Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1986 Dec 1;5(12):3335–3342. doi: 10.1002/j.1460-2075.1986.tb04648.x

Regulated splicing produces different forms of dopa decarboxylase in the central nervous system and hypoderm of Drosophila melanogaster.

B A Morgan, W A Johnson, J Hirsh
PMCID: PMC1167331  PMID: 3102230

Abstract

The dopa decarboxylase gene (Ddc) of Drosophila melanogaster is expressed in the hypoderm and the nervous system and promoter elements mediating differential expression in these tissues have been identified (Scholnick et al., 1986). Here we report an additional mode of regulation; the unique primary transcript of the Ddc gene is spliced to form mRNAs in these two tissues which differ by a single internal exon. In vitro mutagenesis and P-element-mediated transformation were employed to manipulate the tissue-specific expression of these RNAs. This approach demonstrated that regulated splicing rather than differential stability causes the tissue-specific expression of these RNAs and allowed the identification of Ddc enzyme isoforms encoded by each mRNA. The Ddc enzyme in the central nervous system differs from the hypodermal Ddc protein by the addition of 33-35 amino acids on the N terminus.

Full text

PDF
3335

Images in this article

Selected References

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

  1. Beall C. J., Hirsh J. High levels of intron-containing RNAs are associated with expression of the Drosophila DOPA decarboxylase gene. Mol Cell Biol. 1984 Sep;4(9):1669–1674. doi: 10.1128/mcb.4.9.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bernstein S. I., Hansen C. J., Becker K. D., Wassenberg D. R., 2nd, Roche E. S., Donady J. J., Emerson C. P., Jr Alternative RNA splicing generates transcripts encoding a thorax-specific isoform of Drosophila melanogaster myosin heavy chain. Mol Cell Biol. 1986 Jul;6(7):2511–2519. doi: 10.1128/mcb.6.7.2511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  4. Bossa F., Martini F., Barra D., Voltattorni C. B., Minelli A., Turano C. The chymotryptic phosphopyridoxyl peptide of DOPA decarboxylase from pig kidney. Biochem Biophys Res Commun. 1977 Sep 9;78(1):177–184. doi: 10.1016/0006-291x(77)91237-2. [DOI] [PubMed] [Google Scholar]
  5. Breitbart R. E., Nguyen H. T., Medford R. M., Destree A. T., Mahdavi V., Nadal-Ginard B. Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell. 1985 May;41(1):67–82. doi: 10.1016/0092-8674(85)90062-5. [DOI] [PubMed] [Google Scholar]
  6. Eveleth D. D., Gietz R. D., Spencer C. A., Nargang F. E., Hodgetts R. B., Marsh J. L. Sequence and structure of the dopa decarboxylase gene of Drosophila: evidence for novel RNA splicing variants. EMBO J. 1986 Oct;5(10):2663–2672. doi: 10.1002/j.1460-2075.1986.tb04549.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Falkenthal S., Parker V. P., Davidson N. Developmental variations in the splicing pattern of transcripts from the Drosophila gene encoding myosin alkali light chain result in different carboxyl-terminal amino acid sequences. Proc Natl Acad Sci U S A. 1985 Jan;82(2):449–453. doi: 10.1073/pnas.82.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gilbert D., Hirsh J., Wright T. R. Molecular mapping of a gene cluster flanking the Drosophila Dopa decarboxylase gene. Genetics. 1984 Apr;106(4):679–694. doi: 10.1093/genetics/106.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hirsh J., Davidson N. Isolation and characterization of the dopa decarboxylase gene of Drosophila melanogaster. Mol Cell Biol. 1981 Jun;1(6):475–485. doi: 10.1128/mcb.1.6.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res. 1985 Jul 11;13(13):4971–4981. doi: 10.1093/nar/13.13.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kraminsky G. P., Clark W. C., Estelle M. A., Gietz R. D., Sage B. A., O'Connor J. D., Hodgetts R. B. Induction of translatable mRNA for dopa decarboxylase in Drosophila: an early response to ecdysterone. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4175–4179. doi: 10.1073/pnas.77.7.4175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Livingstone M. S., Tempel B. L. Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature. 1983 May 5;303(5912):67–70. doi: 10.1038/303067a0. [DOI] [PubMed] [Google Scholar]
  14. Marsh J. L., Wright T. R. Developmental relationship between dopa decarboxylase, dopamine acetyltransferase, and ecdysone in Drosophila. Dev Biol. 1980 Dec;80(2):379–387. doi: 10.1016/0012-1606(80)90412-1. [DOI] [PubMed] [Google Scholar]
  15. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nawa H., Kotani H., Nakanishi S. Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature. 1984 Dec 20;312(5996):729–734. doi: 10.1038/312729a0. [DOI] [PubMed] [Google Scholar]
  17. Ohshima Y., Itoh M., Okada N., Miyata T. Novel models for RNA splicing that involve a small nuclear RNA. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4471–4474. doi: 10.1073/pnas.78.7.4471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Peabody D. S., Berg P. Termination-reinitiation occurs in the translation of mammalian cell mRNAs. Mol Cell Biol. 1986 Jul;6(7):2695–2703. doi: 10.1128/mcb.6.7.2695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  20. Rozek C. E., Davidson N. Differential processing of RNA transcribed from the single-copy Drosophila myosin heavy chain gene produces four mRNAs that encode two polypeptides. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2128–2132. doi: 10.1073/pnas.83.7.2128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Schmidt-Nielsen B. K., Gepner J. I., Teng N. N., Hall L. M. Characterization of an alpha-bungarotoxin binding component from Drosophila melanogaster. J Neurochem. 1977 Dec;29(6):1013–1029. doi: 10.1111/j.1471-4159.1977.tb06505.x. [DOI] [PubMed] [Google Scholar]
  23. Scholnick S. B., Morgan B. A., Hirsh J. The cloned dopa decarboxylase gene is developmentally regulated when reintegrated into the Drosophila genome. Cell. 1983 Aug;34(1):37–45. doi: 10.1016/0092-8674(83)90134-4. [DOI] [PubMed] [Google Scholar]
  24. Solnick D. Alternative splicing caused by RNA secondary structure. Cell. 1985 Dec;43(3 Pt 2):667–676. doi: 10.1016/0092-8674(85)90239-9. [DOI] [PubMed] [Google Scholar]
  25. Wright T. R., Bewley G. C., Sherald A. F. The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopa-decarboxylase-deficient mutants and their relationship to the alpha-methyl-dopa-hypersensitive mutants. Genetics. 1976 Oct;84(2):287–310. doi: 10.1093/genetics/84.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES