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