Sperm Initiate a Ca2+ Wave in Frog Eggs that is More Similar to Ca2+ Waves Initiated by IP3 than by Ca2+

Abstract

We have measured the initial propagation velocity of the sperm-induced Ca(2+) wave in the egg of Xenopus laevis and have compared it with the initial propagation velocities of the inositol triphosphate (IP(3))-induced and Ca(2+)-induced Ca(2+) waves. The initial mean propagation velocity of the sperm-induced wave (13 microm/s) is very similar to that of the IP(3)-induced waves (12.3 microm/s) and two times faster than the mean Ca(2+)-induced wave velocity (6.6 microm/s). We have generated realistic simulations of the fertilization wave in the frog egg using a computational technique based on the finite difference method. Modeling refinements presented here include equations for the production, degradation, and diffusion of IP(3), a description for Ca(2+) dynamics in the endoplasmic reticulum, and a highly concentrated endoplasmic reticulum in the egg cortex. We conclude that models incorporating sperm-induced IP(3) generation fit the data best and those involving the influx of either Ca(2+) or a diffusible sperm factor fit the data poorly. This independence from Ca(2+) influx is also supported by electrophysiological data indicating that Ca(2+) influx is not needed to maintain open Cl(-) channels that generate the fertilization potential.

Simulation of calcium waves in ascidian eggs: insights into the origin of the pacemaker sites and the possible nature of the sperm factor

“…We have indeed seen above [see section 'An artificial pacemaker site (PM3) is revealed by flash-photolysis of Ins(1,4,5)P3 or gPtdIns(4,5)P2'] that Ins(1,4,5)P3 appears to be a local messenger that cannot, through a single increase, induce repetitive Ca 2+ rises. By contrast, a theoretical study of the fertilization Ca 2+ wave in Xenopus oocyte (Bugrim et al, 2003) concludes that an elevated concentration of Ins(1,4,5)P3 near the site of fertilization appears as the most probable mechanism to reproduce the experimental observations. The contradiction between the latter theoretical results and ours can be explained by the fact that the study for Xenopus oocytes simulates the unique fertilization wave as a switch between a stable state with low cytosolic Ca 2+ and another stable state with a high cytosolic Ca 2+ .…”

“…It was shown that the correct shape of the fertilization wave in Xenopus oocyte can be reproduced by assuming that Ins(1,4,5)P3 is locally generated at the fertilization site (Bugrim et al, 2003). Moreover, these studies emphasize the role of the spatial inhomogeneities in the ER distribution (Bugrim et al, 2003;Hunding and Ipsen, 2003), in the Ins(1,4,5)P3Rs distribution (Bugrim et al, 2003) or in Ins(1,4,5)P3 production (Wagner et al, 1998) to reproduce the experimentally observed spatial profiles. None of these studies, however, deals with repetitive Ca 2+ waves, as those observed at fertilization of many species, including ascidians and mammals.…”

“…In the model, we have also assumed a higher ER density just below the plasma membrane to support the higher speed of propagation of the Ca 2+ waves in the ascidian egg cortex. Such an assumption was also found to be necessary to reproduce the correct shape of the fertilization Ca 2+ wave in frog eggs (Bugrim et al, 2003).…”

“…(1) If the ER density is modelled by taking into account the respective volumes accessible to both compartments (the ER and the cytosol), it represents a bifurcation parameter that can determine the excitability of a given part of the cell, unlike in other existing models (Wagner et al, 1998;Fink et al, 2000;Bugrim et al, 2003;Hunding et al, 2003). Under these conditions, the regions with higher ER density naturally play the role of pacemaker sites.…”

“…Some theoretical models have already investigated the spatial characteristics of the Ca 2+ increase occuring at fertilization (Wagner et al, 1998;Bugrim et al, 2003;Hunding and Ipsen, 2003). It was shown that the correct shape of the fertilization wave in Xenopus oocyte can be reproduced by assuming that Ins(1,4,5)P3 is locally generated at the fertilization site (Bugrim et al, 2003).…”