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. 1999 Nov;153(3):1371–1383. doi: 10.1093/genetics/153.3.1371

The function of the broad-complex during Drosophila melanogaster oogenesis.

G Tzolovsky 1, W M Deng 1, T Schlitt 1, M Bownes 1
PMCID: PMC1460822  PMID: 10545465

Abstract

The Broad-Complex (BR-C) is an early ecdysone response gene that functions during metamorphosis and encodes a family of zinc-finger transcription factors. It is expressed in a dynamic pattern during oogenesis. Its late expression in the lateral-dorsal-anterior follicle cells is related to the morphogenesis of the chorionic appendages. All four zinc-finger isoforms are expressed in oogenesis, which is consistent with the abnormal appendage phenotypes resulting from their ectopic expression. We investigated the mechanism by which the BR-C affects chorion deposition by using BrdU to follow the effects of BR-C misexpression on DNA replication and in situ hybridization to ovarian mRNA to evaluate chorion gene expression. Ectopic BR-C expression leads to prolonged endoreplication and to additional amplification of genes, besides the chorion genes, at other sites in the genome. The pattern of chorion gene expression is not affected along the anterior-posterior axis, but the follicle cells at the anterior of the oocyte fail to migrate correctly in an anterior direction when BR-C is misexpressed. We conclude that the target genes of the BR-C in oogenesis include a protein essential for endoreplication and chorion gene amplification. This may provide a link between steroid hormones and the control of DNA replication during oogenesis.

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Selected References

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  1. Ashburner M. Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster. II. The effects of inhibitors of protein synthesis. Dev Biol. 1974 Jul;39(1):141–157. doi: 10.1016/s0012-1606(74)80016-3. [DOI] [PubMed] [Google Scholar]
  2. Bardwell V. J., Treisman R. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994 Jul 15;8(14):1664–1677. doi: 10.1101/gad.8.14.1664. [DOI] [PubMed] [Google Scholar]
  3. Bayer C. A., Holley B., Fristrom J. W. A switch in broad-complex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol. 1996 Jul 10;177(1):1–14. doi: 10.1006/dbio.1996.0140. [DOI] [PubMed] [Google Scholar]
  4. Bayer C. A., von Kalm L., Fristrom J. W. Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev Biol. 1997 Jul 15;187(2):267–282. doi: 10.1006/dbio.1997.8620. [DOI] [PubMed] [Google Scholar]
  5. Belyaeva E. S., Aizenzon M. G., Semeshin V. F., Kiss I. I., Koczka K., Baritcheva E. M., Gorelova T. D., Zhimulev I. F. Cytogenetic analysis of the 2B3-4--2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma. 1980;81(2):281–306. doi: 10.1007/BF00285954. [DOI] [PubMed] [Google Scholar]
  6. Bownes M. The regulation of the yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. Bioessays. 1994 Oct;16(10):745–752. doi: 10.1002/bies.950161009. [DOI] [PubMed] [Google Scholar]
  7. Brennan C. A., Ashburner M., Moses K. Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development. 1998 Jul;125(14):2653–2664. doi: 10.1242/dev.125.14.2653. [DOI] [PubMed] [Google Scholar]
  8. Calvi B. R., Lilly M. A., Spradling A. C. Cell cycle control of chorion gene amplification. Genes Dev. 1998 Mar 1;12(5):734–744. doi: 10.1101/gad.12.5.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chao A. T., Guild G. M. Molecular analysis of the ecdysterone-inducible 2B5 "early' puff in Drosophila melanogaster. EMBO J. 1986 Jan;5(1):143–150. doi: 10.1002/j.1460-2075.1986.tb04188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crispi S., Giordano E., D'Avino P. P., Furia M. Cross-talking among Drosophila nuclear receptors at the promiscuous response element of the ng-1 and ng-2 intermolt genes. J Mol Biol. 1998 Jan 30;275(4):561–574. doi: 10.1006/jmbi.1997.1473. [DOI] [PubMed] [Google Scholar]
  11. Delidakis C., Kafatos F. C. Amplification enhancers and replication origins in the autosomal chorion gene cluster of Drosophila. EMBO J. 1989 Mar;8(3):891–901. doi: 10.1002/j.1460-2075.1989.tb03450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deng W. M., Bownes M. Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development. 1997 Nov;124(22):4639–4647. doi: 10.1242/dev.124.22.4639. [DOI] [PubMed] [Google Scholar]
  13. DiBello P. R., Withers D. A., Bayer C. A., Fristrom J. W., Guild G. M. The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics. 1991 Oct;129(2):385–397. doi: 10.1093/genetics/129.2.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Emery I. F., Bedian V., Guild G. M. Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development. 1994 Nov;120(11):3275–3287. doi: 10.1242/dev.120.11.3275. [DOI] [PubMed] [Google Scholar]
  15. Hodgetts R. B., Clark W. C., O'Keefe S. L., Schouls M., Crossgrove K., Guild G. M., von Kalm L. Hormonal induction of Dopa decarboxylase in the epidermis of Drosophila is mediated by the Broad-Complex. Development. 1995 Nov;121(11):3913–3922. doi: 10.1242/dev.121.11.3913. [DOI] [PubMed] [Google Scholar]
  16. Horner M. A., Chen T., Thummel C. S. Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev Biol. 1995 Apr;168(2):490–502. doi: 10.1006/dbio.1995.1097. [DOI] [PubMed] [Google Scholar]
  17. Huang R. Y., Orr W. C. Broad-complex function during oogenesis in Drosophila melanogaster. Dev Genet. 1992;13(4):277–288. doi: 10.1002/dvg.1020130405. [DOI] [PubMed] [Google Scholar]
  18. Karim F. D., Guild G. M., Thummel C. S. The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development. 1993 Jul;118(3):977–988. doi: 10.1242/dev.118.3.977. [DOI] [PubMed] [Google Scholar]
  19. Kiss I., Beaton A. H., Tardiff J., Fristrom D., Fristrom J. W. Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics. 1988 Feb;118(2):247–259. doi: 10.1093/genetics/118.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lilly M. A., Spradling A. C. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 1996 Oct 1;10(19):2514–2526. doi: 10.1101/gad.10.19.2514. [DOI] [PubMed] [Google Scholar]
  21. Lin H., Spradling A. C. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993 Sep;159(1):140–152. doi: 10.1006/dbio.1993.1228. [DOI] [PubMed] [Google Scholar]
  22. Orr-Weaver T. L. Drosophila chorion genes: cracking the eggshell's secrets. Bioessays. 1991 Mar;13(3):97–105. doi: 10.1002/bies.950130302. [DOI] [PubMed] [Google Scholar]
  23. Orr-Weaver T. L., Spradling A. C. Drosophila chorion gene amplification requires an upstream region regulating s18 transcription. Mol Cell Biol. 1986 Dec;6(12):4624–4633. doi: 10.1128/mcb.6.12.4624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Orr W. C., Galanopoulos V. K., Romano C. P., Kafatos F. C. A female sterile screen of the Drosophila melanogaster X chromosome using hybrid dysgenesis: identification and characterization of egg morphology mutants. Genetics. 1989 Aug;122(4):847–858. doi: 10.1093/genetics/122.4.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Soller M., Bownes M., Kubli E. Control of oocyte maturation in sexually mature Drosophila females. Dev Biol. 1999 Apr 15;208(2):337–351. doi: 10.1006/dbio.1999.9210. [DOI] [PubMed] [Google Scholar]
  26. Spradling A. C., Digan M. E., Mahowald A. P., Scott M., Craig E. A. Two clusters of genes for major chorion proteins of Drosophila melanogaster. Cell. 1980 Apr;19(4):905–914. doi: 10.1016/0092-8674(80)90082-3. [DOI] [PubMed] [Google Scholar]
  27. Spradling A. C., Mahowald A. P. Amplification of genes for chorion proteins during oogenesis in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1096–1100. doi: 10.1073/pnas.77.2.1096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Yao T. P., Segraves W. A., Oro A. E., McKeown M., Evans R. M. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell. 1992 Oct 2;71(1):63–72. doi: 10.1016/0092-8674(92)90266-f. [DOI] [PubMed] [Google Scholar]
  30. Zollman S., Godt D., Privé G. G., Couderc J. L., Laski F. A. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10717–10721. doi: 10.1073/pnas.91.22.10717. [DOI] [PMC free article] [PubMed] [Google Scholar]

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