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Mol Cell Biol. May 1990; 10(5): 1921–1930.
PMCID: PMC360538

The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development.

Abstract

The cyclic nucleotide phosphodiesterase (phosphodiesterase) plays essential roles throughout the development of Dictyostelium discoideum. It is crucial to cellular aggregation and to postaggregation morphogenesis. The phosphodiesterase gene is transcribed into three mRNAs, containing the same coding sequence connected to different 5' untranslated sequences, that accumulate at different times during the life cycle. A 1.9-kilobase (kb) mRNA is specific for growth, a 2.4-kb mRNA is specific for aggregation, and a 2.2-kb mRNA is specific for late development and is only expressed in prestalk cells. Hybridization of RNA isolated from cells at various stages of development with different upstream regions of the gene indicated separate promoters for each of the three mRNAs. The existence of specific promoters was confirmed by fusing the three putative promoter regions to the chloramphenicol acetyltransferase reporter gene, and the analysis of transformants containing these constructs. The three promoters are scattered within a 4.1-kilobase pair (kbp) region upstream of the initiation codon. The late promoter is proximal to the coding sequence, the growth-specific promoter has an initiation site that is 1.9 kbp upstream of the ATG codon, and the aggregation-specific promoter has an initiation site 3 kbp upstream.

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Selected References

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  • Barklis E, Lodish HF. Regulation of dictyostelium discoideum mRNAs specific for prespore or prestalk cells. Cell. 1983 Apr;32(4):1139–1148. [PubMed]
  • Barra J, Barrand P, Blondelet MH, Brachet P. pdsA, a gene involved in the production of active phosphodiesterase during starvation of Dictyostelium discoideum amoebae. Mol Gen Genet. 1980;177(4):607–613. [PubMed]
  • Darmon M, Barra J, Brachet P. The role of phosphodiesterase in aggregation of Dictyostelium discoideum. J Cell Sci. 1978 Jun;31:233–243. [PubMed]
  • Davis RL, Davidson N. The memory gene dunce+ encodes a remarkable set of RNAs with internal heterogeneity. Mol Cell Biol. 1986 May;6(5):1464–1470. [PMC free article] [PubMed]
  • Devreotes P. Dictyostelium discoideum: a model system for cell-cell interactions in development. Science. 1989 Sep 8;245(4922):1054–1058. [PubMed]
  • de Wit RJ, Konijn TM. Identification of the acrasin of Dictyostelium minutum as a derivative of folic acid. Cell Differ. 1983 Apr;12(4):205–210. [PubMed]
  • Early AE, Williams JG. Two vectors which facilitate gene manipulation and a simplified transformation procedure for Dictyostelium discoideum. Gene. 1987;59(1):99–106. [PubMed]
  • Faure M, Podgorski GJ, Franke J, Kessin RH. Disruption of Dictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8076–8080. [PMC free article] [PubMed]
  • Faure M, Podgorski GJ, Franke J, Kessin RH. Rescue of a Dictyostelium discoideum mutant defective in cyclic nucleotide phosphodiesterase. Dev Biol. 1989 Feb;131(2):366–372. [PubMed]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed]
  • Firtel RA, van Haastert PJ, Kimmel AR, Devreotes PN. G protein linked signal transduction pathways in development: dictyostelium as an experimental system. Cell. 1989 Jul 28;58(2):235–239. [PubMed]
  • Franke J, Kessin R. A defined minimal medium for axenic strains of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1977 May;74(5):2157–2161. [PMC free article] [PubMed]
  • Franke J, Kessin RH. The cyclic nucleotide phosphodiesterase inhibitory protein of Dictyostelium discoideum. Purification and characterization. J Biol Chem. 1981 Jul 25;256(14):7628–7637. [PubMed]
  • Frohman MA, Dush MK, Martin GR. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. [PMC free article] [PubMed]
  • Gerisch G. Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium. Annu Rev Biochem. 1987;56:853–879. [PubMed]
  • Gorman CM, Moffat LF, Howard BH. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. [PMC free article] [PubMed]
  • Janssens PM, Van Haastert PJ. Molecular basis of transmembrane signal transduction in Dictyostelium discoideum. Microbiol Rev. 1987 Dec;51(4):396–418. [PMC free article] [PubMed]
  • Kay RR, Dhokia B, Jermyn KA. Purification of stalk-cell-inducing morphogens from Dictyostelium discoideum. Eur J Biochem. 1983 Oct 17;136(1):51–56. [PubMed]
  • Kesbeke F, Snaar-Jagalska BE, Van Haastert PJ. Signal transduction in Dictyostelium fgd A mutants with a defective interaction between surface cAMP receptors and a GTP-binding regulatory protein. J Cell Biol. 1988 Aug;107(2):521–528. [PMC free article] [PubMed]
  • Kessin RH. Genetics of early Dictyostelium discoideum development. Microbiol Rev. 1988 Mar;52(1):29–49. [PMC free article] [PubMed]
  • Kimmel AR, Firtel RA. Sequence organization in Dictyostelium: unique structure at the 5'-ends of protein coding genes. Nucleic Acids Res. 1983 Jan 25;11(2):541–552. [PMC free article] [PubMed]
  • Klein C, Juliani MH. cAMP,-induced changes in cAMP-binding sites on D; discoideum amebae. Cell. 1977 Feb;10(2):329–335. [PubMed]
  • Kozak M. Leader length and secondary structure modulate mRNA function under conditions of stress. Mol Cell Biol. 1988 Jul;8(7):2737–2744. [PMC free article] [PubMed]
  • Kumagai A, Pupillo M, Gundersen R, Miake-Lye R, Devreotes PN, Firtel RA. Regulation and function of G alpha protein subunits in Dictyostelium. Cell. 1989 Apr 21;57(2):265–275. [PubMed]
  • Lacombe ML, Podgorski GJ, Franke J, Kessin RH. 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]
  • Luo XC, Park K, Lopez-Casillas F, Kim KH. Structural features of the acetyl-CoA carboxylase gene: mechanisms for the generation of mRNAs with 5' end heterogeneity. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4042–4046. [PMC free article] [PubMed]
  • Malchow D, Nägele B, Schwarz H, Gerisch G. Membrane-bound cyclic AMP phosphodiesterase in chemotactically responding cells of Dictyostelium discoideum. Eur J Biochem. 1972 Jun 23;28(1):136–142. [PubMed]
  • May T, Kern H, Müller-Taubenberger A, Nellen W. Identification of a cis-acting element controlling induction of early gene expression in Dictyostelium discoideum. Mol Cell Biol. 1989 Nov;9(11):4653–4659. [PMC free article] [PubMed]
  • Morris HR, Taylor GW, Masento MS, Jermyn KA, Kay RR. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. Nature. 328(6133):811–814. [PubMed]
  • Nellen W, Datta S, Reymond C, Sivertsen A, Mann S, Crowley T, Firtel RA. Molecular biology in Dictyostelium: tools and applications. Methods Cell Biol. 1987;28:67–100. [PubMed]
  • Orlow SJ, Shapiro RI, Franke J, Kessin RH. The extracellular cyclic nucleotide phosphodiesterase of Dictyostelium discoideum. Purification and characterization. J Biol Chem. 1981 Jul 25;256(14):7620–7627. [PubMed]
  • Podgorski GJ, Franke J, Faure M, Kessin RH. The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs. Mol Cell Biol. 1989 Sep;9(9):3938–3950. [PMC free article] [PubMed]
  • Podgorski GJ, Franke J, Kessin RH. Isolation of a cDNA encoding a portion of the cyclic nucleotide phosphodiesterase of Dictyostelium discoideum. J Gen Microbiol. 1986 Apr;132(4):1043–1050. [PubMed]
  • Ratner D, Borth W. Comparison of differentiating Dictyostelium discoideum cell types separated by an improved method of density gradient centrifugation. Exp Cell Res. 1983 Jan;143(1):1–13. [PubMed]
  • Rossier C, Franke J, Mullens IA, Kelley KJ, Kessin RH. Detection and regulation of the mRNA for the inhibitor of extracellular cAMP phosphodiesterase of Dictyostelium discoideum. Eur J Biochem. 1983 Jun 15;133(2):383–391. [PubMed]
  • Brown SS, Rutherford CL. Localization of cyclic nucleotide phosphodiesterase in the multicellular stages of Dictyostelium discoideum. Differentiation. 1980 Jun;16(3):173–183. [PubMed]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [PubMed]
  • Schaap P, Konijn TM, van Haastert PJ. cAMP pulses coordinate morphogenetic movement during fruiting body formation of Dictyostelium minutum. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2122–2126. [PMC free article] [PubMed]
  • Schaap P, Wang M. The possible involvement of oscillatory cAMP signaling in multicellular morphogenesis of the cellular slime molds. Dev Biol. 1984 Oct;105(2):470–478. [PubMed]
  • Schaap P, Wang M. Interactions between adenosine and oscillatory cAMP signaling regulate size and pattern in Dictyostelium. Cell. 1986 Apr 11;45(1):137–144. [PubMed]
  • Shimomura O, Suthers HL, Bonner JT. Chemical identity of the acrasin of the cellular slime mold Polysphondylium violaceum. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7376–7379. [PMC free article] [PubMed]
  • Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. [PubMed]
  • Sussman M. Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol. 1987;28:9–29. [PubMed]
  • van Haastert PJ, De Wit RJ, Konijn TM. Antagonists of chemoattractants reveal separate receptors for cAMP, folic acid and pterin in Dictyostelium. Exp Cell Res. 1982 Aug;140(2):453–456. [PubMed]
  • Van Haastert PJ, Van der Heijden PR. Excitation, adaptation, and deadaptation of the cAMP-mediated cGMP response in Dictyostelium discoideum. J Cell Biol. 1983 Feb;96(2):347–353. [PMC free article] [PubMed]
  • Vaughan RA, Devreotes PN. Ligand-induced phosphorylation of the cAMP receptor from Dictyostelium discoideum. J Biol Chem. 1988 Oct 5;263(28):14538–14543. [PubMed]
  • Williams JG. The role of diffusible molecules in regulating the cellular differentiation of Dictyostelium discoideum. Development. 1988 May;103(1):1–16. [PubMed]
  • Yeh RP, Chan FK, Coukell MB. Independent regulation of the extracellular cyclic AMP phosphodiesterase-inhibitor system and membrane differentiation by exogenous cyclic AMP in Dictyostelium discoideum. Dev Biol. 1978 Oct;66(2):361–374. [PubMed]

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