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. 1995 Oct;141(2):587–594. doi: 10.1093/genetics/141.2.587

A Role for the Kp Leucine Zipper in Regulating P Element Transposition in Drosophila Melanogaster

J D Andrews 1, G B Gloor 1
PMCID: PMC1206758  PMID: 8647395

Abstract

The KP element can repress P element mobility in Drosophila melanogaster. Three mutant KP elements were made that had either two amino acid substitutions or a single amino acid deletion in the putative leucine zipper domain found in the KP polypeptide. Each KP element was expressed from the actin 5C proximal promoter. The wild-type control construct strongly repressed P element mobility, measured by the GD sterility and sn(w) mutability assays, in a position-independent manner. The single amino acid deletion mutant failed to repress P mobility regardless of its insertion site, while repression of P element mobility by the double amino acid substitution mutants was position dependent. The results show that the leucine zipper of the KP polypeptide is important for P element regulation. This supports the multimer-poisoning model of P element repression, because leucine zipper motifs are involved in protein-protein interactions.

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Selected References

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

  1. Bainton R., Gamas P., Craig N. L. Tn7 transposition in vitro proceeds through an excised transposon intermediate generated by staggered breaks in DNA. Cell. 1991 May 31;65(5):805–816. doi: 10.1016/0092-8674(91)90388-f. [DOI] [PubMed] [Google Scholar]
  2. Busch S. J., Sassone-Corsi P. Dimers, leucine zippers and DNA-binding domains. Trends Genet. 1990 Feb;6(2):36–40. doi: 10.1016/0168-9525(90)90071-d. [DOI] [PubMed] [Google Scholar]
  3. Chung Y. T., Keller E. B. Regulatory elements mediating transcription from the Drosophila melanogaster actin 5C proximal promoter. Mol Cell Biol. 1990 Jan;10(1):206–216. doi: 10.1128/mcb.10.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cohen C., Parry D. A. Alpha-helical coiled coils: more facts and better predictions. Science. 1994 Jan 28;263(5146):488–489. doi: 10.1126/science.8290957. [DOI] [PubMed] [Google Scholar]
  5. Engels W. R. Extrachromosomal control of mutability in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Aug;76(8):4011–4015. doi: 10.1073/pnas.76.8.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
  7. Engels W. R. The estimation of mutation rates when premeiotic events are involved. Environ Mutagen. 1979;1(1):37–43. doi: 10.1002/em.2860010110. [DOI] [PubMed] [Google Scholar]
  8. Gloor G. B., Nassif N. A., Johnson-Schlitz D. M., Preston C. R., Engels W. R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. doi: 10.1126/science.1653452. [DOI] [PubMed] [Google Scholar]
  9. Gloor G. B., Preston C. R., Johnson-Schlitz D. M., Nassif N. A., Phillis R. W., Benz W. K., Robertson H. M., Engels W. R. Type I repressors of P element mobility. Genetics. 1993 Sep;135(1):81–95. doi: 10.1093/genetics/135.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hagemann S., Miller W. J., Pinsker W. Identification of a complete P-element in the genome of Drosophila bifasciata. Nucleic Acids Res. 1992 Feb 11;20(3):409–413. doi: 10.1093/nar/20.3.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Haniford D. B., Chelouche A. R., Kleckner N. A specific class of IS10 transposase mutants are blocked for target site interactions and promote formation of an excised transposon fragment. Cell. 1989 Oct 20;59(2):385–394. doi: 10.1016/0092-8674(89)90299-7. [DOI] [PubMed] [Google Scholar]
  12. Jackson M. S., Black D. M., Dover G. A. Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics. 1988 Dec;120(4):1003–1013. doi: 10.1093/genetics/120.4.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Kaufman P. D., Doll R. F., Rio D. C. Drosophila P element transposase recognizes internal P element DNA sequences. Cell. 1989 Oct 20;59(2):359–371. doi: 10.1016/0092-8674(89)90297-3. [DOI] [PubMed] [Google Scholar]
  15. Kaufman P. D., Rio D. C. Drosophila P-element transposase is a transcriptional repressor in vitro. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2613–2617. doi: 10.1073/pnas.88.7.2613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaufman P. D., Rio D. C. P element transposition in vitro proceeds by a cut-and-paste mechanism and uses GTP as a cofactor. Cell. 1992 Apr 3;69(1):27–39. doi: 10.1016/0092-8674(92)90116-t. [DOI] [PubMed] [Google Scholar]
  17. Kidwell M. G., Kidwell J. F., Sved J. A. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics. 1977 Aug;86(4):813–833. doi: 10.1093/genetics/86.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kneller D. G., Cohen F. E., Langridge R. Improvements in protein secondary structure prediction by an enhanced neural network. J Mol Biol. 1990 Jul 5;214(1):171–182. doi: 10.1016/0022-2836(90)90154-E. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  21. Laski F. A., Rubin G. M. Analysis of the cis-acting requirements for germ-line-specific splicing of the P-element ORF2-ORF3 intron. Genes Dev. 1989 May;3(5):720–728. doi: 10.1101/gad.3.5.720. [DOI] [PubMed] [Google Scholar]
  22. Lavoie B. D., Chan B. S., Allison R. G., Chaconas G. Structural aspects of a higher order nucleoprotein complex: induction of an altered DNA structure at the Mu-host junction of the Mu type 1 transpososome. EMBO J. 1991 Oct;10(10):3051–3059. doi: 10.1002/j.1460-2075.1991.tb07856.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lemaitre B., Coen D. P regulatory products repress in vivo the P promoter activity in P-lacZ fusion genes. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4419–4423. doi: 10.1073/pnas.88.10.4419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lemaitre B., Ronsseray S., Coen D. Maternal repression of the P element promoter in the germline of Drosophila melanogaster: a model for the P cytotype. Genetics. 1993 Sep;135(1):149–160. doi: 10.1093/genetics/135.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Misra S., Rio D. C. Cytotype control of Drosophila P element transposition: the 66 kd protein is a repressor of transposase activity. Cell. 1990 Jul 27;62(2):269–284. doi: 10.1016/0092-8674(90)90365-l. [DOI] [PubMed] [Google Scholar]
  26. Nassif N., Penney J., Pal S., Engels W. R., Gloor G. B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol. 1994 Mar;14(3):1613–1625. doi: 10.1128/mcb.14.3.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nitasaka E., Mukai T., Yamazaki T. Repressor of P elements in Drosophila melanogaster: Cytotype determination by a defective P element carrying only open reading frames 0 through 2. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7605–7608. doi: 10.1073/pnas.84.21.7605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. O'Hare K., Driver A., McGrath S., Johnson-Schiltz D. M. Distribution and structure of cloned P elements from the Drosophila melanogaster P strain pi 2. Genet Res. 1992 Aug;60(1):33–41. doi: 10.1017/s0016672300030640. [DOI] [PubMed] [Google Scholar]
  29. O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
  30. Rasmusson K. E., Raymond J. D., Simmons M. J. Repression of hybrid dysgenesis in Drosophila melanogaster by individual naturally occurring P elements. Genetics. 1993 Mar;133(3):605–622. doi: 10.1093/genetics/133.3.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rio D. C., Laski F. A., Rubin G. M. Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell. 1986 Jan 17;44(1):21–32. doi: 10.1016/0092-8674(86)90481-2. [DOI] [PubMed] [Google Scholar]
  32. Rio D. C. Molecular mechanisms regulating Drosophila P element transposition. Annu Rev Genet. 1990;24:543–578. doi: 10.1146/annurev.ge.24.120190.002551. [DOI] [PubMed] [Google Scholar]
  33. Rio D. C. Regulation of Drosophila P element transposition. Trends Genet. 1991 Sep;7(9):282–287. doi: 10.1016/0168-9525(91)90309-E. [DOI] [PubMed] [Google Scholar]
  34. Robertson H. M., Engels W. R. Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics. 1989 Dec;123(4):815–824. doi: 10.1093/genetics/123.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Roiha H., Rubin G. M., O'Hare K. P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics. 1988 May;119(1):75–83. doi: 10.1093/genetics/119.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ronsseray S., Lehmann M., Anxolabéhère D. The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics. 1991 Oct;129(2):501–512. doi: 10.1093/genetics/129.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rost B., Sander C. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993 Jul 20;232(2):584–599. doi: 10.1006/jmbi.1993.1413. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Siebel C. W., Rio D. C. Regulated splicing of the Drosophila P transposable element third intron in vitro: somatic repression. Science. 1990 Jun 8;248(4960):1200–1208. doi: 10.1126/science.2161558. [DOI] [PubMed] [Google Scholar]
  40. Simmons M. J., Bucholz L. M. Transposase titration in Drosophila melanogaster: a model of cytotype in the P-M system of hybrid dysgenesis. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8119–8123. doi: 10.1073/pnas.82.23.8119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Simonelig M., Anxolabéhère D. A P element of Scaptomyza pallida is active in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6102–6106. doi: 10.1073/pnas.88.14.6102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  43. Steller H., Pirrotta V. P transposons controlled by the heat shock promoter. Mol Cell Biol. 1986 May;6(5):1640–1649. doi: 10.1128/mcb.6.5.1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tseng J. C., Zollman S., Chain A. C., Laski F. A. Splicing of the Drosophila P element ORF2-ORF3 intron is inhibited in a human cell extract. Mech Dev. 1991 Aug;35(1):65–72. doi: 10.1016/0925-4773(91)90042-5. [DOI] [PubMed] [Google Scholar]

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