Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 Oct;9(10):4170–4178. doi: 10.1128/mcb.9.10.4170

Expression and organization of BP74, a cyclic AMP-regulated gene expressed during Dictyostelium discoideum development.

S B Hopkinson 1, R S Pollenz 1, I Drummond 1, R L Chisholm 1
PMCID: PMC362495  PMID: 2555685

Abstract

We have characterized a cDNA and the corresponding gene for a cyclic AMP-inducible gene expressed during Dictyostelium development. This gene, BP74, was found to be first expressed about the time of aggregate formation, approximately 6 h after starvation. Accumulation of BP74 mRNA did not occur in Dictyostelium cells that had been starved in fast-shaken suspension cultures but was induced in similar cultures to which cyclic AMP pulses had been added. The BP74 cDNA and gene were characterized by DNA sequence analysis and transcriptional mapping. When the BP74 promoter region was fused with a chloramphenicol acetyltransferase reporter gene and reintroduced into Dictyostelium cells, the transfected chloramphenicol acetyltransferase gene displayed the same developmentally regulated pattern of expression as did the endogenous BP74 gene, suggesting that all of the cis-acting elements required for regulated expression were carried by a 2-kilobase cloned genomic fragment. On the basis of sequence analysis, the gene appeared to encode a protein containing a 20-residue hydrophobic sequence at the amino-terminal end and 26 copies of a 20-amino-acid repeat.

Full text

PDF
4170

Images in this article

Selected References

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

  1. Ashworth J. M., Sussman M. The appearance and disappearance of uridine diphosphate glucose pyrophosphorylase activity during differntiation of the cellular slime mold Dictyostelium discoideum. J Biol Chem. 1967 Apr 25;242(8):1696–1700. [PubMed] [Google Scholar]
  2. Barklis E., Pontius B., Lodish H. F. Structure of the Dictyostelium discoideum prestalk D11 gene and protein. Mol Cell Biol. 1985 Jun;5(6):1473–1479. doi: 10.1128/mcb.5.6.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blumberg D. D., Comer J. F., Higinbotham K. G. A Ca2+-dependent signal transduction system participates in coupling expression of some cAMP-dependent prespore genes to the cell surface receptor. Dev Genet. 1988;9(4-5):359–369. doi: 10.1002/dvg.1020090417. [DOI] [PubMed] [Google Scholar]
  4. Bonner J. T. Induction of stalk cell differentiation by cyclic AMP in the cellular slime mold Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1970 Jan;65(1):110–113. doi: 10.1073/pnas.65.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cardelli J. A., Knecht D. A., Wunderlich R., Dimond R. L. Major changes in gene expression occur during at least four stages of development of Dictyostelium discoideum. Dev Biol. 1985 Jul;110(1):147–156. doi: 10.1016/0012-1606(85)90072-7. [DOI] [PubMed] [Google Scholar]
  6. Ceccarelli A., McRobbie S. J., Jermyn K. A., Duffy K., Early A., Williams J. G. Structural and functional characterization of a Dictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence. Nucleic Acids Res. 1987 Sep 25;15(18):7463–7476. doi: 10.1093/nar/15.18.7463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chisholm R. L., Barklis E., Lodish H. F. Mechanism of sequential induction of cell-type specific mRNAs in Dictyostelium differentiation. Nature. 1984 Jul 5;310(5972):67–69. doi: 10.1038/310067a0. [DOI] [PubMed] [Google Scholar]
  8. Datta S., Firtel R. A. An 80-bp cis-acting regulatory region controls cAMP and development regulation of a prestalk gene in Dictyostelium. Genes Dev. 1988 Mar;2(3):294–304. doi: 10.1101/gad.2.3.294. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Devine J. M., Tsang A. S., Williams J. G. Differential expression of the members of the discoidin I multigene family during growth and development of Dictyostelium discoideum. Cell. 1982 Apr;28(4):793–800. doi: 10.1016/0092-8674(82)90058-7. [DOI] [PubMed] [Google Scholar]
  12. Dowds B. C., Loomis W. F. Hexapeptide repeat structure in Dictyostelium spore coat protein. Biochem Biophys Res Commun. 1986 Feb 26;135(1):336–339. doi: 10.1016/0006-291x(86)90982-4. [DOI] [PubMed] [Google Scholar]
  13. Driscoll D. M., Williams J. G. Two divergently transcribed genes of Dictyostelium discoideum are cyclic AMP-inducible and coregulated during development. Mol Cell Biol. 1987 Dec;7(12):4482–4489. doi: 10.1128/mcb.7.12.4482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Drummond I. A., Chisholm R. L. The effect of caffeine, adenosine, and buffer ionic composition on the induction of cell-surface cAMP binding during starvation of Dictyostelium discoideum. Dev Genet. 1988;9(4-5):293–301. doi: 10.1002/dvg.1020090411. [DOI] [PubMed] [Google Scholar]
  15. Fishel B. R., Ragheb J. A., Rajkovic A., Haribabu B., Schweinfest C. W., Dottin R. P. Molecular cloning of a cDNA complementary to a UDP-glucose pyrophosphorylase mRNA of dictyostelium discoideum. Dev Biol. 1985 Aug;110(2):369–381. doi: 10.1016/0012-1606(85)90096-x. [DOI] [PubMed] [Google Scholar]
  16. Gomer R. H., Armstrong D., Leichtling B. H., Firtel R. A. cAMP induction of prespore and prestalk gene expression in Dictyostelium is mediated by the cell-surface cAMP receptor. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8624–8628. doi: 10.1073/pnas.83.22.8624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Haribabu B., Dottin R. P. Pharmacological characterization of cyclic AMP receptors mediating gene regulation in Dictyostelium discoideum. Mol Cell Biol. 1986 Jul;6(7):2402–2408. doi: 10.1128/mcb.6.7.2402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haribabu B., Rajkovic A., Dottin R. P. Cell-cell contact and cAMP regulate the expression of a UDP glucose pyrophosphorylase gene of Dictyostelium discoideum. Dev Biol. 1986 Feb;113(2):436–442. doi: 10.1016/0012-1606(86)90178-8. [DOI] [PubMed] [Google Scholar]
  19. Jacobson A., Firtel R. A., Lodish H. F. Synthesis of messenger and ribosomal RNA precursors in isolated nuclei of the cellular slime mold Dictyostelium discoideum. J Mol Biol. 1974 Jan 15;82(2):213–230. doi: 10.1016/0022-2836(74)90342-8. [DOI] [PubMed] [Google Scholar]
  20. Kimmel A. R. Different molecular mechanisms for cAMP regulation of gene expression during Dictyostelium development. Dev Biol. 1987 Jul;122(1):163–171. doi: 10.1016/0012-1606(87)90342-3. [DOI] [PubMed] [Google Scholar]
  21. Kimmel A. R., Firtel R. A. Sequence organization in Dictyostelium: unique structure at the 5'-ends of protein coding genes. Nucleic Acids Res. 1983 Jan 25;11(2):541–552. doi: 10.1093/nar/11.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Klein P., Vaughan R., Borleis J., Devreotes P. The surface cyclic AMP receptor in Dictyostelium. Levels of ligand-induced phosphorylation, solubilization, identification of primary transcript, and developmental regulation of expression. J Biol Chem. 1987 Jan 5;262(1):358–364. [PubMed] [Google Scholar]
  23. Knecht D. A., Loomis W. F. Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science. 1987 May 29;236(4805):1081–1086. doi: 10.1126/science.3576221. [DOI] [PubMed] [Google Scholar]
  24. Kochan J., Perkins M., Ravetch J. V. A tandemly repeated sequence determines the binding domain for an erythrocyte receptor binding protein of P. falciparum. Cell. 1986 Mar 14;44(5):689–696. doi: 10.1016/0092-8674(86)90834-2. [DOI] [PubMed] [Google Scholar]
  25. Lacombe M. L., Podgorski G. J., Franke J., Kessin R. H. Molecular cloning and developmental expression of the cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum. J Biol Chem. 1986 Dec 25;261(36):16811–16817. [PubMed] [Google Scholar]
  26. Landfear S. M., Lefebvre P., Chung S., Lodish H. F. Transcriptional control of gene expression during development of Dictyostelium discoideum. Mol Cell Biol. 1982 Nov;2(11):1417–1426. doi: 10.1128/mcb.2.11.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Landfear S. M., Lodish H. F. A role for cyclic AMP in expression of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1044–1048. doi: 10.1073/pnas.77.2.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mangiarotti G., Giorda R., Ceccarelli A., Perlo C. mRNA stabilization controls the expression of a class of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5786–5790. doi: 10.1073/pnas.82.17.5786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Maniak M., Nellen W. A developmentally regulated membrane protein gene in Dictyostelium discoideum is also induced by heat shock and cold shock. Mol Cell Biol. 1988 Jan;8(1):153–159. doi: 10.1128/mcb.8.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. McRobbie S. J., Tilly R., Blight K., Ceccarelli A., Williams J. G. Identification and localization of proteins encoded by two DIF-inducible genes of Dictyostelium. Dev Biol. 1988 Jan;125(1):59–63. doi: 10.1016/0012-1606(88)90058-9. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Muskavitch M. A., Hogness D. S. An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell. 1982 Jul;29(3):1041–1051. doi: 10.1016/0092-8674(82)90467-6. [DOI] [PubMed] [Google Scholar]
  34. Nellen W., Datta S., Reymond C., Sivertsen A., Mann S., Crowley T., Firtel R. A. Molecular biology in Dictyostelium: tools and applications. Methods Cell Biol. 1987;28:67–100. doi: 10.1016/s0091-679x(08)61637-4. [DOI] [PubMed] [Google Scholar]
  35. Oyama M., Blumberg D. D. Interaction of cAMP with the cell-surface receptor induces cell-type-specific mRNA accumulation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4819–4823. doi: 10.1073/pnas.83.13.4819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ozaki L. S., Svec P., Nussenzweig R. S., Nussenzweig V., Godson G. N. Structure of the plasmodium knowlesi gene coding for the circumsporozoite protein. Cell. 1983 Oct;34(3):815–822. doi: 10.1016/0092-8674(83)90538-x. [DOI] [PubMed] [Google Scholar]
  37. Pavlovic J., Haribabu B., Dottin R. P. Transmembrane signal transduction regulates gene expression in Dictyostelium discoideum. Dev Genet. 1988;9(4-5):371–382. doi: 10.1002/dvg.1020090418. [DOI] [PubMed] [Google Scholar]
  38. Pears C. J., Mahbubani H. M., Williams J. G. Characterization of two highly diverged but developmentally co-regulated cysteine proteinase genes in Dictyostelium discoideum. Nucleic Acids Res. 1985 Dec 20;13(24):8853–8866. doi: 10.1093/nar/13.24.8853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ragheb J. A., Dottin R. P. Structure and sequence of a UDP glucose pyrophosphorylase gene of Dictyostelium discoideum. Nucleic Acids Res. 1987 May 11;15(9):3891–3906. doi: 10.1093/nar/15.9.3891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Schaap P., van Driel R. V. Induction of post-aggregative differentiation in Dictyostelium discoideum by cAMP. Evidence of involvement of the cell surface cAMP receptor. Exp Cell Res. 1985 Aug;159(2):388–398. doi: 10.1016/s0014-4827(85)80012-4. [DOI] [PubMed] [Google Scholar]
  42. Schwarzbauer J. E., Tamkun J. W., Lemischka I. R., Hynes R. O. Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell. 1983 Dec;35(2 Pt 1):421–431. doi: 10.1016/0092-8674(83)90175-7. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Williams J. G., Tsang A. S., Mahbubani H. A change in the rate of transcription of a eukaryotic gene in response to cyclic AMP. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7171–7175. doi: 10.1073/pnas.77.12.7171. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES