Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Jul;83(13):4819–4823. doi: 10.1073/pnas.83.13.4819

Interaction of cAMP with the cell-surface receptor induces cell-type-specific mRNA accumulation in Dictyostelium discoideum.

M Oyama, D D Blumberg
PMCID: PMC323833  PMID: 3014512

Abstract

The accumulation of many postaggregative mRNA species in Dictyostelium discoideum is dependent upon the continuous presence of elevated levels of cAMP. We have analyzed the cyclic nucleotide specificity of this requirement and show that it is similar to that of the cell-surface receptor and distinct from the specificity displayed by the cAMP-dependent protein kinase. The same specificity is displayed for the accumulation of two classes of prespore mRNAs (class I, early; class II, late) and a prestalk mRNA and for the shutoff of a growth-phase mRNA. Under conditions in which cAMP phosphodiesterase activity is competitively inhibited, half-maximal accumulation of prestalk mRNA can be obtained at cAMP concentrations of 320-520 nM, whereas a higher concentration, 1-2 microM, is required for half-maximal accumulation of the prespore mRNAs and shutoff of the growth-phase mRNA. These effects of cAMP and its analogues on gene expression have been obtained under conditions in which cAMP-mediated activation of adenylate cyclase is completely inhibited. We conclude that cAMP acts to stimulate postaggregative gene expression by interacting at the cell-surface receptor.

Full text

PDF
4819

Images in this article

4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821
4821Image
on p.4821

Selected References

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

  1. Abe K., Yanagisawa K. A new class of rapidly developing mutants in Dictyostelium discoideum: implications for cyclic AMP metabolism and cell differentiation. Dev Biol. 1983 Jan;95(1):200–210. doi: 10.1016/0012-1606(83)90018-0. [DOI] [PubMed] [Google Scholar]
  2. Barklis E., Lodish H. F. Regulation of dictyostelium discoideum mRNAs specific for prespore or prestalk cells. Cell. 1983 Apr;32(4):1139–1148. doi: 10.1016/0092-8674(83)90297-0. [DOI] [PubMed] [Google Scholar]
  3. Chang Y. Y. Cyclic 3',5'-adenosine monophosphate phosphodiesterase produced by the slime mold Dictyostelium discoideum. Science. 1968 Jul 5;161(3836):57–59. doi: 10.1126/science.161.3836.57. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chung S., Landfear S. M., Blumberg D. D., Cohen N. S., Lodish H. F. Synthesis and stability of developmentally regulated dictyostelium mRNAs are affected by cell--cell contact and cAMP. Cell. 1981 Jun;24(3):785–797. doi: 10.1016/0092-8674(81)90104-5. [DOI] [PubMed] [Google Scholar]
  6. Darmon M., Brachet P., Da Silva L. H. Chemotactic signals induce cell differentiation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3163–3166. doi: 10.1073/pnas.72.8.3163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Darmon M., Klein C. Effects of amino acids and glucose on adenylate cyclase and cell differentiation of Dictyostelium discoideum. Dev Biol. 1978 Apr;63(2):377–389. doi: 10.1016/0012-1606(78)90142-2. [DOI] [PubMed] [Google Scholar]
  8. Devreotes P. N., Steck T. L. Cyclic 3',5' AMP relay in Dictyostelium discoideum. II. Requirements for the initiation and termination of the response. J Cell Biol. 1979 Feb;80(2):300–309. doi: 10.1083/jcb.80.2.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gerisch G., Fromm H., Huesgen A., Wick U. Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells. Nature. 1975 Jun 12;255(5509):547–549. doi: 10.1038/255547a0. [DOI] [PubMed] [Google Scholar]
  10. Gunzburg J., Veron M. A cAMP-dependent protein kinase is present in differentiating Dictyostelium discoideum cells. EMBO J. 1982;1(9):1063–1068. doi: 10.1002/j.1460-2075.1982.tb01297.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hohman R. J., Guitton M. C., Veron M. Inactivation of S-adenosyl-L-homocysteine hydrolase by cAMP results from dissociation of enzyme-bound NAD+. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4578–4581. doi: 10.1073/pnas.82.14.4578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Juliani M. H., Brusca J., Klein C. cAMP regulation of cell differentiation in Dictyostelium discoideum and the role of the cAMP receptor. Dev Biol. 1981 Apr 15;83(1):114–121. doi: 10.1016/s0012-1606(81)80013-9. [DOI] [PubMed] [Google Scholar]
  13. Klein C., Juliani M. H. cAMP,-induced changes in cAMP-binding sites on D; discoideum amebae. Cell. 1977 Feb;10(2):329–335. doi: 10.1016/0092-8674(77)90227-6. [DOI] [PubMed] [Google Scholar]
  14. Leichtling B. H., Spitz E., Rickenberg H. V. A cAMP-binding protein from Dictyostelium discoideum regulates mammalian protein kinase. Biochem Biophys Res Commun. 1981 May 29;100(2):515–522. doi: 10.1016/s0006-291x(81)80207-0. [DOI] [PubMed] [Google Scholar]
  15. 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. doi: 10.1111/j.1432-1033.1972.tb01894.x. [DOI] [PubMed] [Google Scholar]
  16. Mato J. M., Krens F. A., van Haastert P. J., Konijn T. M. 3':5'-cyclic AMP-dependent 3':5'-cyclic GMP accumulation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2348–2351. doi: 10.1073/pnas.74.6.2348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Nandini-Kishore S. G., Frazier W. A. [3H]Methotrexate as a ligand for the folate receptor of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7299–7303. doi: 10.1073/pnas.78.12.7299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Oyama M., Okamoto K., Takeuchi I. Effects of cyclic AMP on contact formation and differentiation in Dictyostelium discoideum. J Cell Sci. 1982 Aug;56:223–232. doi: 10.1242/jcs.56.1.223. [DOI] [PubMed] [Google Scholar]
  20. Pan P., Hall E. M., Bonner J. T. Folic acid as second chemotactic substance in the cellular slime moulds. Nat New Biol. 1972 Jun 7;237(75):181–182. doi: 10.1038/newbio237181a0. [DOI] [PubMed] [Google Scholar]
  21. Sampson J., Town C., Gross J. Cyclic AMP and the control of aggregative phase gene expression in Dictyostelium discoideum. Dev Biol. 1978 Nov;67(1):54–64. doi: 10.1016/0012-1606(78)90299-3. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Theibert A., Klein P., Devreotes P. N. Specific photoaffinity labeling of the cAMP surface receptor in Dictyostelium discoideum. J Biol Chem. 1984 Oct 25;259(20):12318–12321. [PubMed] [Google Scholar]
  24. Tomchik K. J., Devreotes P. N. Adenosine 3',5'-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution--fluorography. Science. 1981 Apr 24;212(4493):443–446. doi: 10.1126/science.6259734. [DOI] [PubMed] [Google Scholar]
  25. Van Haastert P. J., De Wit R. J. Demonstration of receptor heterogeneity and affinity modulation by nonequilibrium binding experiments. The cell surface cAMP receptor of Dictyostelium discoideum. J Biol Chem. 1984 Nov 10;259(21):13321–13328. [PubMed] [Google Scholar]
  26. Van Haastert P. J., Kien E. Binding of cAMP derivatives to Dictyostelium discoideum cells. Activation mechanism of the cell surface cAMP receptor. J Biol Chem. 1983 Aug 25;258(16):9636–9642. [PubMed] [Google Scholar]
  27. de Wit R. J., Hekstra D., Jastorff B., Stec W. J., Baraniak J., Van Driel R., Van Haastert P. J. Inhibitory action of certain cyclophosphate derivatives of cAMP on cAMP-dependent protein kinases. Eur J Biochem. 1984 Jul 16;142(2):255–260. doi: 10.1111/j.1432-1033.1984.tb08279.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES