The path of calcium in cytosolic calcium oscillations: a unifying hypothesis.

Abstract

Data from 42 systems have been assembled in which the overall spatial course of relatively natural, intracellular calcium pulses has been or can be determined. These include 21 cases ofsolitary pulses in activating eggs and 21 cases of periodic (as well as solitary) pulses in various fully active cells. In all cases, these pulses prove to be waves of elevated calcium that travel from one pole of a cell to the other or from the periphery inward. The velocities of these waves are remarkably conserved-at -10 pm/sec in activating eggs and -25 pxm/sec in other cells at room temperature. Moreover, in three cases, the data suffice to show that these velocities fit the Luther equation for a reaction/diffusion wave of calcium through the cytosol. It is proposed that (i) natural intracellular calcium pulses quite generally take the form of cytosolic calcium waves and (ii) cytoplasmically controlled calcium waves are triggered and then propagated by the successive action of two distinct modes of calcium-induced calcium release. First, in the lumenal mode, a slow increase of calcium within the lumen of the endoplasmic reticulum reaches a level that triggers fast lumenal release as well as fast localized release into the cytosol. Then, the well-known cytosolic mode drives a reaction/diffusion wave across or into the cell.

Synchronized calcium spiking resulting from spontaneous calcium action potentials in monolayers of NRK fibroblasts

“…The velocity of the signal underlying the virtually synchronous increase in [Ca2+]j signal would be, therefore, at least 1000 p,m/s. This is considerably higher than the fastest measured intracellular Ca2+ wave (160 pm/s; [21]) and rules out the possibility of a diffusible second messenger that triggers the Ca2+ spikes, but instead suggests an electrical signal.…”

“…The fastest velocity of an intracellular Ca2+ wave has been reported to occur in heart myocytes and was 160 \xm/s [21], while the velocity of intercellular Ca2+ waves is in the range of 2-20 \xm/s [35],…”

Calcium signalling in early embryos

“…Fertilization calcium waves are a subset of the class of calcium waves of this velocity, which are found widely in both germ line and somatic cells ( Jaffe 1995( Jaffe , 2008. Jaffe presents the evidence that these are, in terms of chemistry, reactiondiffusion waves analogous to the well-known BelousovZhabotinsky reaction (Speksnijder et al 1989;Jaffe 1991Jaffe , 2008. The major source of calcium for the wave is the ER (Galione et al 1991;Terasaki & Jaffe 1991;Kline 2000), which is charged with calcium by a SERCA pump (Kline & Kline 1992b;Jones et al 1995;Lawrence & Cuthbertson 1995;Lee & Aarhus 2000).…”

Flipping the switch: How a sperm activates the egg at fertilization

“…3; Whitaker and Swann, 1993;Evans and Kopf, 1998;Parrington, 2001). The first model was based around the idea that the sperm introduced a bolus of Ca 2ϩ during gamete fusion (Jaffe, 1983(Jaffe, , 1991, later modified to the suggestion that channels in the surface membrane of the sperm allowed it to act as a conduit for Ca 2ϩ entry (Creton and Jaffe, 2001). Ca 2ϩ introduced in this way would then act to trigger Ca 2ϩ induced Ca 2ϩ release (CICR) within the egg (Jaffe, 1991).…”

“…The first model was based around the idea that the sperm introduced a bolus of Ca 2ϩ during gamete fusion (Jaffe, 1983(Jaffe, , 1991, later modified to the suggestion that channels in the surface membrane of the sperm allowed it to act as a conduit for Ca 2ϩ entry (Creton and Jaffe, 2001). Ca 2ϩ introduced in this way would then act to trigger Ca 2ϩ induced Ca 2ϩ release (CICR) within the egg (Jaffe, 1991). Although attractive in its straightforwardness, and consistent with the finding that sperm-egg fusion in both the sea urchin and the mouse always precedes egg Ca 2ϩ release (McCulloh and Chambers, 1992;Lawrence et al, 1997), a number of studies have now cast doubt upon the validity of this model.…”