AJP - Cell Physiology, Vol 268, Issue 6 C1537-C1545, Copyright © 1995 by American Physiological Society

ARTICLES

Intercellular calcium waves mediated by diffusion of inositol trisphosphate: a two-dimensional model

J. Sneyd, B. T. Wetton, A. C. Charles and M. J. Sanderson
Department of Biomathematics, School of Medicine, University of California, Los Angeles 90024, USA.

In response to mechanical stimulation of a single cell, airway epithelial cells in culture exhibit a wave of increased intracellular free Ca2+ concentration that spreads from cell to cell over a limited distance through the culture. We present a detailed analysis of the intercellular wave in a two-dimensional sheet of cells. The model is based on the hypothesis that the wave is the result of diffusion of inositol trisphosphate (IP3) from the stimulated cell. The two-dimensional model agrees well with experimental data and makes the following quantitative predictions: as the distance from the stimulated cells increases, 1) the intercellular delay increases exponentially, 2) the intracellular wave speed decreases exponentially, and 3) the arrival time increases exponentially. Furthermore, 4) a proportion of the cells at the periphery of the response will exhibit waves of decreased amplitude, 5) the intercellular membrane permeability to IP3 must be approximately 2 microns/s or greater, and 6) the ratio of the maximum concentration of IP3 in the stimulated cell to the Km of the IP3 receptor (with respect to IP3) must be approximately 300 or greater. These predictions constitute a rigorous test of the hypothesis that the intercellular Ca2+ waves are mediated by IP3 diffusion.

This article has been cited by other articles:

				J. M. A. M. Kusters, W. P. M. van Meerwijk, D. L. Ypey, A. P. R. Theuvenet, and C. C. A. M. Gielen Fast calcium wave propagation mediated by electrically conducted excitation and boosted by CICR Am J Physiol Cell Physiol, April 1, 2008; 294(4): C917 - C930. [Abstract] [Full Text] [PDF]

				N. P. Barrera, B. Morales, and M. Villalon Plasma and intracellular membrane inositol 1,4,5-trisphosphate receptors mediate the Ca2+ increase associated with the ATP-induced increase in ciliary beat frequency Am J Physiol Cell Physiol, October 1, 2004; 287(4): C1114 - C1124. [Abstract] [Full Text] [PDF]

				O. K. Nihei, A. C. Campos de Carvalho, D. C. Spray, W. Savino, and L. A. Alves A novel form of cellular communication among thymic epithelial cells: intercellular calcium wave propagation Am J Physiol Cell Physiol, November 1, 2003; 285(5): C1304 - C1313. [Abstract] [Full Text] [PDF]

				M. Salomonsson, F. Gustafsson, D. Andreasen, B. L. Jensen, and N.-H. Holstein-Rathlou Local electric stimulation causes conducted calcium response in rat interlobular arteries Am J Physiol Renal Physiol, September 1, 2002; 283(3): F473 - F480. [Abstract] [Full Text] [PDF]

				T. Hofer, L. Venance, and C. Giaume Control and Plasticity of Intercellular Calcium Waves in Astrocytes: A Modeling Approach J. Neurosci., June 15, 2002; 22(12): 4850 - 4859. [Abstract] [Full Text] [PDF]

				T. Korkiamaki, H. Yla-Outinen, J. Koivunen, S.-L. Karvonen, and J. Peltonen Altered Calcium-Mediated Cell Signaling in Keratinocytes Cultured from Patients with Neurofibromatosis Type 1 Am. J. Pathol., June 1, 2002; 160(6): 1981 - 1990. [Abstract] [Full Text] [PDF]

				L. Homolya, T. H. Steinberg, and R. C. Boucher Cell to Cell Communication in Response to Mechanical Stress via Bilateral Release of ATP and UTP in Polarized Epithelia J. Cell Biol., September 18, 2000; 150(6): 1349 - 1360. [Abstract] [Full Text] [PDF]

				J. A. Felix, E. R. Dirksen, and M. L. Woodruff Physiology of a Microgravity Environment: Selected Contribution: PKC activation inhibits Ca2+ signaling in tracheal epithelial cells kept in simulated microgravity J Appl Physiol, August 1, 2000; 89(2): 855 - 864. [Abstract] [Full Text] [PDF]

				G. DUPONT, T. TORDJMANN, C. CLAIR, S. SWILLENS, M. CLARET, and L. COMBETTES Mechanism of receptor-oriented intercellular calcium wave propagation in hepatocytes FASEB J, February 1, 2000; 14(2): 279 - 289. [Abstract] [Full Text]

				D. Parthimos, D. H. Edwards, and T. M. Griffith Minimal model of arterial chaos generated by coupled intracellular and membrane Ca2+ oscillators Am J Physiol Heart Circ Physiol, September 1, 1999; 277(3): H1119 - H1144. [Abstract] [Full Text] [PDF]

				K. Hirose, S. Kadowaki, M. Tanabe, H. Takeshima, and M. Iino Spatiotemporal Dynamics of Inositol 1,4,5-Trisphosphate That Underlies Complex Ca2+ Mobilization Patterns Science, May 28, 1999; 284(5419): 1527 - 1530. [Abstract] [Full Text]

				B. HIMPENS, P. STALMANS, P. GOMEZ, M. MALFAIT, and J. VEREECKE Intra- and intercellular Ca2+ signaling in retinal pigment epithelial cells during mechanical stimulation FASEB J, May 1, 1999; 13(9001): 63 - 68. [Abstract] [Full Text] [PDF]

				M. L. Woodruff, V. V. Chaban, C. M. Worley, and E. R. Dirksen PKC role in mechanically induced Ca2+ waves and ATP-induced Ca2+ oscillations in airway epithelial cells Am J Physiol Lung Cell Mol Physiol, April 1, 1999; 276(4): L669 - L678. [Abstract] [Full Text] [PDF]

				P. B. Guthrie, J. Knappenberger, M. Segal, M. V. L. Bennett, A. C. Charles, and S. B. Kater ATP Released from Astrocytes Mediates Glial Calcium Waves J. Neurosci., January 15, 1999; 19(2): 520 - 528. [Abstract] [Full Text] [PDF]

				D. T. Kurjiaka, T. D. Steele, M. V. Olsen, and J. M. Burt Gap junction permeability is diminished in proliferating vascular smooth muscle cells Am J Physiol Cell Physiol, December 1, 1998; 275(6): C1674 - C1682. [Abstract] [Full Text] [PDF]

				G. J. Christ, D. C. Spray, M. El-Sabban, L. K. Moore, and P. R. Brink Gap Junctions in Vascular Tissues: Evaluating the Role of Intercellular Communication in the Modulation of Vasomotor Tone Circ. Res., October 1, 1996; 79(4): 631 - 646. [Abstract] [Full Text]