Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Oct;75(4):2088–2097. doi: 10.1016/S0006-3495(98)77651-9

Simulation of the fertilization Ca2+ wave in Xenopus laevis eggs.

J Wagner 1, Y X Li 1, J Pearson 1, J Keizer 1
PMCID: PMC1299881  PMID: 9746551

Abstract

In the preceding paper Fontanilla and Nuccitelli (Biophysical Journal 75:2079-2087 (1998)) present detailed measurements of the shape and speed of the fertilization Ca2+ wave in Xenopus laevis eggs. In order to help interpret their results, we develop here a computational technique based on the finite element method that allows us to carry out realistic simulations of the fertilization wave. Our simulations support the hypothesis that the physiological state of the mature egg is bistable, i.e., that its cytoplasm can accommodate two alternative physiological Ca2+ concentrations: a low concentration characteristic of the prefertilization state and a greatly elevated concentration characteristic of the state following the passage of the wave. We explore this hypothesis by assuming that the bistability is due to the release and re-uptake properties of the endoplasmic reticulum (ER) as determined by inositol trisphosphate (IP3) receptor/Ca2+ channels and sarcoendoplasmic reticulum calcium ATPase (SERCA) pumps. When combined with buffered diffusion of Ca2+ in the cytoplasm, our simulations show that inhomogeneities in the Ca2+ release properties near the plasma membrane are required to explain the temporal and spatial dependences of the shape and speed of these waves. Our results are consistent with an elevated IP3 concentration near the plasma membrane in the unfertilized egg that is augmented significantly near the site of fertilization. These gradients are essential in determining the concave shape of the Ca2+ fertilization wave front.

Full Text

The Full Text of this article is available as a PDF (283.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allbritton N. L., Meyer T., Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science. 1992 Dec 11;258(5089):1812–1815. doi: 10.1126/science.1465619. [DOI] [PubMed] [Google Scholar]
  2. Atri A., Amundson J., Clapham D., Sneyd J. A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys J. 1993 Oct;65(4):1727–1739. doi: 10.1016/S0006-3495(93)81191-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Babcock D. F., Herrington J., Goodwin P. C., Park Y. B., Hille B. Mitochondrial participation in the intracellular Ca2+ network. J Cell Biol. 1997 Feb 24;136(4):833–844. doi: 10.1083/jcb.136.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  5. Bezprozvanny I., Watras J., Ehrlich B. E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature. 1991 Jun 27;351(6329):751–754. doi: 10.1038/351751a0. [DOI] [PubMed] [Google Scholar]
  6. Busa W. B., Ferguson J. E., Joseph S. K., Williamson J. R., Nuccitelli R. Activation of frog (Xenopus laevis) eggs by inositol trisphosphate. I. Characterization of Ca2+ release from intracellular stores. J Cell Biol. 1985 Aug;101(2):677–682. doi: 10.1083/jcb.101.2.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Campanella C., Andreuccetti P., Taddei C., Talevi R. The modifications of cortical endoplasmic reticulum during in vitro maturation of Xenopus laevis oocytes and its involvement in cortical granule exocytosis. J Exp Zool. 1984 Feb;229(2):283–293. doi: 10.1002/jez.1402290214. [DOI] [PubMed] [Google Scholar]
  8. Charbonneau M., Grey R. D. The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis. Dev Biol. 1984 Mar;102(1):90–97. doi: 10.1016/0012-1606(84)90177-5. [DOI] [PubMed] [Google Scholar]
  9. De Young G. W., Keizer J. A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9895–9899. doi: 10.1073/pnas.89.20.9895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DeLisle S., Welsh M. J. Inositol trisphosphate is required for the propagation of calcium waves in Xenopus oocytes. J Biol Chem. 1992 Apr 25;267(12):7963–7966. [PubMed] [Google Scholar]
  11. Ferrell J. E., Jr, Machleder E. M. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science. 1998 May 8;280(5365):895–898. doi: 10.1126/science.280.5365.895. [DOI] [PubMed] [Google Scholar]
  12. Finch E. A., Turner T. J., Goldin S. M. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science. 1991 Apr 19;252(5004):443–446. doi: 10.1126/science.2017683. [DOI] [PubMed] [Google Scholar]
  13. Fontanilla R. A., Nuccitelli R. Characterization of the sperm-induced calcium wave in Xenopus eggs using confocal microscopy. Biophys J. 1998 Oct;75(4):2079–2087. doi: 10.1016/S0006-3495(98)77650-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Iino M. Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol. 1990 Jun;95(6):1103–1122. doi: 10.1085/jgp.95.6.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jaffe L. F. The path of calcium in cytosolic calcium oscillations: a unifying hypothesis. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9883–9887. doi: 10.1073/pnas.88.21.9883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jafri M. S., Keizer J. Diffusion of inositol 1,4,5-trisphosphate but not Ca2+ is necessary for a class of inositol 1,4,5-trisphosphate-induced Ca2+ waves. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9485–9489. doi: 10.1073/pnas.91.20.9485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jafri M. S., Keizer J. On the roles of Ca2+ diffusion, Ca2+ buffers, and the endoplasmic reticulum in IP3-induced Ca2+ waves. Biophys J. 1995 Nov;69(5):2139–2153. doi: 10.1016/S0006-3495(95)80088-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jouaville L. S., Ichas F., Holmuhamedov E. L., Camacho P., Lechleiter J. D. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature. 1995 Oct 5;377(6548):438–441. doi: 10.1038/377438a0. [DOI] [PubMed] [Google Scholar]
  19. Kaftan E. J., Ehrlich B. E., Watras J. Inositol 1,4,5-trisphosphate (InsP3) and calcium interact to increase the dynamic range of InsP3 receptor-dependent calcium signaling. J Gen Physiol. 1997 Nov;110(5):529–538. doi: 10.1085/jgp.110.5.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Keizer J., Li Y. X., Stojilković S., Rinzel J. InsP3-induced Ca2+ excitability of the endoplasmic reticulum. Mol Biol Cell. 1995 Aug;6(8):945–951. doi: 10.1091/mbc.6.8.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lechleiter J. D., Clapham D. E. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes. Cell. 1992 Apr 17;69(2):283–294. doi: 10.1016/0092-8674(92)90409-6. [DOI] [PubMed] [Google Scholar]
  22. Li Y. X., Rinzel J. Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J Theor Biol. 1994 Feb 21;166(4):461–473. doi: 10.1006/jtbi.1994.1041. [DOI] [PubMed] [Google Scholar]
  23. Marshall I. C., Taylor C. W. Regulation of inositol 1,4,5-trisphosphate receptors. J Exp Biol. 1993 Nov;184:161–182. doi: 10.1242/jeb.184.1.161. [DOI] [PubMed] [Google Scholar]
  24. Murray S. E. Patient assessment in the postanesthesia care unit: a critical care approach. J Post Anesth Nurs. 1989 Aug;4(4):232–238. [PubMed] [Google Scholar]
  25. Nuccitelli R. How do sperm activate eggs? Curr Top Dev Biol. 1991;25:1–16. doi: 10.1016/s0070-2153(08)60409-3. [DOI] [PubMed] [Google Scholar]
  26. Nuccitelli R., Yim D. L., Smart T. The sperm-induced Ca2+ wave following fertilization of the Xenopus egg requires the production of Ins(1, 4, 5)P3. Dev Biol. 1993 Jul;158(1):200–212. doi: 10.1006/dbio.1993.1179. [DOI] [PubMed] [Google Scholar]
  27. Parker I., Ivorra I. Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: a possible mechanism for oscillatory release of Ca2+. Proc Natl Acad Sci U S A. 1990 Jan;87(1):260–264. doi: 10.1073/pnas.87.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Parys J. B., Sernett S. W., DeLisle S., Snyder P. M., Welsh M. J., Campbell K. P. Isolation, characterization, and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. J Biol Chem. 1992 Sep 15;267(26):18776–18782. [PubMed] [Google Scholar]
  29. Ridgway E. B., Gilkey J. C., Jaffe L. F. Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A. 1977 Feb;74(2):623–627. doi: 10.1073/pnas.74.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schaff J., Fink C. C., Slepchenko B., Carson J. H., Loew L. M. A general computational framework for modeling cellular structure and function. Biophys J. 1997 Sep;73(3):1135–1146. doi: 10.1016/S0006-3495(97)78146-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sims C. E., Allbritton N. L. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate by the oocytes of Xenopus laevis. J Biol Chem. 1998 Feb 13;273(7):4052–4058. doi: 10.1074/jbc.273.7.4052. [DOI] [PubMed] [Google Scholar]
  32. Snow P., Yim D. L., Leibow J. D., Saini S., Nuccitelli R. Fertilization stimulates an increase in inositol trisphosphate and inositol lipid levels in Xenopus eggs. Dev Biol. 1996 Nov 25;180(1):108–118. doi: 10.1006/dbio.1996.0288. [DOI] [PubMed] [Google Scholar]
  33. Taylor C. T., Lawrence Y. M., Kingsland C. R., Biljan M. M., Cuthbertson K. S. Oscillations in intracellular free calcium induced by spermatozoa in human oocytes at fertilization. Hum Reprod. 1993 Dec;8(12):2174–2179. doi: 10.1093/oxfordjournals.humrep.a137999. [DOI] [PubMed] [Google Scholar]
  34. Terasaki M., Jaffe L. A., Hunnicutt G. R., Hammer J. A., 3rd Structural change of the endoplasmic reticulum during fertilization: evidence for loss of membrane continuity using the green fluorescent protein. Dev Biol. 1996 Nov 1;179(2):320–328. doi: 10.1006/dbio.1996.0263. [DOI] [PubMed] [Google Scholar]
  35. Terasaki M., Slater N. T., Fein A., Schmidek A., Reese T. S. Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7510–7514. doi: 10.1073/pnas.91.16.7510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wagner J., Keizer J. Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys J. 1994 Jul;67(1):447–456. doi: 10.1016/S0006-3495(94)80500-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watras J., Bezprozvanny I., Ehrlich B. E. Inositol 1,4,5-trisphosphate-gated channels in cerebellum: presence of multiple conductance states. J Neurosci. 1991 Oct;11(10):3239–3245. doi: 10.1523/JNEUROSCI.11-10-03239.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yim D. L., Opresko L. K., Wiley H. S., Nuccitelli R. Highly polarized EGF receptor tyrosine kinase activity initiates egg activation in Xenopus. Dev Biol. 1994 Mar;162(1):41–55. doi: 10.1006/dbio.1994.1065. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES