Abstract
Upon starvation, Dictyostelium discoideum amoebae aggregate in a wave-like manner around centers, by a chemotactic response to cAMP signals. These signals are emitted by the centers in the form of pulses, with a periodicity of several minutes. Relay of the cAMP signals by chemotactically responding cells allows one center to control the aggregation of up to 105 amoebae. We analyse a model for the cAMP signalling system, based on the activation of cAMP synthesis upon binding of cAMP to a cell surface receptor, and on desensitisation of this receptor upon incubation with cAMP. The analysis shows that the self-amplifying properties of the signalling system may give rise to an instability leading to autonomous oscillations of cAMP. The model also accounts for the relay of suprathreshold cAMP pulses; such behaviour reflects the excitability of D. discoideum cells. Besides relay and periodic oscillations, the model also shows evidence for bursting and for aperiodic oscillations of cAMP, i.e. chaos (J.L. Martiel and A. Goldbeter, Nature 313:590–592, 1985). The results on chaotic behaviour may be related to experimental observations by Durston (Devel. Biol. 38:308–319, 1974) who found that in contrast to the wild type which aggregates in a periodic manner, the D. discoideum mutant Fr17 is characterised by the property of aperiodic aggregation. Ways to test the possibility that Fr17 behaviour represents an example of chaos in intercellular communication will be discussed, in the light of the modelling study.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
J.T. Bonner, ‘The Cellular Slime Molds’, Princeton University Press, Princeton, N.J. (1967).
B. Coukell, Differentiation 20: 29–35 (1981).
M.B. Coukell and F.K. Chan, FEBS Lett 110: 39–42 (1980).
Decrouly, This volume pp (1987).
Decrouly and A. Goldbeter, Proc. Nat. Acad. Sci. USA 79:6917–6921 (1982).
P.N. Devreotes, in ‘The Development of Dictyostelium discoideum’ ed. W.F. Loomis, pp 117–168, Academic Press, New York (1982).
P.N. Devreotes and J.A. Sherríng, J. Biol. Chem 260:6378–6384 (1985).
A.J. Durston, Devel. Biol 38:308–319.
M.J. Feigenbaum, J. Stat. Phys 19:25–52 (1978).
G. Gerisch, Ann. Rev. Physiol 44:535–552 (1982).
G. Gerisch, D. Malchow, W. Roos and U. Wick, J. Exp. Biol 81:33–47 (1979).
A. Goldbeter, Nature 252: 540–542 (1975).
A. Goldbeter, in ‘Molecular Mechanisms of Desensitisation’, eds. T. Konijin, P.J.M. Van Haastert, H. Van der Wel and M.D. Houslay, pp 43–62, Springer, Berlin (1986).
A. Goldbeter, in ‘Temporal Disorder in Human Oscillatory Systems’, eds. L. Rensing, U. an der Heiden and M.C. Mackey, in press, Springer, Berlin (1987).
A. Goldbeter and J.L. Martiel, in ‘Sensing and Response in Microorganisms’, eds. M. Eisenbach and M. Balaban, pp 185–198, Elsevier, Amsterdam (1985).
A. Goldbeter, J.L. Martield and 0. Decroly, in ‘Dynamics of Biochemical Systems’, eds. J. Ricard and A. Cornish-Bowden, pp 173–212 Plenum, New York (1984).
A. Goldbeter and L.A. Segel, Proc. Nat. Acad. Sci. USA 74:1543–1547 (1977).
A. Goldbeter and L.A. Segel, Differentiation 17: 127–135 (1980).
A.V. Holden, W. Winlow and P.G. Haydon, Biol. Cybern 43:169–173.
R.H. Kessin, Cell 10: 703–708 (1977).
C. Klein, J. Lubs-Haukeness and S. Simons, J. Cell. Biol 100:715–720 (1985).
P. Klein, A. Theibert, D. Fontana and P.N. Devreotes, J. Biol. Chem 260:1757–1764 (1985).
T.M. Konijin, J.G.C. Van de Meene, J.T. Bonner and D.S. Barkley, Proc. Nat. Acad. Sci. USA 58:1152–1154.
M. Markus and B. Hess, Proc. Nat Acad. Sci. USA 81:4394–4398 (1984).
M. Markus, D. Kuschmitz and B. Hess, FEBS Lett 172: 235–238 (1984).
J.L. Martiel, In preparation (1987).
J.L. Martiel and A. Goldbeter, C.R. Acad. Sci. (Paris) Ser. III 298: 549–552 (1984).
J.L. Martiel and A. Goldbeter, Nature 313: 590–592.
P.C. Newell, in Microbial Interactions (Receptors and Recognition), Ser. B. Vol. 3, ed. J.L. Reissig, pp 3–57, Chapman and Hall, London (1977).
L.F. Olsen and H. Degn, Nature 267: 177–178 (1977).
L.F. Olsen and H. Degn, Quart. Rev. Biophys 18:165–225 (1985).
H.G. Othmer, P.B. Monk and P.E. Rapp, Math. Biosci 77: 79–139 (1985).
P.E. Rapp, P.B. Monk and H.G. Othmer, Math. Biosci 77:35–78 (1985).
W. Roos, C. Scheidegger and G. Gerisch, Nature 266: 259–261 (1977).
A. Theibert and P.N. Devreotes, J. Cell Biol. 97:173–177 (1983).
B. Wurster, Biophys. Struct. Mech 9:137–143 (1982).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1987 Springer Science+Business Media New York
About this chapter
Cite this chapter
Goldbeter, A., Martiel, J.L. (1987). Periodic Behaviour and Chaos in the Mechanism of Intercellular Communication Governing Aggregation of Dictyostelium Amoebae. In: Degn, H., Holden, A.V., Olsen, L.F. (eds) Chaos in Biological Systems. NATO ASI Series, vol 138. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9631-5_10
Download citation
DOI: https://doi.org/10.1007/978-1-4757-9631-5_10
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4757-9633-9
Online ISBN: 978-1-4757-9631-5
eBook Packages: Springer Book Archive