Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1996 Sep;144(1):159–170. doi: 10.1093/genetics/144.1.159

The Drosophila Eip78c Gene Is Not Vital but Has a Role in Regulating Chromosome Puffs

SRH Russell 1, G Heimbeck 1, C M Goddard 1, ATC Carpenter 1, M Ashburner 1
PMCID: PMC1207490  PMID: 8878682

Abstract

We have generated a number of chromosomal aberrations that disrupt the early-late ecdysone-induced 78C puff gene (Eip78C, ecdysone-induced protein, FlyBase name for the E78 gene of STONE and THUMMEL 1993), which encodes the two members of the nuclear hormone receptor superfamily Eip78C-A and Eip78C-B. The aberrations include deletions of the ligand-binding/dimerization domain of both, inversions that split Eip78C-A but retain residual Eip78C-B expression, and a small deletion specific for Eip78C-B. We find that wild-type Eip78C functions are completely dispensable for normal development under laboratory conditions. However, we show that Eip78C-B is required for the maximal puffing activity of a subset of late puffs (63E and 82F) since these puffs are reduced in size in Eip78C-B mutant backgrounds. Paradoxically the same late puffs are reduced, as well as at least one other, when the Eip78C-B cDNA is overexpressed from a heat shock promoter. These data indicate either that Eip78C function is redundant or that it plays a subtle modulating role in the regulation of chromosome puffing.

Full Text

The Full Text of this article is available as a PDF (5.1 MB).

Selected References

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

  1. Ashburner M., Chihara C., Meltzer P., Richards G. Temporal control of puffing activity in polytene chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:655–662. doi: 10.1101/sqb.1974.038.01.070. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M. Patterns of puffing activity in the salivary gland chromosomes of Drosophila. VI. Induction by ecdysone in salivary glands of D. melanogaster cultured in vitro. Chromosoma. 1972;38(3):255–281. doi: 10.1007/BF00290925. [DOI] [PubMed] [Google Scholar]
  3. Ashburner M. Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster. I. Dependence upon ecdysone concentration. Dev Biol. 1973 Nov;35(1):47–61. doi: 10.1016/0012-1606(73)90006-7. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. BECKER H. J. [The puffs of salivary gland chromosomes of Drosophilia melanogaster. Part 1. Observations on the behavior of a typical puff in the normal strain and in two mutants, giant and lethal giant larvae]. Chromosoma. 1959;10:654–678. doi: 10.1007/BF00396591. [DOI] [PubMed] [Google Scholar]
  6. Bellen H. J., O'Kane C. J., Wilson C., Grossniklaus U., Pearson R. K., Gehring W. J. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. doi: 10.1101/gad.3.9.1288. [DOI] [PubMed] [Google Scholar]
  7. Belyaeva E. S., Vlassova I. E., Biyasheva Z. M., Kakpakov V. T., Richards G., Zhimulev I. F. Cytogenetic analysis of the 2B3-4-2B11 region of the X chromosome of Drosophila melanogaster. II. Changes in 20-OH ecdysone puffing caused by genetic defects of puff 2B5. Chromosoma. 1981;84(2):207–219. doi: 10.1007/BF00399132. [DOI] [PubMed] [Google Scholar]
  8. Berendes H. D. The hormone ecdysone as effector of specific changes in the pattern of gene activities of Drosophila hydei. Chromosoma. 1967;22(3):274–293. doi: 10.1007/BF00319878. [DOI] [PubMed] [Google Scholar]
  9. Boyd L., O'Toole E., Thummel C. S. Patterns of E74A RNA and protein expression at the onset of metamorphosis in Drosophila. Development. 1991 Aug;112(4):981–995. doi: 10.1242/dev.112.4.981. [DOI] [PubMed] [Google Scholar]
  10. Burtis K. C., Thummel C. S., Jones C. W., Karim F. D., Hogness D. S. The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell. 1990 Apr 6;61(1):85–99. doi: 10.1016/0092-8674(90)90217-3. [DOI] [PubMed] [Google Scholar]
  11. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  12. Crosby M. A., Meyerowitz E. M. Drosophila glue gene Sgs-3: sequences required for puffing and transcriptional regulation. Dev Biol. 1986 Dec;118(2):593–607. doi: 10.1016/0012-1606(86)90029-1. [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. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 1988 May 13;240(4854):889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Feigl G., Gram M., Pongs O. A member of the steroid hormone receptor gene family is expressed in the 20-OH-ecdysone inducible puff 75B in Drosophila melanogaster. Nucleic Acids Res. 1989 Sep 25;17(18):7167–7178. doi: 10.1093/nar/17.18.7167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  17. Fisk G. J., Thummel C. S. Isolation, regulation, and DNA-binding properties of three Drosophila nuclear hormone receptor superfamily members. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10604–10608. doi: 10.1073/pnas.92.23.10604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fletcher J. C., Burtis K. C., Hogness D. S., Thummel C. S. The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development. 1995 May;121(5):1455–1465. doi: 10.1242/dev.121.5.1455. [DOI] [PubMed] [Google Scholar]
  19. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Huet F., Ruiz C., Richards G. Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes. Development. 1995 Apr;121(4):1195–1204. doi: 10.1242/dev.121.4.1195. [DOI] [PubMed] [Google Scholar]
  22. Janknecht R., Taube W., Lüdecke H. J., Pongs O. Characterization of a putative transcription factor gene expressed in the 20-OH-ecdysone inducible puff 74EF in Drosophila melanogaster. Nucleic Acids Res. 1989 Jun 26;17(12):4455–4464. doi: 10.1093/nar/17.12.4455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kastner P., Mark M., Chambon P. Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell. 1995 Dec 15;83(6):859–869. doi: 10.1016/0092-8674(95)90202-3. [DOI] [PubMed] [Google Scholar]
  24. Koelle M. R., Segraves W. A., Hogness D. S. DHR3: a Drosophila steroid receptor homolog. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6167–6171. doi: 10.1073/pnas.89.13.6167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lavorgna G., Karim F. D., Thummel C. S., Wu C. Potential role for a FTZ-F1 steroid receptor superfamily member in the control of Drosophila metamorphosis. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3004–3008. doi: 10.1073/pnas.90.7.3004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leid M., Kastner P., Chambon P. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem Sci. 1992 Oct;17(10):427–433. doi: 10.1016/0968-0004(92)90014-z. [DOI] [PubMed] [Google Scholar]
  27. Mangelsdorf D. J., Evans R. M. The RXR heterodimers and orphan receptors. Cell. 1995 Dec 15;83(6):841–850. doi: 10.1016/0092-8674(95)90200-7. [DOI] [PubMed] [Google Scholar]
  28. McCarron M., Duttaroy A., Doughty G., Chovnick A. Drosophila P element transposase induces male recombination additively and without a requirement for P element excision or insertion. Genetics. 1994 Mar;136(3):1013–1023. doi: 10.1093/genetics/136.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohno C. K., Petkovich M. FTZ-F1 beta, a novel member of the Drosophila nuclear receptor family. Mech Dev. 1993 Jan;40(1-2):13–24. doi: 10.1016/0925-4773(93)90084-b. [DOI] [PubMed] [Google Scholar]
  30. Segraves W. A., Hogness D. S. The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev. 1990 Feb;4(2):204–219. doi: 10.1101/gad.4.2.204. [DOI] [PubMed] [Google Scholar]
  31. Stone B. L., Thummel C. S. The Drosophila 78C early late puff contains E78, an ecdysone-inducible gene that encodes a novel member of the nuclear hormone receptor superfamily. Cell. 1993 Oct 22;75(2):307–320. doi: 10.1016/0092-8674(93)80072-m. [DOI] [PubMed] [Google Scholar]
  32. Stunnenberg H. G. Mechanisms of transactivation by retinoic acid receptors. Bioessays. 1993 May;15(5):309–315. doi: 10.1002/bies.950150504. [DOI] [PubMed] [Google Scholar]
  33. Thomas H. E., Stunnenberg H. G., Stewart A. F. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature. 1993 Apr 1;362(6419):471–475. doi: 10.1038/362471a0. [DOI] [PubMed] [Google Scholar]
  34. Walker V. K., Ashburner M. The control of ecdysterone-regulated puffs in Drosophila salivary glands. Cell. 1981 Oct;26(2 Pt 2):269–277. doi: 10.1016/0092-8674(81)90309-3. [DOI] [PubMed] [Google Scholar]
  35. Yao T. P., Forman B. M., Jiang Z., Cherbas L., Chen J. D., McKeown M., Cherbas P., Evans R. M. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature. 1993 Dec 2;366(6454):476–479. doi: 10.1038/366476a0. [DOI] [PubMed] [Google Scholar]
  36. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES