Intercellular Ca2+ wave propagation through gap-junctional Ca2+ diffusion: a theoretical study.

Intercellular regenerative calcium waves in systems such as the liver and the blowfly salivary gland have been hypothesized to spread through calcium-induced calcium release (CICR) and gap-junctional calcium diffusion. A simple mathematical model of this mechanism is developed. It includes CICR and calcium removal from the cytoplasm, cytoplasmic and gap-junctional calcium diffusion, and calcium buffering. For a piecewise linear approximation of the calcium kinetics, expressions in terms of the cellular parameters are derived for 1) the condition for the propagation of intercellular waves, and 2) the characteristic time of the delay of a wave encountered at the gap junctions. Intercellular propagation relies on the local excitation of CICR in the perijunctional space by gap-junctional calcium influx. This mechanism is compatible with low effective calcium diffusivity, and necessitates that CICR can be excited in every cell along the path of a wave. The gap-junctional calcium permeability required for intercellular waves in the model falls in the range of reported gap-junctional permeability values. The concentration of diffusive cytoplasmic calcium buffers and the maximal rate of CICR, in the case of inositol 1,4,5-trisphosphate (IP3) receptor calcium release channels set by the IP(3) concentration, are shown to be further determinants of wave behavior.

[1]  G. Meissner,et al.  Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. , 1994, Annual review of physiology.

[2]  M. Sanderson,et al.  Intercellular calcium signaling via gap junctions in glioma cells , 1992, The Journal of cell biology.

[3]  S. B. Kater,et al.  An extracellular signaling component in propagation of astrocytic calcium waves. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  John Crank,et al.  The Mathematics Of Diffusion , 1956 .

[5]  D C Spray,et al.  Gap junctional conductance and permeability are linearly related. , 1986, Science.

[6]  T Höfer,et al.  Model of intercellular calcium oscillations in hepatocytes: synchronization of heterogeneous cells. , 1999, Biophysical journal.

[7]  Christian Giaume,et al.  Control of gap-junctional communication in astrocytic networks , 1996, Trends in Neurosciences.

[8]  Barbara E. Ehrlich,et al.  Type III InsP3 receptor channel stays open in the presence of increased calcium , 1998, Nature.

[9]  M. Frieden,et al.  An intercellular regenerative calcium wave in porcine coronary artery endothelial cells in primary culture , 1998, The Journal of physiology.

[10]  J. C. Nuño,et al.  Generalization of the theory of transition times in metabolic pathways: a geometrical approach. , 1999, Biophysical journal.

[11]  Laurent Combettes,et al.  Receptor‐oriented intercellular calcium waves evoked by vasopressin in rat hepatocytes , 1998, The EMBO journal.

[12]  G. Christ,et al.  Gap junction-mediated intercellular diffusion of Ca2+ in cultured human corporal smooth muscle cells. , 1992, The American journal of physiology.

[13]  M Claret,et al.  Coordinated intercellular calcium waves induced by noradrenaline in rat hepatocytes: dual control by gap junction permeability and agonist , 1997, The EMBO journal.

[14]  J. Connor,et al.  Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Putney,et al.  Spatial and temporal aspects of cellular calcium signaling , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  L. D. Robb-Gaspers,et al.  Coordination of calcium signalling by endothelial-derived nitric oxide in the intact liver , 1999, Nature Cell Biology.

[17]  James P. Keener,et al.  Propagation and its failure in coupled systems of discrete excitable cells , 1987 .

[18]  J. Sneyd,et al.  Intercellular spiral waves of calcium. , 1998, Journal of theoretical biology.

[19]  M. Berridge,et al.  Elementary and global aspects of calcium signalling. , 1997, The Journal of experimental biology.

[20]  Ca(2+)-mobilizing hormones induce sequentially ordered Ca2+ signals in multicellular systems of rat hepatocytes. , 1994, The Biochemical journal.

[21]  R. Eckert,et al.  Quantitative Determination of Gap Junctional Permeability in the Lens Cortex , 1999, The Journal of Membrane Biology.

[22]  M. Nedergaard,et al.  Impact of Cytoplasmic Calcium Buffering on the Spatial and Temporal Characteristics of Intercellular Calcium Signals in Astrocytes , 1997, The Journal of Neuroscience.

[23]  L. Stryer,et al.  Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. , 1992, Science.

[24]  R. Bruzzone,et al.  Connections with connexins: the molecular basis of direct intercellular signaling. , 1996, European journal of biochemistry.

[25]  P. D'andrea,et al.  Propagation of intercellular Ca2+ waves in mechanically stimulated articular chondrocytes , 1997, FEBS letters.

[26]  E. Stuenkel,et al.  Intercellular calcium waves in rat pancreatic acini: mechanism of transmission. , 1996, The American journal of physiology.

[27]  J. Dufour,et al.  Inositol 1,4,5-Trisphosphate and Calcium Regulate the Calcium Channel Function of the Hepatic Inositol 1,4,5-Trisphosphate Receptor* , 1997, The Journal of Biological Chemistry.

[28]  J. Keizer,et al.  Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. , 1994, Biophysical journal.

[29]  M. Sears,et al.  Novel paracrine signaling mechanism in the ocular ciliary epithelium. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  B. Walz,et al.  The mechanism mediating regenerative intercellular Ca2+ waves in the blowfly salivary gland , 1999, The EMBO journal.

[31]  E. Neher,et al.  Calcium gradients and buffers in bovine chromaffin cells. , 1992, The Journal of physiology.

[32]  S. Thompson,et al.  The lifetime of inositol 1,4,5-trisphosphate in single cells , 1995, The Journal of general physiology.

[33]  A. Fabiato,et al.  Time and calcium dependence of activation and inactivation of calcium- induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell , 1985, The Journal of general physiology.

[34]  M. Hori,et al.  Intercellular Calcium Signaling via Gap Junction in Connexin-43-transfected Cells* , 1998, The Journal of Biological Chemistry.

[35]  M. Nathanson,et al.  Isolated rat hepatocytes can signal to other hepatocytes and bile duct cells by release of nucleotides. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Finkbeiner,et al.  Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. , 1990, Science.

[37]  M. Sanderson,et al.  Intercellular calcium waves mediated by inositol trisphosphate. , 2007, Ciba Foundation symposium.

[38]  L. Venance,et al.  Intercellular calcium signaling and gap junctional communication in astrocytes , 1998, Glia.

[39]  J. Watras,et al.  Inositol 1,4,5-Trisphosphate (InsP3) and Calcium Interact to Increase the Dynamic Range of InsP3 Receptor-dependent Calcium Signaling , 1997, The Journal of general physiology.

[40]  V. Ganitkevich,et al.  An estimate of rapid cytoplasmic calcium buffering in a single smooth muscle cell. , 2000, Cell calcium.

[41]  A P Thomas,et al.  Coordination of Ca2+ Signaling by Intercellular Propagation of Ca2+ Waves in the Intact Liver (*) , 1995, The Journal of Biological Chemistry.

[42]  A Goldbeter,et al.  One-pool model for Ca2+ oscillations involving Ca2+ and inositol 1,4,5-trisphosphate as co-agonists for Ca2+ release. , 1993, Cell calcium.