Home LiteratureArticle Details
PMID: 2779573 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs.

Molecular and cellular biology ·Vol. 9 ·No. 9 ·1989-09-00 ·Pages 3938-50

Podgorski GJ, Franke J, Faure M, Kessin RH

Abstract

The cyclic nucleotide phosphodiesterase (phosphodiesterase) gene plays essential roles in the development of Dictyostelium discoideum during cellular aggregation and postaggregation morphogenesis. Genomic clones spanning the gene were isolated and used to determine the sequence and structure of the phosphodiesterase gene. We found an unusually complex organization for a gene of D. discoideum. Two transcripts of 2.4 and 1.9 kilobases (kb) were synthesized from start sites separated by 1.1 kb. A developmentally regulated promoter was utilized for the 2.4-kb mRNA, and a constitutive promoter regulated synthesis of the 1.9-kb transcript. The gene was found to be divided into four exons that are alternately spliced to give rise to the two mRNAs. The precursor of the 2.4-kb mRNA contained a 2.3-kb intron, whereas the precursor of the constitutive transcript was synthesized with a 1.7-kb intron. The two transcripts contained identical protein-coding regions and 400-nucleotide 3' untranslated sequences. The 2.4-kb developmentally regulated mRNA was distinguished by a long 5' untranslated leader of 666 nucleotides. The complex structure of the gene may allow multiple levels of control of the expression of the phosphodiesterase during development.

MeSH Terms
Base Sequence Calmodulin/genetics DNA/genetics Dictyostelium/enzymology,genetics Genes, Fungal Molecular Sequence Data Promoter Regions, Genetic RNA Splicing RNA, Fungal/biosynthesis,genetics RNA, Messenger/biosynthesis,genetics Restriction Mapping Transcription, Genetic
Chemicals
Calmodulin RNA, Fungal RNA, Messenger DNA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Podgorski G J
Department of Anatomy and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, New York 10032.
Franke J
Faure M
Kessin R H
References (62)
62 references, click to expand
  1. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA.
    Plasmid. 1985 Jan;13(1):31-40 PMID: 3991809
  2. Structure of the promoter of the Dictyostelium discoideum prespore EB4 gene.
    Mol Cell Biol. 1985 Jun;5(6):1465-72 PMID: 3897836
  3. Regulation and function of G alpha protein subunits in Dictyostelium.
    Cell. 1989 Apr 21;57(2):265-75 PMID: 2539262
  4. 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):458-69 PMID: 3031475
  5. Cyclic 3',5'-AMP relay in Dictyostelium discoideum IV. Recovery of the cAMP signaling response after adaptation to cAMP.
    J Cell Biol. 1980 Aug;86(2):545-53 PMID: 6249826
  6. Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells.
    Nature. 1975 Jun 12;255(5509):547-9 PMID: 167285
  7. Dictyostelium discoideum myosin: isolation and characterization of cDNAs encoding the essential light chain.
    Mol Cell Biol. 1988 Feb;8(2):794-801 PMID: 2451126
  8. Organization of a gene family developmentally regulated during Dictyostelium discoideum spore germination.
    J Mol Biol. 1989 Jan 5;205(1):63-9 PMID: 2926809
  9. Developmental regulation of a Dictyostelium gene encoding a protein homologous to mammalian ras protein.
    Cell. 1984 Nov;39(1):141-8 PMID: 6091907
  10. Conserved structural features are found upstream from the three co-ordinately regulated discoidin I genes of Dictyostelium discoideum.
    J Mol Biol. 1984 Jan 15;172(2):203-20 PMID: 6694210
  11. Molecular cloning and developmental expression of the cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum.
    J Biol Chem. 1986 Dec 25;261(36):16811-7 PMID: 3023365
  12. Organization of the Dictyostelium discoideum actin multigene family. Flanking sequences show subfamily homologies and unusual dyad symmetries.
    J Mol Biol. 1985 Jun 5;183(3):311-26 PMID: 2991530
  13. Structure and sequence of a UDP glucose pyrophosphorylase gene of Dictyostelium discoideum.
    Nucleic Acids Res. 1987 May 11;15(9):3891-906 PMID: 3035502
  14. Sequence organization in Dictyostelium: unique structure at the 5'-ends of protein coding genes.
    Nucleic Acids Res. 1983 Jan 25;11(2):541-52 PMID: 6828377
  15. pdsA, a gene involved in the production of active phosphodiesterase during starvation of Dictyostelium discoideum amoebae.
    Mol Gen Genet. 1980;177(4):607-13 PMID: 6247610
  16. Regulatory sequences in the promoter of the Dictyostelium Actin 6 gene.
    EMBO J. 1986 Dec 1;5(12):3367-72 PMID: 3816763
  17. Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system.
    Mol Cell Biol. 1988 Apr;8(4):1697-708 PMID: 3380094
  18. A developmentally regulated cysteine proteinase in Dictyostelium discoideum.
    EMBO J. 1985 Apr;4(4):999-1006 PMID: 2990918
  19. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  20. Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium.
    Annu Rev Biochem. 1987;56:853-79 PMID: 3039908
  21. 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):361-74 PMID: 212334
  22. Isolation of developmentally regulated genes.
    Methods Cell Biol. 1987;28:461-70 PMID: 3600416
  23. Sequence rearrangement and duplication of double stranded fibronectin cDNA probably occurring during cDNA synthesis by AMV reverse transcriptase and Escherichia coli DNA polymerase I.
    Nucleic Acids Res. 1980 Jul 11;8(13):3055-64 PMID: 6159581
  24. Rescue of a Dictyostelium discoideum mutant defective in cyclic nucleotide phosphodiesterase.
    Dev Biol. 1989 Feb;131(2):366-72 PMID: 2536338
  25. Isolation of a cDNA encoding a portion of the cyclic nucleotide phosphodiesterase of Dictyostelium discoideum.
    J Gen Microbiol. 1986 Apr;132(4):1043-50 PMID: 3020155
  26. Molecular mechanisms of nucleotide-sequence rearrangements in cDNA clones of human fibroblast interferon mRNA.
    Gene. 1981 Nov;15(2-3):215-23 PMID: 6170541
  27. The expression of two transcripts of the phosphodiesterase gene during the development of Dictyostelium discoideum.
    Dev Biol. 1987 Dec;124(2):504-11 PMID: 2824253
  28. Sequence analysis of a Dictyostelium discoideum gene coding for an active dihydroorotate dehydrogenase in yeast.
    Biochimie. 1985 Jun;67(6):583-8 PMID: 2996629
  29. Genetics of early Dictyostelium discoideum development.
    Microbiol Rev. 1988 Mar;52(1):29-49 PMID: 2832716
  30. Molecular characterization of a Dictyostelium discoideum gene encoding a multifunctional enzyme of the pyrimidine pathway.
    Eur J Biochem. 1989 Feb 1;179(2):345-58 PMID: 2917570
  31. A catalogue of splice junction sequences.
    Nucleic Acids Res. 1982 Jan 22;10(2):459-72 PMID: 7063411
  32. Nucleotide-sequence heterogeneity and sequence rearrangements in influenza virus cDNA.
    Gene. 1981 Nov;15(2-3):207-14 PMID: 6895362
  33. Interactions between adenosine and oscillatory cAMP signaling regulate size and pattern in Dictyostelium.
    Cell. 1986 Apr 11;45(1):137-44 PMID: 3006924
  34. Leader length and secondary structure modulate mRNA function under conditions of stress.
    Mol Cell Biol. 1988 Jul;8(7):2737-44 PMID: 3405216
  35. The complete sequence of the mouse skeletal alpha-actin gene reveals several conserved and inverted repeat sequences outside of the protein-coding region.
    Mol Cell Biol. 1986 Jan;6(1):15-25 PMID: 3023820
  36. A defined minimal medium for axenic strains of Dictyostelium discoideum.
    Proc Natl Acad Sci U S A. 1977 May;74(5):2157-61 PMID: 17120
  37. Structure of two developmentally regulated Dictyostelium discoideum ubiquitin genes.
    Mol Cell Biol. 1987 Jun;7(6):2097-103 PMID: 3037345
  38. 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):153-9 PMID: 3336356
  39. Disruption of Dictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8076-80 PMID: 2847151
  40. Characterization of two highly diverged but developmentally co-regulated cysteine proteinase genes in Dictyostelium discoideum.
    Nucleic Acids Res. 1985 Dec 20;13(24):8853-66 PMID: 3909109
  41. cAMP,-induced changes in cAMP-binding sites on D; discoideum amebae.
    Cell. 1977 Feb;10(2):329-35 PMID: 189939
  42. Two-phase regulatory pathway controls cAMP receptor-mediated expression of early genes in Dictyostelium.
    Proc Natl Acad Sci U S A. 1989 Mar;86(6):1924-8 PMID: 2538821
  43. Inheritance of extrachromosomal ribosomal DNA during the asexual life cycle of Dictyostelium discoideum: examination by use of DNA polymorphisms.
    Mol Cell Biol. 1985 Feb;5(2):273-80 PMID: 2983186
  44. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia.
    Science. 1989 Jan 6;243(4887):75-7 PMID: 2911720
  45. Nucleotide sequence and characterization of the transcript of a Dictyostelium ribosomal protein gene.
    Nucleic Acids Res. 1987 Dec 23;15(24):10285-98 PMID: 2827119
  46. 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 PMID: 2461560
  47. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs.
    Nucleic Acids Res. 1987 Oct 26;15(20):8125-48 PMID: 3313277
  48. Studies on the transcription, translation, and structure of alpha-actinin in Dictyostelium discoideum.
    J Cell Biol. 1986 Sep;103(3):969-75 PMID: 3745276
  49. Two divergently transcribed genes of Dictyostelium discoideum are cyclic AMP-inducible and coregulated during development.
    Mol Cell Biol. 1987 Dec;7(12):4482-9 PMID: 2830496
  50. The role of diffusible molecules in regulating the cellular differentiation of Dictyostelium discoideum.
    Development. 1988 May;103(1):1-16 PMID: 2848678
  51. 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 PMID: 2897942
  52. Structural and functional characterization of a Dictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence.
    Nucleic Acids Res. 1987 Sep 25;15(18):7463-76 PMID: 3658700
  53. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination.
    Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963-5 PMID: 6575390
  54. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences.
    Nature. 1988 Nov 24;336(6197):396-9 PMID: 3194021
  55. Molecular basis of transmembrane signal transduction in Dictyostelium discoideum.
    Microbiol Rev. 1987 Dec;51(4):396-418 PMID: 2893972
  56. Multiple copies of a G-rich element upstream of a cAMP-inducible Dictyostelium gene are necessary but not sufficient for efficient gene expression.
    Nucleic Acids Res. 1988 Sep 12;16(17):8467-86 PMID: 2843819
  57. 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 PMID: 16453747
  58. Nucleotide sequences of adenovirus DNAs.
    Curr Top Microbiol Immunol. 1984;110:73-142 PMID: 6383725
  59. 3' non-coding region sequences in eukaryotic messenger RNA.
    Nature. 1976 Sep 16;263(5574):211-4 PMID: 822353
  60. Sequence analysis of the DdPYR5-6 gene coding for UMP synthase in Dictyostelium discoideum and comparison with orotate phosphoribosyl transferases and OMP decarboxylases.
    Mol Gen Genet. 1988 Mar;211(3):441-5 PMID: 2835631
  61. Structural characterization of Dictyostelium discoideum prespore-specific gene D19 and of its product, cell surface glycoprotein PsA.
    Mol Cell Biol. 1988 Aug;8(8):3458-66 PMID: 2850494
  62. Structure of the Dictyostelium discoideum prestalk D11 gene and protein.
    Mol Cell Biol. 1985 Jun;5(6):1473-9 PMID: 4033661
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.9.9.3938-3950.1989
Published
1989-09-00
Pages
3938-50
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC362456
Subset
IM
Grants
NIGMS NIH HHS · GM10174 · United States
NIGMS NIH HHS · GM33136 · United States
Databases
GENBANK
M23449
External Links
PubMed source DOI: 10.1128/mcb.9.9.3938-3950.1989 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2