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Am J Physiol Cell Physiol 294: C917-C930, 2008. First published January 16, 2008; doi:10.1152/ajpcell.00181.2007
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MEMBRANE TRANSPORTERS, ION CHANNELS, AND PUMPS

Fast calcium wave propagation mediated by electrically conducted excitation and boosted by CICR

J. M. A. M. Kusters,1 W. P. M. van Meerwijk,2 D. L. Ypey,2 A. P. R. Theuvenet,2 and C. C. A. M. Gielen1

1Department of Biophysics and 2Department of Cell Biology, Radboud University Nijmegen, Nijmegen, The Netherlands

Submitted 2 May 2007 ; accepted in final form 13 January 2008

We have investigated synchronization and propagation of calcium oscillations, mediated by gap junctional excitation transmission. For that purpose we used an experimentally based model of normal rat kidney (NRK) cells, electrically coupled in a one-dimensional configuration (linear strand). Fibroblasts such as NRK cells can form an excitable syncytium and generate spontaneous inositol 1,4,5-trisphosphate (IP3)-mediated intracellular calcium waves, which may spread over a monolayer culture in a coordinated fashion. An intracellular calcium oscillation in a pacemaker cell causes a membrane depolarization from within that cell via calcium-activated chloride channels, leading to an L-type calcium channel-based action potential (AP) in that cell. This AP is then transmitted to the electrically connected neighbor cell, and the calcium inflow during that transmitted AP triggers a calcium wave in that neighbor cell by opening of IP3 receptor channels, causing calcium-induced calcium release (CICR). In this way the calcium wave of the pacemaker cell is rapidly propagated by the electrically transmitted AP. Propagation of APs in a strand of cells depends on the number of terminal pacemaker cells, the L-type calcium conductance of the cells, and the electrical coupling between the cells. Our results show that the coupling between IP3-mediated calcium oscillations and AP firing provides a robust mechanism for fast propagation of activity across a network of cells, which is representative for many other cell types such as gastrointestinal cells, urethral cells, and pacemaker cells in the heart.

gap junctions; calcium waves; pacemaking; electrical coupling; action potential propagation; inositol 1,4,5-trisphosphate receptor; normal rat kidney cell; calcium-induced calcium release


Address for reprint requests and other correspondence: C. C. A. M. Gielen, Dept. of Biophysics, Radboud Univ. Nijmegen, Geert Grooteplein 21, 6525 EZ Nijmegen, The Netherlands (e-mail: s.gielen{at}science.ru.nl)






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