Skip to main content
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
. 1977 Apr;74(4):1543–1547. doi: 10.1073/pnas.74.4.1543

Unified mechanism for relay and oscillation of cyclic AMP in Dictyostelium discoideum.

A Goldbeter, L A Segel
PMCID: PMC430826  PMID: 193105

Abstract

A modified version of an allosteric model for adenylate cyclase [ATP pyrophosphate-lyase (cyclizing), EC 4.6.1.1] previously analyzed for sustained oscillations of adenosine 3':5'-cyclic monophosphate (cAMP) in Dictyostelium discoideum [Goldbeter, A. (1975) Nature 253, 540-542] is examined to see whether it can account for the relay of cAMP pulses. Oscillations occur around a nonequilibrium, unstable stationary state when system parameters are in a certain domain. It is found that relay can occur outside this domain, in a restricted set of parameter values for which the solution ultimately tends to a stable steady state. A suprathreshold level of extracellular cAMP is needed to elicit relay which consists in a pulsatory synthesis of intracellular cAMP. Theoretical predictions are compared with the results of experiments on cAMP relay and oscillation in aggregation-competent cells of D. discoideum. The model suggests an explanation for the emergence of aggregation centers and for a sequence of developmental events observed in interphase amoebae.

Full text

PDF
1547

Selected References

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

  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. Blumenthal R. Instabilities, oscillations and chemical waves in an oligomeric model for membrane transport. J Theor Biol. 1975 Jan;49(1):219–239. doi: 10.1016/s0022-5193(75)80030-0. [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. Cohen M. H., Robertson A. Wave propagation in the early stages of aggregation of cellular slime molds. J Theor Biol. 1971 Apr;31(1):101–118. doi: 10.1016/0022-5193(71)90124-x. [DOI] [PubMed] [Google Scholar]
  5. Cutler L. S., Rossomando E. F. Localization of adenylate cyclase in Dictyostelium discoideum. II. Cytochemical studies on whole cells and isolated plasma membrane vesicles. Exp Cell Res. 1975 Oct 1;95(1):79–87. doi: 10.1016/0014-4827(75)90611-4. [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. Durston A. J. Pacemaker mutants of Dictyostelium discoideum. Dev Biol. 1974 Jun;38(2):308–319. doi: 10.1016/0012-1606(74)90009-8. [DOI] [PubMed] [Google Scholar]
  8. Gerisch G. Cell aggregation and differentiation in Dictyostelium. Curr Top Dev Biol. 1968;3:157–197. doi: 10.1016/s0070-2153(08)60354-3. [DOI] [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. Gerisch G., Hess B. Cyclic-AMP-controlled oscillations in suspended Dictyostelium cells: their relation to morphogenetic cell interactions. Proc Natl Acad Sci U S A. 1974 May;71(5):2118–2122. doi: 10.1073/pnas.71.5.2118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gerisch G., Hülser D., Malchow D., Wick U. Cell communication by periodic cyclic-AMP pulses. Philos Trans R Soc Lond B Biol Sci. 1975 Nov 6;272(915):181–192. doi: 10.1098/rstb.1975.0080. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Gingle A. R., Robertson A. The development of the relaying competence in Dictyostelium discoideum. J Cell Sci. 1976 Jan;20(1):21–27. doi: 10.1242/jcs.20.1.21. [DOI] [PubMed] [Google Scholar]
  14. Goldbeter A., Caplan S. R. Oscillatory enzymes. Annu Rev Biophys Bioeng. 1976;5:449–476. doi: 10.1146/annurev.bb.05.060176.002313. [DOI] [PubMed] [Google Scholar]
  15. Goldbeter A. Mechanism for oscillatory synthesis of cyclic AMP in Dictyostelium discoideum. Nature. 1975 Feb 13;253(5492):540–542. doi: 10.1038/253540a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Gross J. D., Peacey M. J., Trevan D. J. Signal emission and signal propagation during early aggregation in Dictyostelium discoideum. J Cell Sci. 1976 Dec;22(3):645–656. doi: 10.1242/jcs.22.3.645. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Klein C. Adenylate cyclase activity in Dictyostelium discoideum amoebae and its changes during differentiation. FEBS Lett. 1976 Sep 15;68(1):125–128. doi: 10.1016/0014-5793(76)80419-x. [DOI] [PubMed] [Google Scholar]
  20. Klein C., Darmon M. The relationship of phosphodiesterase to the developmental cycle of Dictyostelium discoideum. Biochem Biophys Res Commun. 1975 Nov 3;67(1):440–447. doi: 10.1016/0006-291x(75)90335-6. [DOI] [PubMed] [Google Scholar]
  21. Konijn T. M., Van De Meene J. G., Bonner J. T., Barkley D. S. The acrasin activity of adenosine-3',5'-cyclic phosphate. Proc Natl Acad Sci U S A. 1967 Sep;58(3):1152–1154. doi: 10.1073/pnas.58.3.1152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MONOD J., WYMAN J., CHANGEUX J. P. ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. J Mol Biol. 1965 May;12:88–118. doi: 10.1016/s0022-2836(65)80285-6. [DOI] [PubMed] [Google Scholar]
  23. Malchow D., Gerisch G. Short-term binding and hydrolysis of cyclic 3':5'-adenosine monophosphate by aggregating Dictyostelium cells. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2423–2427. doi: 10.1073/pnas.71.6.2423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Robertson A., Drage D. J., Cohen M. H. Control of Aggregation in Dictyostelium discoideum by an External Periodic Pulse of Cyclic Adenosine Monophosphate. Science. 1972 Jan 21;175(4019):333–335. doi: 10.1126/science.175.4019.333. [DOI] [PubMed] [Google Scholar]
  26. Roos W., Gerisch G. Receptor-mediated adenylate cyclase activation in Dictyostelium discoideum. FEBS Lett. 1976 Oct 1;68(2):170–172. doi: 10.1016/0014-5793(76)80429-2. [DOI] [PubMed] [Google Scholar]
  27. Roos W., Nanjundiah V., Malchow D., Gerisch G. Amplification of cyclic-AMP signals in aggregating cells of Dictyostelium discoideum. FEBS Lett. 1975 May 1;53(2):139–142. doi: 10.1016/0014-5793(75)80005-6. [DOI] [PubMed] [Google Scholar]
  28. Rossomando E. F., Sussman M. A 5'-Adenosine Monophosphate-Dependent Adenylate Cyclase and an Adenosine 3':5'-Cyclic Monophosphate-Dependent Adenosine Triphosphate Pyrophosphohydrolase in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Apr;70(4):1254–1257. doi: 10.1073/pnas.70.4.1254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Winfree A. T. Spiral waves of chemical activity. Science. 1972 Feb 11;175(4022):634–636. doi: 10.1126/science.175.4022.634. [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