Skip to main content
Log in

A Mathematical Model for Simultaneous Spatio-Temporal Dynamics of Calcium and Inositol 1,4,5-Trisphosphate in Madin–Darby Canine Kidney Epithelial Cells

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

The landmark paper by Hirose et al. (Hirose, K., Kadowaki, S., Tanabe, M., Takeshima, H., Iino, M., Science 284:1527–1530, 1999) presented experimental investigations to show that not only can calcium upregulate IP3, but that it can also have an inhibitory effect on IP3. In this paper, we present a preliminary model, which is consistent with these experiments. This model includes positive and negative feedback between calcium and IP3 and is able to reproduce more precisely the data presented in Hirose et al. (Hirose, K., Kadowaki, S., Tanabe, M., Takeshima, H., Iino, M., Science 284:1527–1530, 1999). In the second part of the paper, the intracellular and intercellular calcium movement in Madin–Darby canine kidney epithelial cells is investigated. With the aid of the model we are able to identify the aspects of IP3 and calcium signalling, which should be studied further experimentally before refining the model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

IP3 :

inositol 1,4,5-trisphosphate

ER:

endo(sarco)plasmic reticulum

IP3R:

inositol 1,4,5-trisphosphate receptor

ATP:

adenosine triphosphate

GFP:

green fluorescent protein

References

  • Allbritton, N.L., Meyer, T., Stryer, L., 1992. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812–1815.

    Article  Google Scholar 

  • Atri, A., Amundson, J., Clapham, D., Sneyd, J., 1993. A single-pool model for intracellular calcium oscillations and waves in the xenopus laevis oocyte. Biophys. J. 65, 1727–1739.

    Google Scholar 

  • Berridge, M.J., Bootman, M.D., Lipp, P., 1998. Calcium—A life and death signal. Nature 395, 645–648.

    Article  Google Scholar 

  • Berridge, M.J., Lipp, P., Bootman, M.D., 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11–21.

    Article  Google Scholar 

  • Blackman, B.R., Thibault, L.E., Barbee, K.A. 2000. Selective modulation of endothelial cell [Ca2+] i response to flow by the onset rate of shear stress. J. Biomech. Eng. 122, 274–282.

    Article  Google Scholar 

  • Boitano, S., Dirksen, E.R., Sanderson, M.J., 1992. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 258, 292–295.

    Article  Google Scholar 

  • Carafoli, E., 2003. The calcium-signalling saga: Tap water and protein crystals. Nat. Rev. Mol. Cell Biol. 4, 326–332.

    Article  Google Scholar 

  • Chicurel, M.E., Singer, R.H., Meyer, C.J., Ingber, D.E., 1998. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392, 730–733.

    Article  Google Scholar 

  • Dolmetsch, R.E., Xu, K., Lewis, R.S., 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933–936.

    Article  Google Scholar 

  • Farge, E., 2003. Mechanical induction of twist in the Drosophila foregut/stomodeal primordium. Curr. Biol. 13, 1365–1377.

    Article  Google Scholar 

  • Felix, J.A., Woodruff, M.L., Dirksen, E.R., 1996. Strech increases inositol 1,4,5-trisphosphate concentration in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 14(3), 296–301.

    Google Scholar 

  • Fink, C.C., Slepchenko, B., Moraru, I.I., Schaff, J., Watras, J., Loew, L.M., 1999. Morphological control of inositol-1,4,5-trisphosphate-dependent signals. J. Cell Biol. 147(5), 929–935.

    Article  Google Scholar 

  • Hirose, K., Kadowaki, S., Tanabe, M., Takeshima, H., Iino, M., 1999. Spatiotemporal dynamics of inositol 1,4,5-triphosphate that underlies complex Ca2+ mobilization patterns. Science 284, 1527–1530.

    Article  Google Scholar 

  • Höfer, T., Venance, L., Giaume, C., 2002. Control and plasticity of intercellular calcium waves in astrocytes: A modeling approach. J. Neurosci. 22(12), 4850–4859.

    Google Scholar 

  • Keener, J., Sneyd, J., 1998. Mathematical Physiology. Springer, Berlin Heidelberg New York.

    MATH  Google Scholar 

  • Kummer, U., Olsen, L.F., Dixon, C.J., Green, A.K., Bornberg-Bauer, E., Baier, G., 2000. Switching from simple to complex oscillations in calcium signalling. Biophys. J. 79, 1188–1195.

    Article  Google Scholar 

  • Luzzi, V., Murtazina, D., Allbritton, N.L., 2000. Characterization of a biological detector cell for quantification of inositol 1,4,5-trisphosphate. Anal. Biochem. 277, 221–227.

    Article  Google Scholar 

  • Luzzi, V., Sims, C.E., Soughayer, J.S., Allbritton, N.L., 1998. The physiologic concentration of inostiol 1,4,5-trisphosphate in the oocytes of Xenopus laevis. J. Biol. Chem. 273(44), 28657–28662.

    Article  Google Scholar 

  • Marks, A.R., 2003. Arrhythmias of the heart: Beyond ion channels. Nat. Med. 9(3), 263–264.

    Article  MathSciNet  Google Scholar 

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

    Article  Google Scholar 

  • Meyer, T., Stryer, L., 1991. Calcium spiking. Annu. Rev. Biophys. Biophys. Chem. 20, 153–174.

    Article  Google Scholar 

  • Mishra, J., Bhalla, U.S., 2002. Simulations of inositol phosphate metabolism and its interaction with InsP3-mediated calcium release. Biophys. J. 83, 1298–1316.

    Google Scholar 

  • Mohanti, M.J., Li, X., 2002. Strech-induced Ca2+ release via an IP3-insensitive Ca2+-channel. Am. J. Physiol. Cell Physiol. 283, 456–462.

    Google Scholar 

  • Mohanti, M.J., Ye, M., Li, X., Rossi, N.F., 2001. Hypotonic swelling-induced Ca2+ release by an IP3-insensitive Ca2+ store. Am. J. Physiol. Cell Physiol. 281, C555–C562.

    Google Scholar 

  • Murray, J.D., 1993. Mathematical Biology. Springer-Verlag, Berlin.

    MATH  Google Scholar 

  • Okubo, Y., Kakizawa, S., Hirose, K., Iino, M., 2001. Visualization of IP3 dynamics reveals a novel AMPA receptor-triggered IP3 production pathway mediated by voltage-dependent Ca2+ influx in Purkinje cells. Neuron 32, 113–122.

    Article  Google Scholar 

  • Schuster, S., Marhl, M., Höfer, T., 2002. Modelling of simple and complex calcium oscillations: From single-cell responses to intercellular signalling. Eur. J. Biochem. 269, 1333–1355.

    Article  Google Scholar 

  • Sneyd, J., (Ed.), 2005. Tutorials in Mathematical Biosciences II Mathematical Modelling of Calcium Dynamics and Signal Transduction. Springer, Berlin Heidelberg New York.

    Google Scholar 

  • Sneyd, J., Dale, P.D., Duffy, A., 1998a. Travelling waves in buffered systems: Applications to calcium waves. SIAM J. Appl. Math. 58(4), 1178–1192.

    Article  MATH  MathSciNet  Google Scholar 

  • Sneyd, J., Wilkins, M., Strahonja, A., Sanderson, M.J., 1998b. Calcium waves and oscillations driven by an intercellular gradient of inositol (1,4,5)-trisphosphate. Biophys. Chem. 72, 101–109.

    Article  Google Scholar 

  • Sneyd, J., Wetton, B.T.R., Charles, A.C., Sanderson, M.J., 1995. Intercellular calcium waves mediated by diffusion of inositol trisphosphate: A two-dimensional model. Am. J. Physiol. Cell Physiol. 37, 1537–1545.

    Google Scholar 

  • Wallingford, J.B., Ewald, A.J., Harland, R.M., Fraser, S.E., 2002. Calcium signalling during convergent extension in Xenopus. Curr. Biol. 11, 652–661.

    Article  Google Scholar 

  • Wilkins, M., Sneyd, J., 1998. Intercellular spiral waves of calcium. J. Theor. Biol. 191, 299–308.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Roose.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roose, T., Chapman, S.J. & Maini, P.K. A Mathematical Model for Simultaneous Spatio-Temporal Dynamics of Calcium and Inositol 1,4,5-Trisphosphate in Madin–Darby Canine Kidney Epithelial Cells. Bull. Math. Biol. 68, 2027–2051 (2006). https://doi.org/10.1007/s11538-006-9064-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-006-9064-1

Keywords

Navigation