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. 1991 Mar;10(3):665–674. doi: 10.1002/j.1460-2075.1991.tb07995.x

Repression of the Drosophila fushi tarazu (ftz) segmentation gene.

J L Brown 1, S Sonoda 1, H Ueda 1, M P Scott 1, C Wu 1
PMCID: PMC452699  PMID: 2001679

Abstract

The striped expression of the Drosophila segmentation gene fushi tarazu in alternate parasegments of the early embryo is controlled by the 740 bp zebra element. Among multiple protein factors that bind to the zebra element, FTZ-F2 behaves as a transcriptional repressor of ftz. Point mutations in the zebra element which disrupt FTZ-F2 binding to DNA cause ectopic expression of zebra-lacZ activity in transformed embryos. The mutant constructs are expressed from the zygotic genome in preblastoderm embryos as early as the third nuclear division cycle. This unprecedented early transcription suggests that ftz requires active repression during initial nuclear division cycles, a novel type of embryonic gene regulation. A putative FTZ-F2 cDNA clone isolated by recognition site screening of an expression library was found to be identical in sequence with the zinc finger protein tramtrack (Harrison and Travers, 1990).

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Selected References

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

  1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
  2. Anderson K. V., Lengyel J. A. Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol. 1979 May;70(1):217–231. doi: 10.1016/0012-1606(79)90018-6. [DOI] [PubMed] [Google Scholar]
  3. Carroll S. B., Laughon A., Thalley B. S. Expression, function, and regulation of the hairy segmentation protein in the Drosophila embryo. Genes Dev. 1988 Jul;2(7):883–890. doi: 10.1101/gad.2.7.883. [DOI] [PubMed] [Google Scholar]
  4. Carroll S. B., Scott M. P. Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell. 1985 Nov;43(1):47–57. doi: 10.1016/0092-8674(85)90011-x. [DOI] [PubMed] [Google Scholar]
  5. Carroll S. B., Scott M. P. Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell. 1986 Apr 11;45(1):113–126. doi: 10.1016/0092-8674(86)90543-x. [DOI] [PubMed] [Google Scholar]
  6. Carroll S. B. Zebra patterns in fly embryos: activation of stripes or repression of interstripes? Cell. 1990 Jan 12;60(1):9–16. doi: 10.1016/0092-8674(90)90711-m. [DOI] [PubMed] [Google Scholar]
  7. Dearolf C. R., Topol J., Parker C. S. The caudal gene product is a direct activator of fushi tarazu transcription during Drosophila embryogenesis. Nature. 1989 Sep 28;341(6240):340–343. doi: 10.1038/341340a0. [DOI] [PubMed] [Google Scholar]
  8. Dearolf C. R., Topol J., Parker C. S. Transcriptional control of Drosophila fushi tarazu zebra stripe expression. Genes Dev. 1989 Mar;3(3):384–398. doi: 10.1101/gad.3.3.384. [DOI] [PubMed] [Google Scholar]
  9. Doe C. Q., Hiromi Y., Gehring W. J., Goodman C. S. Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science. 1988 Jan 8;239(4836):170–175. doi: 10.1126/science.2892267. [DOI] [PubMed] [Google Scholar]
  10. Edgar B. A., Kiehle C. P., Schubiger G. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell. 1986 Jan 31;44(2):365–372. doi: 10.1016/0092-8674(86)90771-3. [DOI] [PubMed] [Google Scholar]
  11. Edgar B. A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell. 1986 Mar 28;44(6):871–877. doi: 10.1016/0092-8674(86)90009-7. [DOI] [PubMed] [Google Scholar]
  12. Edgar B. A., Weir M. P., Schubiger G., Kornberg T. Repression and turnover pattern fushi tarazu RNA in the early Drosophila embryo. Cell. 1986 Dec 5;47(5):747–754. doi: 10.1016/0092-8674(86)90517-9. [DOI] [PubMed] [Google Scholar]
  13. Frasch M., Levine M. Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila. Genes Dev. 1987 Nov;1(9):981–995. doi: 10.1101/gad.1.9.981. [DOI] [PubMed] [Google Scholar]
  14. Hafen E., Kuroiwa A., Gehring W. J. Spatial distribution of transcripts from the segmentation gene fushi tarazu during Drosophila embryonic development. Cell. 1984 Jul;37(3):833–841. doi: 10.1016/0092-8674(84)90418-5. [DOI] [PubMed] [Google Scholar]
  15. Harrison S. D., Travers A. A. Identification of the binding sites for potential regulatory proteins in the upstream enhancer element of the Drosophila fushi tarazu gene. Nucleic Acids Res. 1988 Dec 23;16(24):11403–11416. doi: 10.1093/nar/16.24.11403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harrison S. D., Travers A. A. The tramtrack gene encodes a Drosophila finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J. 1990 Jan;9(1):207–216. doi: 10.1002/j.1460-2075.1990.tb08097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Hiromi Y., Kuroiwa A., Gehring W. J. Control elements of the Drosophila segmentation gene fushi tarazu. Cell. 1985 Dec;43(3 Pt 2):603–613. doi: 10.1016/0092-8674(85)90232-6. [DOI] [PubMed] [Google Scholar]
  19. Hooper K. L., Parkhurst S. M., Ish-Horowicz D. Spatial control of hairy protein expression during embryogenesis. Development. 1989 Nov;107(3):489–504. doi: 10.1242/dev.107.3.489. [DOI] [PubMed] [Google Scholar]
  20. Howard K., Ingham P. Regulatory interactions between the segmentation genes fushi tarazu, hairy, and engrailed in the Drosophila blastoderm. Cell. 1986 Mar 28;44(6):949–957. doi: 10.1016/0092-8674(86)90018-8. [DOI] [PubMed] [Google Scholar]
  21. Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
  22. Ish-Horowicz D., Pinchin S. M., Ingham P. W., Gyurkovics H. G. Autocatalytic ftz activation and metameric instability induced by ectopic ftz expression. Cell. 1989 Apr 21;57(2):223–232. doi: 10.1016/0092-8674(89)90960-4. [DOI] [PubMed] [Google Scholar]
  23. Ish-Horowicz D., Pinchin S. M. Pattern abnormalities induced by ectopic expression of the Drosophila gene hairy are associated with repression of ftz transcription. Cell. 1987 Nov 6;51(3):405–415. doi: 10.1016/0092-8674(87)90636-2. [DOI] [PubMed] [Google Scholar]
  24. Karr T. L., Kornberg T. B. fushi tarazu protein expression in the cellular blastoderm of Drosophila detected using a novel imaging technique. Development. 1989 May;106(1):95–103. doi: 10.1242/dev.106.1.95. [DOI] [PubMed] [Google Scholar]
  25. Karr T. L., Weir M. P., Ali Z., Kornberg T. Patterns of engrailed protein in early Drosophila embryos. Development. 1989 Mar;105(3):605–612. doi: 10.1242/dev.105.3.605. [DOI] [PubMed] [Google Scholar]
  26. Krause H. M., Klemenz R., Gehring W. J. Expression, modification, and localization of the fushi tarazu protein in Drosophila embryos. Genes Dev. 1988 Aug;2(8):1021–1036. doi: 10.1101/gad.2.8.1021. [DOI] [PubMed] [Google Scholar]
  27. Lamb M. M., Laird C. D. Increase in nuclear poly(A)-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. Dev Biol. 1976 Aug;52(1):31–42. doi: 10.1016/0012-1606(76)90004-x. [DOI] [PubMed] [Google Scholar]
  28. Lawrence P. A., Johnston P., Macdonald P., Struhl G. Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes. 1987 Jul 30-Aug 5Nature. 328(6129):440–442. doi: 10.1038/328440a0. [DOI] [PubMed] [Google Scholar]
  29. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  30. McKnight S. L., Miller O. L., Jr Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell. 1976 Jun;8(2):305–319. doi: 10.1016/0092-8674(76)90014-3. [DOI] [PubMed] [Google Scholar]
  31. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
  32. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  33. Nüsslein-Volhard C., Frohnhöfer H. G., Lehmann R. Determination of anteroposterior polarity in Drosophila. Science. 1987 Dec 18;238(4834):1675–1681. doi: 10.1126/science.3686007. [DOI] [PubMed] [Google Scholar]
  34. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980 Oct 30;287(5785):795–801. doi: 10.1038/287795a0. [DOI] [PubMed] [Google Scholar]
  35. Pankratz M. J., Seifert E., Gerwin N., Billi B., Nauber U., Jäckle H. Gradients of Krüppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the Drosophila embryo. Cell. 1990 Apr 20;61(2):309–317. doi: 10.1016/0092-8674(90)90811-r. [DOI] [PubMed] [Google Scholar]
  36. Pick L., Schier A., Affolter M., Schmidt-Glenewinkel T., Gehring W. J. Analysis of the ftz upstream element: germ layer-specific enhancers are independently autoregulated. Genes Dev. 1990 Jul;4(7):1224–1239. doi: 10.1101/gad.4.7.1224. [DOI] [PubMed] [Google Scholar]
  37. Rosenfeld P. J., Kelly T. J. Purification of nuclear factor I by DNA recognition site affinity chromatography. J Biol Chem. 1986 Jan 25;261(3):1398–1408. [PubMed] [Google Scholar]
  38. Schröder C., Tautz D., Seifert E., Jäckle H. Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback. EMBO J. 1988 Sep;7(9):2881–2887. doi: 10.1002/j.1460-2075.1988.tb03145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Scott M. P., Carroll S. B. The segmentation and homeotic gene network in early Drosophila development. Cell. 1987 Dec 4;51(5):689–698. doi: 10.1016/0092-8674(87)90092-4. [DOI] [PubMed] [Google Scholar]
  40. Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
  41. Struhl G. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature. 1985 Dec 19;318(6047):677–680. doi: 10.1038/318677a0. [DOI] [PubMed] [Google Scholar]
  42. Ueda H., Sonoda S., Brown J. L., Scott M. P., Wu C. A sequence-specific DNA-binding protein that activates fushi tarazu segmentation gene expression. Genes Dev. 1990 Apr;4(4):624–635. doi: 10.1101/gad.4.4.624. [DOI] [PubMed] [Google Scholar]
  43. Vinson C. R., LaMarco K. L., Johnson P. F., Landschulz W. H., McKnight S. L. In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. Genes Dev. 1988 Jul;2(7):801–806. doi: 10.1101/gad.2.7.801. [DOI] [PubMed] [Google Scholar]
  44. Wakimoto B. T., Kaufman T. C. Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. Dev Biol. 1981 Jan 15;81(1):51–64. doi: 10.1016/0012-1606(81)90347-x. [DOI] [PubMed] [Google Scholar]
  45. Weir M. P., Kornberg T. Patterns of engrailed and fushi tarazu transcripts reveal novel intermediate stages in Drosophila segmentation. Nature. 1985 Dec 5;318(6045):433–439. doi: 10.1038/318433a0. [DOI] [PubMed] [Google Scholar]

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