Home LiteratureArticle Details
PMID: 3022299 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

cAMP induction of prespore and prestalk gene expression in Dictyostelium is mediated by the cell-surface cAMP receptor.

Gomer RH, Armstrong D, Leichtling BH, Firtel RA

Abstract

Extracellular adenosine 3',5'-cyclic monophosphate (cAMP) is required for cell-type-specific gene expression in developing Dictyostelium discoideum. We have developed a microassay for the expression of these genes, using antibodies directed against their protein products. To characterize the transduction mechanism, we have used in this assay cAMP analogues that preferentially activate either the cell-surface cAMP receptor or the internal cAMP-dependent protein kinase. N6-(aminohexyl) cAMP activates the Dictyostelium cAMP-dependent protein kinase but does not bind to the cell-surface cAMP receptor and does not cause cell-type-specific gene expression. 2'-Deoxy-cAMP does not activate the cAMP-dependent protein kinase but binds to the receptor and causes cell-type-specific gene expression. Cyclic AMP-induced accumulation of prestalk mRNA in shaking cultures still occurs in the presence of caffeine, which blocks the receptor-coupled activation of adenyl cyclase. This suggests that the extracellular cAMP induction of cell-type-specific gene expression in developing Dictyostelium cells is mediated by the cell-surface cAMP receptor and that activating adenyl cyclase by this receptor is not essential. Using the N6-(aminohexyl) cAMP to competitively inhibit phosphodiesterase, we show that 30 nM cAMP is sufficient to induce prestalk or prespore gene expression.

MeSH Terms
Caffeine/pharmacology Cell Differentiation Cyclic AMP/analogs & derivatives,pharmacology Dictyostelium/genetics Gene Expression Regulation/drug effects RNA, Messenger/biosynthesis Receptors, Cyclic AMP/physiology
Chemicals
RNA, Messenger Receptors, Cyclic AMP Caffeine Cyclic AMP
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gomer R H
Armstrong D
Leichtling B H
Firtel R A
References (27)
27 references, click to expand
  1. A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. II. Developmental regulation.
    J Biol Chem. 1984 Jan 10;259(1):662-8 PMID: 6323417
  2. Amplification of cyclic-AMP signals in aggregating cells of Dictyostelium discoideum.
    FEBS Lett. 1975 May 1;53(2):139-42 PMID: 166875
  3. A secreted factor and cyclic AMP jointly regulate cell-type-specific gene expression in Dictyostelium discoideum.
    Mol Cell Biol. 1985 Apr;5(4):705-13 PMID: 2985966
  4. cAMP regulation of cell differentiation in Dictyostelium discoideum and the role of the cAMP receptor.
    Dev Biol. 1981 Apr 15;83(1):114-21 PMID: 6263735
  5. Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells.
    Nature. 1975 Jun 12;255(5509):547-9 PMID: 167285
  6. Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mould Dictyostelium discoideum.
    Nature. 1975 Jun 12;255(5509):549-52 PMID: 167286
  7. The specificity of the cAMP receptor mediating activation of adenylate cyclase in Dictyostelium discoideum.
    Dev Biol. 1986 Apr;114(2):529-33 PMID: 3007244
  8. Investigations on stimulation of lac transcription in vivo in Escherichia coli by cAMP analogues. Biological activities and structure-activity correlations.
    Eur J Biochem. 1984 Jan 2;138(1):101-9 PMID: 6319129
  9. A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. I. Properties.
    J Biol Chem. 1984 Jan 10;259(1):654-61 PMID: 6706957
  10. 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):4819-23 PMID: 3014512
  11. Pharmacological characterization of cyclic AMP receptors mediating gene regulation in Dictyostelium discoideum.
    Mol Cell Biol. 1986 Jul;6(7):2402-8 PMID: 3023932
  12. Differential cellular distribution of cAMP-dependent protein kinase during development of Dictyostelium discoideum.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):2127-31 PMID: 16593449
  13. Effects of cyclic AMP pulses on adenylate cyclase and the phosphodiesterase inhibitor of D. discoideum.
    Nature. 1977 Jul 7;268(5615):76-8 PMID: 196203
  14. Binding of cAMP and adenosine derivatives to Dictyostelium discoideum cells. Relationships of binding, chemotactic, and antagonistic activities.
    J Biol Chem. 1983 Aug 25;258(16):9643-8 PMID: 6309779
  15. Aggregation in Dictyostelium discoideum.
    Cell. 1981 Jun;24(3):603-11 PMID: 6265098
  16. The relationship of phosphodiesterase to the developmental cycle of Dictyostelium discoideum.
    Biochem Biophys Res Commun. 1975 Nov 3;67(1):440-7 PMID: 173312
  17. Isolation and properties of cyclic AMP-dependent protein kinase from Dictyostelium discoideum.
    Biochim Biophys Acta. 1984 Jan 18;784(1):1-8 PMID: 6318830
  18. Phosphodiesterase induction in Dictyostelium discoideum by inhibition of extracellular phosphodiesterase activity.
    Dev Biol. 1982 Nov;94(1):240-5 PMID: 6295848
  19. Induction and modulation of cell-type-specific gene expression in Dictyostelium.
    Cell. 1983 Mar;32(3):763-71 PMID: 6299575
  20. Intracellular oscillations and release of cyclic AMP from Dictyostelium cells.
    Biochem Biophys Res Commun. 1975 Jul 8;65(1):364-70 PMID: 167769
  21. The regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum: cellular localization and developmental regulation analyzed by immunoblotting.
    Cell Differ. 1985 Nov;17(4):221-7 PMID: 3907861
  22. Caffeine blocks activation of cyclic AMP synthesis in Dictyostelium discoideum.
    Dev Biol. 1984 Jan;101(1):136-46 PMID: 6319207
  23. 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):388-98 PMID: 2993006
  24. Regulation of cell-type-specific gene expression in Dictyostelium.
    Cold Spring Harb Symp Quant Biol. 1985;50:801-12 PMID: 3868507
  25. Binding of cAMP derivatives to Dictyostelium discoideum cells. Activation mechanism of the cell surface cAMP receptor.
    J Biol Chem. 1983 Aug 25;258(16):9636-42 PMID: 6309778
  26. Regulation of dictyostelium discoideum mRNAs specific for prespore or prestalk cells.
    Cell. 1983 Apr;32(4):1139-48 PMID: 6301681
  27. The acrasin activity of adenosine-3',5'-cyclic phosphate.
    Proc Natl Acad Sci U S A. 1967 Sep;58(3):1152-4 PMID: 4861307
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1986-11-00
Pages
8624-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC386983
Subset
IM
Grants
NIGMS NIH HHS · GM24279 · United States
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: [email protected]