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. 1992 Mar 25;20(6):1325–1332. doi: 10.1093/nar/20.6.1325

Regulation of the Dictyostelium cAMP-induced, prestalk-specific DdrasD gene: identification of cis-acting elements.

R K Esch 1, P K Howard 1, R A Firtel 1
PMCID: PMC312178  PMID: 1313967

Abstract

We have shown previously that expression of the Dictyostelium ras gene DdrasD (previously denoted Ddras) is induced during multicellular development and in single-cell shaking culture in response to cAMP (1). Analysis of transformants carrying DdrasD/lacZ reporter constructs showed DdrasD expression to be prestalk-specific (2). The gene is transcribed from three start sites with transcription from the distal site producing an approximately 1.2 kb transcript, which is expressed at low levels in growing cells and is subsequently induced late in aggregation. This promoter is also induced to high levels by cAMP. Transcription from the two more proximal sites is coregulated and is induced during development, resulting in approximately 1.0 kb transcripts. In this study, we examine cis-acting regions required for proper regulation of DdrasD expression using a DdrasD/beta-glucuronidase reporter gene construct. We have identified distinct sequence elements required for developmental and vegetative expression of DdrasD. A domain containing a CA repeat, similar to ones found in other late, cAMP-induced Dictyostelium genes, is required for cAMP-induced and developmental expression.

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Selected References

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

  1. Adhya S., Gottesman M. Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982 Jul;29(3):939–944. doi: 10.1016/0092-8674(82)90456-1. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  3. Cullen B. R., Lomedico P. T., Ju G. Transcriptional interference in avian retroviruses--implications for the promoter insertion model of leukaemogenesis. Nature. 1984 Jan 19;307(5948):241–245. doi: 10.1038/307241a0. [DOI] [PubMed] [Google Scholar]
  4. Datta S., Firtel R. A. Identification of the sequences controlling cyclic AMP regulation and cell-type-specific expression of a prestalk-specific gene in Dictyostelium discoideum. Mol Cell Biol. 1987 Jan;7(1):149–159. doi: 10.1128/mcb.7.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Datta S., Gomer R. H., Firtel R. A. Spatial and temporal regulation of a foreign gene by a prestalk-specific promoter in transformed Dictyostelium discoideum. Mol Cell Biol. 1986 Mar;6(3):811–820. doi: 10.1128/mcb.6.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Devreotes P. Dictyostelium discoideum: a model system for cell-cell interactions in development. Science. 1989 Sep 8;245(4922):1054–1058. doi: 10.1126/science.2672337. [DOI] [PubMed] [Google Scholar]
  7. Dynes J. L., Firtel R. A. Molecular complementation of a genetic marker in Dictyostelium using a genomic DNA library. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7966–7970. doi: 10.1073/pnas.86.20.7966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Esch R. K., Firtel R. A. cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium. Genes Dev. 1991 Jan;5(1):9–21. doi: 10.1101/gad.5.1.9. [DOI] [PubMed] [Google Scholar]
  9. Firtel R. A., van Haastert P. J., Kimmel A. R., Devreotes P. N. G protein linked signal transduction pathways in development: dictyostelium as an experimental system. Cell. 1989 Jul 28;58(2):235–239. doi: 10.1016/0092-8674(89)90837-4. [DOI] [PubMed] [Google Scholar]
  10. Haberstroh L., Firtel R. A. A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium. Genes Dev. 1990 Apr;4(4):596–612. doi: 10.1101/gad.4.4.596. [DOI] [PubMed] [Google Scholar]
  11. Hjorth A. L., Khanna N. C., Firtel R. A. A trans-acting factor required for cAMP-induced gene expression in Dictyostelium is regulated developmentally and induced by cAMP. Genes Dev. 1989 Jun;3(6):747–759. doi: 10.1101/gad.3.6.747. [DOI] [PubMed] [Google Scholar]
  12. Hjorth A. L., Pears C., Williams J. G., Firtel R. A. A developmentally regulated trans-acting factor recognizes dissimilar G/C-rich elements controlling a class of cAMP-inducible Dictyostelium genes. Genes Dev. 1990 Mar;4(3):419–432. doi: 10.1101/gad.4.3.419. [DOI] [PubMed] [Google Scholar]
  13. Howard P. K., Ahern K. G., Firtel R. A. Establishment of a transient expression system for Dictyostelium discoideum. Nucleic Acids Res. 1988 Mar 25;16(6):2613–2623. doi: 10.1093/nar/16.6.2613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kimmel A. R., Firtel R. A. cAMP signal transduction pathways regulating development of Dictyostelium discoideum. Curr Opin Genet Dev. 1991 Oct;1(3):383–390. doi: 10.1016/s0959-437x(05)80304-1. [DOI] [PubMed] [Google Scholar]
  15. Kunkel G. R., Martinson H. G. Nucleosomes will not form on double-stranded RNa or over poly(dA).poly(dT) tracts in recombinant DNA. Nucleic Acids Res. 1981 Dec 21;9(24):6869–6888. doi: 10.1093/nar/9.24.6869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leiting B., Lindner I. J., Noegel A. A. The extrachromosomal replication of Dictyostelium plasmid Ddp2 requires a cis-acting element and a plasmid-encoded trans-acting factor. Mol Cell Biol. 1990 Jul;10(7):3727–3736. doi: 10.1128/mcb.10.7.3727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mann S. K., Firtel R. A. Cyclic AMP regulation of early gene expression in Dictyostelium discoideum: mediation via the cell surface cyclic AMP receptor. Mol Cell Biol. 1987 Jan;7(1):458–469. doi: 10.1128/mcb.7.1.458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mehdy M. C., Firtel R. A. A secreted factor and cyclic AMP jointly regulate cell-type-specific gene expression in Dictyostelium discoideum. Mol Cell Biol. 1985 Apr;5(4):705–713. doi: 10.1128/mcb.5.4.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mehdy M. C., Ratner D., Firtel R. A. Induction and modulation of cell-type-specific gene expression in Dictyostelium. Cell. 1983 Mar;32(3):763–771. doi: 10.1016/0092-8674(83)90062-4. [DOI] [PubMed] [Google Scholar]
  20. Noegel A., Metz B. A., Williams K. L. Developmentally regulated transcription of Dictyostelium discoideum plasmid Ddp1. EMBO J. 1985 Dec 30;4(13B):3797–3803. doi: 10.1002/j.1460-2075.1985.tb04150.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pawson T., Amiel T., Hinze E., Auersperg N., Neave N., Sobolewski A., Weeks G. Regulation of a ras-related protein during development of Dictyostelium discoideum. Mol Cell Biol. 1985 Jan;5(1):33–39. doi: 10.1128/mcb.5.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pears C. J., Williams J. G. Identification of a DNA sequence element required for efficient expression of a developmentally regulated and cAMP-inducible gene of Dictyostelium discoideum. EMBO J. 1987 Jan;6(1):195–200. doi: 10.1002/j.1460-2075.1987.tb04738.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Prunell A. Nucleosome reconstitution on plasmid-inserted poly(dA) . poly(dT). EMBO J. 1982;1(2):173–179. doi: 10.1002/j.1460-2075.1982.tb01143.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Reymond C. D., Gomer R. H., Mehdy M. C., Firtel R. A. Developmental regulation of a Dictyostelium gene encoding a protein homologous to mammalian ras protein. Cell. 1984 Nov;39(1):141–148. doi: 10.1016/0092-8674(84)90199-5. [DOI] [PubMed] [Google Scholar]
  25. Reymond C. D., Gomer R. H., Nellen W., Theibert A., Devreotes P., Firtel R. A. Phenotypic changes induced by a mutated ras gene during the development of Dictyostelium transformants. 1986 Sep 25-Oct 1Nature. 323(6086):340–343. doi: 10.1038/323340a0. [DOI] [PubMed] [Google Scholar]
  26. Reymond C. D., Nellen W., Firtel R. A. Regulated expression of ras gene constructs in Dictyostelium transformants. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7005–7009. doi: 10.1073/pnas.82.20.7005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reymond C. D., Thompson N. A. Analysis of the multiple transcripts of the Dd ras gene during Dictyostelium discoideum development. Dev Genet. 1991;12(1-2):139–146. doi: 10.1002/dvg.1020120122. [DOI] [PubMed] [Google Scholar]
  28. Robbins S. M., Williams J. G., Jermyn K. A., Spiegelman G. B., Weeks G. Growing and developing Dictyostelium cells express different ras genes. Proc Natl Acad Sci U S A. 1989 Feb;86(3):938–942. doi: 10.1073/pnas.86.3.938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sternfeld J., David C. N. Fate and regulation of anterior-like cells in Dictyostelium slugs. Dev Biol. 1982 Sep;93(1):111–118. doi: 10.1016/0012-1606(82)90244-5. [DOI] [PubMed] [Google Scholar]
  30. Vales L. D., Darnell J. E., Jr Promoter occlusion prevents transcription of adenovirus polypeptide IX mRNA until after DNA replication. Genes Dev. 1989 Jan;3(1):49–59. doi: 10.1101/gad.3.1.49. [DOI] [PubMed] [Google Scholar]
  31. Van Haastert P. J., Snaar-Jagalska B. E., Janssens P. M. The regulation of adenylate cyclase by guanine nucleotides in Dictyostelium discoideum membranes. Eur J Biochem. 1987 Jan 15;162(2):251–258. doi: 10.1111/j.1432-1033.1987.tb10592.x. [DOI] [PubMed] [Google Scholar]
  32. Van der Kaay J., Draijer R., Van Haastert P. J. Increased conversion of phosphatidylinositol to phosphatidylinositol phosphate in Dictyostelium cells expressing a mutated ras gene. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9197–9201. doi: 10.1073/pnas.87.23.9197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Williams J. G., Ceccarelli A., McRobbie S., Mahbubani H., Kay R. R., Early A., Berks M., Jermyn K. A. Direct induction of Dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell. 1987 Apr 24;49(2):185–192. doi: 10.1016/0092-8674(87)90559-9. [DOI] [PubMed] [Google Scholar]
  34. Williams J. G. The role of diffusible molecules in regulating the cellular differentiation of Dictyostelium discoideum. Development. 1988 May;103(1):1–16. [PubMed] [Google Scholar]

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