T. J., Findley S. D., Gelbart W. M. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell. 1991 Aug 9;66(3):465–471. doi: 10.1016/0092-8674(81)90010-6. [DOI] [PubMed] [Google Scholar]
  5. Campuzano S., Carramolino L., Cabrera C. V., Ruíz-Gómez M., Villares R., Boronat A., Modolell J. Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell. 1985 Feb;40(2):327–338. doi: 10.1016/0092-8674(85)90147-3. [DOI] [PubMed] [Google Scholar]
  6. Chung J. H., Whiteley M., Felsenfeld G. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell. 1993 Aug 13;74(3):505–514. doi: 10.1016/0092-8674(93)80052-g. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Dorer D. R., Henikoff S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell. 1994 Jul 1;77(7):993–1002. doi: 10.1016/0092-8674(94)90439-1. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Eggleston W. B., Rim N. R., Lim J. K. Molecular characterization of hobo-mediated inversions in Drosophila melanogaster. Genetics. 1996 Oct;144(2):647–656. doi: 10.1093/genetics/144.2.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Georgiev P. G., Corces V. G. The su(Hw) protein bound to gypsy sequences in one chromosome can repress enhancer-promoter interactions in the paired gene located in the other homolog. Proc Natl Acad Sci U S A. 1995 May 23;92(11):5184–5188. doi: 10.1073/pnas.92.11.5184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Georgiev P. G., Elagin V. A., Buff E. M., Koliagin N. P. Svoistva supernestabil'nykh mutatsii v lokuse yellow Drosophila melanogaster. Genetika. 1992 Apr;28(4):98–107. [PubMed] [Google Scholar]
  13. Georgiev P. G., Gerasimova T. I. Novel genes influencing the expression of the yellow locus and mdg4 (gypsy) in Drosophila melanogaster. Mol Gen Genet. 1989 Dec;220(1):121–126. doi: 10.1007/BF00260865. [DOI] [PubMed] [Google Scholar]
  14. Georgiev P., Kozycina M. Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations. Genetics. 1996 Feb;142(2):425–436. doi: 10.1093/genetics/142.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gerasimova T. I., Corces V. G. Boundary and insulator elements in chromosomes. Curr Opin Genet Dev. 1996 Apr;6(2):185–192. doi: 10.1016/s0959-437x(96)80049-9. [DOI] [PubMed] [Google Scholar]
  16. Gerasimova T. I., Gdula D. A., Gerasimov D. V., Simonova O., Corces V. G. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell. 1995 Aug 25;82(4):587–597. doi: 10.1016/0092-8674(95)90031-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Geyer P. K., Corces V. G. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1987 Nov;1(9):996–1004. doi: 10.1101/gad.1.9.996. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Geyer P. K. The role of insulator elements in defining domains of gene expression. Curr Opin Genet Dev. 1997 Apr;7(2):242–248. doi: 10.1016/s0959-437x(97)80134-7. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Hatzopoulos P., Monastirioti M., Yannopoulos G., Louis C. The instability of the TE-like mutation Dp(2:2)GYL of Drosophila melanogaster is intimately associated with the hobo element. EMBO J. 1987 Oct;6(10):3091–3096. doi: 10.1002/j.1460-2075.1987.tb02617.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ho Y. T., Weber S. M., Lim J. K. Interacting hobo transposons in an inbred strain and interaction regulation in hybrids of Drosophila melanogaster. Genetics. 1993 Jul;134(3):895–908. doi: 10.1093/genetics/134.3.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Kellum R., Schedl P. A position-effect assay for boundaries of higher order chromosomal domains. Cell. 1991 Mar 8;64(5):941–950. doi: 10.1016/0092-8674(91)90318-s. [DOI] [PubMed] [Google Scholar]
  26. Laverty T. R., Lim J. K. Site-specific instability in Drosophila melanogaster: evidence for transposition of destabilizing element. Genetics. 1982 Jul-Aug;101(3-4):461–476. doi: 10.1093/genetics/101.3-4.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lim J. K. Intrachromosomal rearrangements mediated by hobo transposons in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9153–9157. doi: 10.1073/pnas.85.23.9153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lim J. K., Simmons M. J. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays. 1994 Apr;16(4):269–275. doi: 10.1002/bies.950160410. [DOI] [PubMed] [Google Scholar]
  29. Lim J. K. Site-specific instability in Drosophila melanogaster: the origin of the mutation and cytogenetic evidence for site specificity. Genetics. 1979 Nov;93(3):681–701. doi: 10.1093/genetics/93.3.681. [DOI] [PMC free article] [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. Martin M., Meng Y. B., Chia W. Regulatory elements involved in the tissue-specific expression of the yellow gene of Drosophila. Mol Gen Genet. 1989 Jul;218(1):118–126. doi: 10.1007/BF00330574. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Morcillo P., Rosen C., Baylies M. K., Dorsett D. Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila. Genes Dev. 1997 Oct 15;11(20):2729–2740. doi: 10.1101/gad.11.20.2729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Morcillo P., Rosen C., Dorsett D. Genes regulating the remote wing margin enhancer in the Drosophila cut locus. Genetics. 1996 Nov;144(3):1143–1154. doi: 10.1093/genetics/144.3.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. 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]
  39. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  40. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Scott K. S., Geyer P. K. Effects of the su(Hw) insulator protein on the expression of the divergently transcribed Drosophila yolk protein genes. EMBO J. 1995 Dec 15;14(24):6258–6267. doi: 10.1002/j.1460-2075.1995.tb00316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sheen F., Lim J. K., Simmons M. J. Genetic instability in Drosophila melanogaster mediated by hobo transposable elements. Genetics. 1993 Feb;133(2):315–334. doi: 10.1093/genetics/133.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. 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]
  46. Spradling A. C., Mahowald A. P. Identification and genetic localization of mRNAs from ovarian follicle cells of Drosophila melanogaster. Cell. 1979 Mar;16(3):589–598. doi: 10.1016/0092-8674(79)90032-1. [DOI] [PubMed] [Google Scholar]
  47. Streck R. D., Macgaffey J. E., Beckendorf S. K. The structure of hobo transposable elements and their insertion sites. EMBO J. 1986 Dec 20;5(13):3615–3623. doi: 10.1002/j.1460-2075.1986.tb04690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Vazquez J., Schedl P. Sequences required for enhancer blocking activity of scs are located within two nuclease-hypersensitive regions. EMBO J. 1994 Dec 15;13(24):5984–5993. doi: 10.1002/j.1460-2075.1994.tb06944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yannopoulos G., Stamatis N., Monastirioti M., Hatzopoulos P., Louis C. hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell. 1987 May 22;49(4):487–495. doi: 10.1016/0092-8674(87)90451-x. [DOI] [PubMed] [Google Scholar]
  50. Zhao K., Hart C. M., Laemmli U. K. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell. 1995 Jun 16;81(6):879–889. doi: 10.1016/0092-8674(95)90008-x. [DOI] [PubMed] [Google Scholar]

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