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. 1987 Feb;84(4):1030–1034. doi: 10.1073/pnas.84.4.1030

Superinduction of the Dictyostelium discoideum cell surface cAMP receptor by pulses of cAMP.

R L Chisholm, S Hopkinson, H F Lodish
PMCID: PMC304355  PMID: 3547400

Abstract

Extracellular cAMP plays a crucial role in regulating the developmental program of Dictyostelium discoideum, functioning as a chemotactic agent, as well as a signal that regulates expression of developmentally expressed genes. These activities appear to be mediated by a cell-surface receptor for cAMP. We have studied the regulation of this receptor in cells developed in starved suspension cultures exposed to 50 nM pulses of cAMP every 6 min. cAMP-pulsed cells display roughly 10-fold higher cAMP receptor levels than cells that developed on filters or that were starved in suspension without cAMP pulses. Based on saturation binding analysis, the superinduced binding activity represents an increase in receptor number, while receptor affinity for cAMP is unaffected. Photoaffinity labeling of superinduced cells results in specific labeling of the same molecules that are labeled in starved cells. This increased cAMP binding activity was also detected in membrane preparations from cAMP-pulsed cells. These results provide evidence for an unusual mode of receptor regulation: autogenous induction of the receptor by its ligand.

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Selected References

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  1. Alcantara F., Monk M. Signal propagation during aggregation in the slime mould Dictyostelium discoideum. J Gen Microbiol. 1974 Dec;85(2):321–334. doi: 10.1099/00221287-85-2-321. [DOI] [PubMed] [Google Scholar]
  2. Blumberg D. D., Lodish H. F. Changes in the messenger RNA population during differentiation of dictyostelium discoideum. Dev Biol. 1980 Aug;78(2):285–300. doi: 10.1016/0012-1606(80)90337-1. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Gerisch G., Wick U. Intracellular oscillations and release of cyclic AMP from Dictyostelium cells. Biochem Biophys Res Commun. 1975 Jul 8;65(1):364–370. doi: 10.1016/s0006-291x(75)80102-1. [DOI] [PubMed] [Google Scholar]
  5. Green A. A., Newell P. C. Evidence for the existence of two types of cAMP binding sites in aggregating cells of Dictyostelium discoideum. Cell. 1975 Oct;6(2):129–136. doi: 10.1016/0092-8674(75)90003-3. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Henderson E. J. The cyclic adenosine 3':5'-monophosphate receptor of Dictyostelium discoideum. Binding characteristics of aggregation-competent cells and variation of binding levels during the life cycle. J Biol Chem. 1975 Jun 25;250(12):4730–4736. [PubMed] [Google Scholar]
  9. Hutchins B. L., Frazier W. A. Purification and characterization of a membrane-associated cAMP-binding protein from developing Dictyostelium discoideum. J Biol Chem. 1984 Apr 10;259(7):4379–4388. [PubMed] [Google Scholar]
  10. Juliani M. H., Klein C. Photoaffinity labeling of the cell surface adenosine 3':5'-monophosphate receptor of Dictyostelium discoideum and its modification in down-regulated cells. J Biol Chem. 1981 Jan 25;256(2):613–619. [PubMed] [Google Scholar]
  11. King A. C., Frazier W. A. Properties of the oscillatory cAMP binding component of Dictyostelium discoideum cells and isolated plasma membranes. J Biol Chem. 1979 Aug 10;254(15):7168–7176. [PubMed] [Google Scholar]
  12. Klein C. Binding of adenosine 3':5'-monophosphate to plasma membranes of Dictyostelium discoideum amoebae. J Biol Chem. 1981 Oct 10;256(19):10050–10053. [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. Konijn T. M., van de Meene J. G., Chang Y. Y., Barkley D. S., Bonner J. T. Identification of adenosine-3',5'-monophosphate as the bacterial attractant for myxamoebae of Dictyostelium discoideum. J Bacteriol. 1969 Aug;99(2):510–512. doi: 10.1128/jb.99.2.510-512.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mato J. M., Jastorff B., Morr M., Konijn T. M. A model for cyclic AMP-chemoreceptor interaction in Dictyostelium discoideum. Biochim Biophys Acta. 1978 Dec 1;544(2):309–314. doi: 10.1016/0304-4165(78)90099-5. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Mullens I. A., Newell P. C. cAMP binding to cell surface receptors of Dictyostelium. Differentiation. 1978 May 26;10(3):171–176. doi: 10.1111/j.1432-0436.1978.tb00960.x. [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., 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]
  20. Shaffer B. M. Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mould Dictyostelium discoideum. Nature. 1975 Jun 12;255(5509):549–552. doi: 10.1038/255549a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Wallace L. J., Frazier W. A. Photoaffinity labeling of cyclic-AMP- and AMP-binding proteins differentiating Dictyostelium discoideum cells. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4250–4254. doi: 10.1073/pnas.76.9.4250. [DOI] [PMC free article] [PubMed] [Google Scholar]

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