Abstract
The propagation of fire-diffuse-fire Ca2+ waves through a three-dimensional rectangular domain is considered. The domain is infinite in extent in the direction of propagation but with lateral barriers to diffusion which contain Ca2+ pumps. The Ca2+ concentration profile due to the firing of a release site (spark) is derived analytically based on the Green’s function for the diffusion equation on the domain. The existence, stability and speed of these waves is shown to be critically dependent on the dimensions of the domain and the Ca2+ pump rate. It is shown that the smaller the dimensions of the region, the lower the Ca2+ release flux required for wave propagation, and the higher the wave speed. Also it is shown that the region may support multiple Ca2+ wavefronts of varying wave speed. This model is relevant to subsarcolemmal waves in atrial myocytes (Kockskämper et al., 2001, Biophys. J. 81, 2590–2605), and the results may be of importance in understanding the roles of the endoplasmic/sarcoplasmic reticulum, surface membranes and Ca2+ pumps in the intracellular Ca2+ dynamics of cells.
Similar content being viewed by others
References
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.
Blatter, L. A., J. Huser and E. Rios (1997). Sarcoplasmic reticulum Ca2+ release flux underlying Ca2+ sparks in cardiac muscle. Proc. Natl Acad. Sci. USA 94, 4176–4181.
Bugrim, A. E., A. M. Zhabotinsky and I. R. Epstein (1997). Calcium waves in a model with a random spatially discrete distribution of Ca2+ release sites. Biophys. J. 73, 2897–2906.
Callamaras, N., J. S. Marchant, X. P. Sun and I. Parker (1998). Activation and co-ordination of InsP3-mediated elementary Ca2+ events during global Ca2+ signals in Xenopus oocytes. J. Physiol. 509, 81–91.
Coombes, S. (2001). The effect of ion pumps on the speed of travelling waves in the fire-diffuse-fire model of Ca2+ release. Bull. Math. Biol. 63, 1–20.
Cordeiro, J. M., K. W. Spitzer, W. R. Giles, P. E. Ershler, M. B. Cannell and J. H. Bridge (2001). Location of the initiation site of calcium transients and sparks in rabbit heart Purkinje cells. J. Physiol. 531, 301–314.
Dawson, S. P., J. Keizer and J. E. Pearson (1999). Fire-diffuse-fire model of dynamics of intracellular calcium waves. Proc. Natl Acad. Sci. USA 96, 6060–6063.
Falcke, M., L Tsimring and H. Levine (2000). Stochastic spreading of intracellular Ca2+ release. Phys. Rev. E 62, 2636–2643.
Fontanilla, R. A. and R. Nuccitelli (1998). Characterization of the sperm-induced calcium wave in Xenopus eggs using confocal microscopy. Biophys. J. 75, 2079–2087.
Gyorke, S. and M. Fill (1993). Ryanodine receptor adaptation: control mechanism of Ca(2+)-induced Ca2+ release in heart. Science 260, 807–809.
Hüser, J. and L. A. Blatter (1997). Elementary events of agonist-induced Ca2+ release in vascular endothelial cells. Am. J. Physiol. 273, C1775–C1782.
Izu, L. T., W. G. Wier and C. W. Balke (2001). Evolution of cardiac calcium waves from stochastic calcium sparks. Biophys. J. 80, 103–120.
Jaggar, J. H., V. A. Porter, W. J. Lederer and M. T. Nelson (2000). Calcium sparks in smooth muscle. Am. J. Physiol. 278, C235–C256.
Kargacin, G. J. (1994). Calcium signaling in restricted diffusion spaces. Biophys. J. 67, 262–272.
Kargacin, G. and F. S. Fay (1991). Ca2+ movement in smooth muscle cells studied with one-and two-dimensional diffusion models. Biophys. J. 60, 1088–1100.
Keizer, J., G. D. Smith, S. Ponce-Dawson and J. E. Pearson (1998). Saltatory propagation of Ca2+ waves by Ca2+ sparks. Biophys. J. 75, 595–600.
Keizer, J. and G. D. Smith (1998). Spark-to-wave transition: saltatory transmission of calcium waves in cardiac myocytes. Biophys. Chem. 72, 87–100.
Kockskämper, J., K. A. Sheehan, D. J. Bare, S. L. Lipsius, G. A. Mignery and L. A. Blatter (2001). Activation and propagation of Ca(2+) release during excitation-contraction coupling in atrial myocytes. Biophys. J. 81, 2590–2605.
Kraut, E. A. (1967). Fundamentals of Mathematical Physics, New York: McGraw-Hill.
Kupferman, R., P. P. Mitra, P. C. Hohenberg and S. S. Wang (1997). Analytical calculation of intracellular calcium wave characteristics. Biophys. J. 72, 2430–2444.
Langer, G. A. and A. Peskoff (1996). Calcium concentration and movement in the diadic cleft space of the cardiac ventricular cell. Biophys. J. 70, 1169–1182.
Lipp, P., M. Egger and E. Niggli (2002). Spatial characteristics of sarcoplasmic reticulum Ca2+ release events triggered by L-type Ca2+ current and Na+ current in guinea-pig cardiac myocytes. J. Physiol. 542, 383–393.
Niggli, E. (1999). Localized intracellular calcium signaling in muscle: calcium sparks and calcium quarks. Annu. Rev. Physiol. 61, 311–335.
Pabelick, C. M., Y. S. Prakash, M. S. Kannan and G. C. Sieck (1999). Spatial and temporal aspects of calcium sparks in porcine tracheal smooth muscle cells. Am. J. Physiol. 277, L1018–L1025.
Parker, I. and Y. Yao (1991). Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc. R. Soc. Lond. B 246, 269–274.
Pearson, J. E. and S. Ponce-Dawson (1998). Crisis on skid row. Physica A 257, 141–148.
Perez, G. J., A. D. Bonev, J. B. Patlak and M. T. Nelson (1999). Functional coupling of Ryanodine receptors to KCa channels in smooth muscle cells from rat cerebral arteries. J. Gen. Physiol. 113, 229–238.
Peskoff, A., J. A. Post and G. A. Langer (1992). Sarcolemmal calcium-binding sites in heart: II. Mathematical model for diffusion of calcium released from the sarcoplasmic reticulum into the diadic region. J. Membr. Biol. 129, 59–69.
Sitsapesan, R. and A. J. Williams (2000). Do inactivation mechanisms rather than adaptation hold the key to understanding Ryanodine receptor channel gating? J. Gen. Physiol. 116, 867–872.
Strauss, W. A. (1992). Partial Differential Equations: an Introduction, New York: John Wiley and Sons.
Subramanian, S., S. Viatchenko-Karpinski, V. Lukyanenko, S. Gyorke and T. F. Wiesner (2001). Underlying mechanisms of symmetric calcium wave propagation in rat ventricular myocytes. Biophys. J. 80, 1–11.
Thomas, D., M. J. Mason and M. P. Mahaut-Smith (2001). Depolarisation-evoked Ca2+ waves in the non-excitable rat megakaryocyte. J. Physiol. 537, 371–378.
Wagner, J. and J. Keizer (1994). Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys. J. 67, 447–456.
Wussling, M. H. P. and H. Salz (1996). Nonlinear propagation of spherical calcium waves in rat cardiac myocytes. Biophys. J. 70, 1144–1153.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lemon, G. Fire-diffuse-fire calcium waves in confined intracellular spaces. Bull. Math. Biol. 66, 65–90 (2004). https://doi.org/10.1016/S0092-8240(03)00074-0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1016/S0092-8240(03)00074-0