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Calcium wave propagation by calcium-induced calcium release: An unusual excitable system

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Abstract

We discuss in detail the behaviour of a model, proposed by Goldbeteret al. (1990.Proc. natn. Acad. Sci. 87, 1461–1465), for intracellular calcium wave propagation by calcium-induced calcium release, focusing our attention on excitability and the propagation of waves in one spatial dimension. The model with no diffusion behaves like a generic excitable system, and threshold behaviour, excitability and oscillations can be understood within this general framework. However, when diffusion is included, the model no longer behaves like a generic excitable system; the fast and slow variables are not distinct and previous results on excitable systems do not necessarily apply. We consider a piecewise linear simplification of the model, and construct travelling pulse and periodic plane wave solutions to the simplified model. The analogous behaviour in the full model is studied numerically. Goldbeter's model for calciuminduced calcium release is an excitable system of a type not previously studied in detail.

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Literature

  • Backx, P. H., P. P. de Tombe, J. H. K. Van Deen, B. J. M. Mulder and H. E. D. J. ter Keurs. 1989. A model of propagating calcium-induced calcium release mediated by calcium diffusion.J. gen. Physiol. 93, 963–977.

    Article  Google Scholar 

  • Berridge, M. J. 1989. Cell signalling through cytoplasmic calcium oscillations. InCell to Cell Signalling: From Experiment to Theoretical Models, A. Goldbeter (Ed.), pp. 449–459. London: Academic Press.

    Google Scholar 

  • Berridge, M. J. 1990. Calcium oscillations.J. Biol. Chem. 265, 9583–9586.

    Google Scholar 

  • Berridge, M. J. 1991. Cytoplasmic calcium oscillations: a two pool model.Cell Calcium 12, 63–72.

    Article  Google Scholar 

  • Berridge, J. J. and A. Galione. 1988. Cytosolic calcium oscillators.FASEB J. 2, 3074–3082.

    Google Scholar 

  • Berridge, M. J. and R. F. Irvine. 1989. Inositol phosphates and cell signalling.Nature 341, 197–205.

    Article  Google Scholar 

  • Bezprozvanny, I., J. Watras and B. E. Ehrlich. 1991. Bell-shaped calcium-response curves of Ins(1,4,5)P3-and calcium-gated channels from endoplasmic reticulum of cerebellum.Nature 351, 751–754.

    Article  Google Scholar 

  • Britton, N. F. 1986.Reaction-Diffusion Equations and Their Applications to Biology, London: Academic Press.

    MATH  Google Scholar 

  • Busa, W. B. and R. Nuccitelli. 1985. An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog,Xenopus laevis.J. Cell Biol. 100, 1325–1329.

    Article  Google Scholar 

  • Cannell, M. B. and D. G. Allen. 1984. Model of calcium movements during activation in the sarcomere of frog skeletal muscle,Biophys. J. 45, 913–925.

    Google Scholar 

  • Casten, R. G., H. Cohen and P. A. Lagerstrom. 1975. Perturbation analysis of an approximation to the Hodgkin-Huxley theory.Q. Appl. Math. 32, 365–402.

    MATH  MathSciNet  Google Scholar 

  • Charles, A. C., J. E. Merrill, E. R. Dirksen and M. J. Sanderson. 1991. Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate.Neuron. 6, 983–992.

    Article  Google Scholar 

  • Cheer, A., J-P. Vincent, R. Nuccitelli and G. Oster. 1987. Cortical activity in vertebrate eggs I: the activation waves.J. theor. Biol. 124, 377–404.

    Article  MathSciNet  Google Scholar 

  • Cobbold, P. H., A. Sanchez-Bueno and C. J. Dixon. 1991. The hepatocyte calcium oscillator.Cell Calcium. 12, 87–95.

    Article  Google Scholar 

  • Cohen, D. S., J. C. Neu and R. R. Rosales. 1978. Rotating spiral wave solutions of reaction-diffusion equations.SIAM J. appl. Math. 35, 536–547.

    Article  MATH  MathSciNet  Google Scholar 

  • Cuthbertson, K. S. R. 1989. Intracellular calcium oscillators, InCell to Cell Signaling: From Experiments to Theoretical Models, A. Goldbeter (Ed.) pp. 435–447. London: Academic Press.

    Google Scholar 

  • Cuthbertson, K. S. R. and T. R. Chay. 1991. Modelling receptor-controlled intracellular calcium oscillators.Cell Calcium. 12, 97–109.

    Article  Google Scholar 

  • Dockery, J. D. and J. P. Keener. 1989. Diffusive effects on dispersion in excitable media.SIAM J. app. Math. 49, 539–566.

    Article  MATH  MathSciNet  Google Scholar 

  • Doedel, E. 1986.Software for continuation and bifurcation problems in ordinary differential equations. California Institute of Technology.

  • Duffy, M. R., N. F. Britton and J. D. Murray. 1980. Spiral wave solutions of practical reaction-diffusion systems.SIAM J. appl. Math. 39, 8–13.

    Article  MATH  MathSciNet  Google Scholar 

  • Dupont, G. and A. Goldbeter. 1989. Theoretical insights into the origin of signal-induced calcium oscillations, InCell to Cell Signalling: From Experiments to Theoretical Models, A. Goldbeter (Ed.), pp. 461–474. London: Academic Press.

    Google Scholar 

  • Dupont, G., M. J. Berridge and A. Goldbeter. 1991. Signal-induced Ca2+ oscillations: properties of a model based on Ca2+-induced Ca2+ release.Cell Calcium.12, 73–85.

    Article  Google Scholar 

  • Endo, M., M. Tanaka and Y. Ogawa. 1970. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres.Nature 228, 34–36.

    Article  Google Scholar 

  • Fabiato, A. 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum.Am. J. Physiol. 245, C1-C14.

    Google Scholar 

  • Fabiato, A. and F. Fabiato. 1975. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells.J. Physiol. 249, 469–495.

    Google Scholar 

  • Finch, E. A., T. J. Turner and S. M. Goldin. 1991. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release.Science 252, 443–446.

    Google Scholar 

  • FitzHugh, R. 1961. Impulses and physiological states in theoretical models of nerve membrane.Biophys. J. 1, 445–466.

    Article  Google Scholar 

  • FitzHugh, R. 1969. Impulses and physiological states in models of nerve membrane. InBiological Engineering, H. P. Schwan (Ed.), pp. 1–85. New York: McGraw-Hill.

    Google Scholar 

  • Gilkey, J. C., L. F. Jaffe, E. B. Ridgway and G. T. Reynolds. 1978. A free calcium wave traverses the activating egg of the medakaoryzias latipes.J. Cell Biol. 76, 448–466.

    Article  Google Scholar 

  • Girard, S., A. Luckhoff, J. Lechleiter, J. Sneyd and D. Clapham. 1992. Two-dimensional model of calcium waves reproduces the patterns observed inXenopus oocytes.Biophys. J. 61, 509–517.

    Google Scholar 

  • Goldbeter, A., G. Dupont and M. J. Berridge. 1990. Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation,Proc. natn. Acad. Sci. 87, 1461–1465.

    Article  Google Scholar 

  • Hagan, P. S. 1982. Spiral waves in reaction-diffusion equations.SIAM J. appl. Math. 42, 762–786.

    Article  MATH  MathSciNet  Google Scholar 

  • Harootunian, A. T., J. P. Y. Kao, S. Paranjape, S. R. Adams, B. V. L. Potter, and R. Y. Tsien. 1991. Cytosolic Ca2+ oscillations in REF52 fibroblasts: Ca2+-stimulated IP3 production or voltage-dependent Ca2+ channels as key positive feedback elements.Cell Calcium 12, 153–164.

    Article  Google Scholar 

  • Hastings, S. P. 1974. The existence of periodic solutions to Nagumo's equation.Q. J. Math. 25, 369–378.

    MATH  MathSciNet  Google Scholar 

  • Hastings, S. P. 1976. On the existence of homoclinic and periodic orbits for the FitzHugh-Nagumo equations.Q. J. Math. 27, 123–134.

    MATH  MathSciNet  Google Scholar 

  • Iino, M. 1990. Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in smooth muscle cells of the Guinea PigTaenia Caeci.J. gen. Physiol. 95, 1103–1122.

    Article  Google Scholar 

  • Jacob, R. 1991. Calcium oscillations in endothelial cells.Cell Calcium 12, 127–134.

    Article  Google Scholar 

  • Keener, J. P. 1980. Waves in excitable media.SIAM J. appl. Math. 39, 528–548.

    Article  MATH  MathSciNet  Google Scholar 

  • Keener, J. P. 1986. A geometrical theory for spiral waves in excitable media.SIAM J. appl. Math. 46, 1039–1056.

    Article  MATH  MathSciNet  Google Scholar 

  • Kopell, N. and L. N. Howard. 1973. Plane wave solutions to reaction-diffusion equations.Stud. appl. Math. 52, 291–328.

    MATH  MathSciNet  Google Scholar 

  • Kopell, N. and L. N. Howard. 1981. Target pattern and spiral solutions to reaction-diffusion equations with more than one space dimension.Adv. Appl. Math. 2, 417–449.

    Article  MATH  MathSciNet  Google Scholar 

  • Kuba, K. and S. Takeshita. 1981. Simulation of intracellular Ca2+ oscillation in a sympathetic neurone.J. theor. Biol. 93, 1009–1031.

    Article  Google Scholar 

  • Lane, D. C., J. D. Murray and V. S. Manoranjan. 1987. Analysis of wave phenomena in a morphogenetic mechanochemical model and an application to post-fertilization waves on eggs.IMA J. Math. appl. Med. Biol. 4, 309–331.

    MATH  MathSciNet  Google Scholar 

  • Lechleiter, J., S. Girard, D. Clapham and E. Peralta. 1991a. Subcellular patterns of calcium release determined by G protein-specific residues of muscarinic receptors.Nature 350, 505–508.

    Article  Google Scholar 

  • Lechleiter, J., S. Girard, E. Peralta and D. Clapham. 1991b. Spiral calcium wave propagation and annihilation inXenopus laevis oocytes.Science 252, 123–126.

    Google Scholar 

  • McKean, H. P. 1970. Nagumo's equation.Adv. Math. 4, 209–223.

    Article  MATH  MathSciNet  Google Scholar 

  • Maginu, K. 1985. Geometrical characteristics associated with stability and bifurcations of periodic travelling waves in reaction-diffusion equations.SIAM J. appl. Math. 45, 750–774.

    Article  MATH  MathSciNet  Google Scholar 

  • Meyer, T. and L. Stryer. 1988. Molecular model for receptor-stimulated calcium spiking.Proc. natn. Acad. Sci. 85, 5051–5055.

    Article  Google Scholar 

  • Murray, J. D. 1989.Mathematical Biology. Berlin: Springer-Verlag.

    MATH  Google Scholar 

  • Murray, J. D. and G. F. Oster. 1984. Generation of biological pattern and form.IMA J. Math. appl. Med. Biol. 1, 51–75.

    MATH  MathSciNet  Google Scholar 

  • Neu, J. C. 1979. Chemical waves and the diffusive coupling of limit cycle oscillators.SIAM J. appl Math. 36, 509–515.

    Article  MATH  MathSciNet  Google Scholar 

  • Oster, G. F. and G. M. Odell. 1984. Mechanics of cytogels I: oscillations in Physarum.Cell Motility 4, 469–503.

    Article  Google Scholar 

  • Parker, I. and I. Ivorra. 1990. Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: a possible mechanism for oscillatory release of Ca2+.Proc. natn. Acad. Sci. 87, 260–264.

    Article  Google Scholar 

  • Peskin, C. S. 1976.Partial Differential Equations in Biology. New York: Courant Insitute of Mathematical Sciences, New York University.

    MATH  Google Scholar 

  • Petersen, O. H., D. V. Gallacher, M. Wakui, D. I. Yule, C. C. H. Petersen and E. C. Toescu. 1991. Receptor-activated cytoplasmic Ca2+ oscillations in pancreatic acinar cells: generation and spreading of Ca2+ signals.Cell Calcium 12, 135–144.

    Article  Google Scholar 

  • Rinzel, J. 1976. Simple model equations for active nerve conduction and passive neuronal integration.Lect. Math. Life Sci. 8, 125–164.

    MATH  MathSciNet  Google Scholar 

  • Rinzel, J. and J. B. Keller. 1973. Traveling wave solutions of a nerve conduction equation.Biophys J. 13, 1313–1337.

    Google Scholar 

  • Sanderson, M. J., A. C. Charles and E. R. Dirksen. 1990. Mechanical stimulation and intercellular communication increases intracellular Ca2+ in epithelial cells.Cell Regulat. 1, 585–596.

    Google Scholar 

  • Sauvé, R., A. Diarra, M. Chahine, C. Simoneau, N. Morier and G. Roy. 1991. Ca2+ oscillations induced by histamine H1 receptor stimulation in HeLa cells: Fura-2 and patch clamp analysis.Cell Calcium. 12, 165–176.

    Article  Google Scholar 

  • Swillens, S. and D. Mercan. 1990. Computer simulation of a cytosolic calcium oscillator.Biochem. J. 271, 835–838.

    Google Scholar 

  • Thomas, A. P., D. C. Renard and T. A. Rooney. 1991. Spatial and temporal organization of calcium signalling in hepatocytes.Cell Calcium 12, 111–126.

    Article  Google Scholar 

  • Troy, W. C. 1976. Bifurcation phenomena in FitzHugh's nerve conduction equations.J. Math. analys. appl. 54, 678–690.

    Article  MATH  MathSciNet  Google Scholar 

  • Tsien, R. W. and R. Y. Tsien. 1990. Calcium channels, stores, and oscillations,A. Rev. Cell Biol. 6, 715–760.

    Article  Google Scholar 

  • Tsunoda, Y. 1991. Oscillatory Ca2+ signaling and its cellular function.The New Biol. 3, 3–17.

    Google Scholar 

  • Zykov, V. S. 1980. Analytic evaluation of the dependence of the speed of excitation wave in a twodimensional excitable medium on the curvature of its front.Biophys. 25, 906–911.

    Google Scholar 

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Sneyd, J., Girard, S. & Clapham, D. Calcium wave propagation by calcium-induced calcium release: An unusual excitable system. Bltn Mathcal Biology 55, 315–344 (1993). https://doi.org/10.1007/BF02460886

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