A cell cycle-associated change in Ca2+ releasing activity leads to the generation of Ca2+ transients in mouse embryos during the first mitotic division

doi:10.1083/jcb.132.5.915

This Article

	Full Text (PDF, 1176K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Kono, T.
	Articles by Carroll, J.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Kono, T.
	Articles by Carroll, J.


Social Bookmarking

	What's this?

ARTICLES

A cell cycle-associated change in Ca2+ releasing activity leads to the generation of Ca2+ transients in mouse embryos during the first mitotic division

T Kono, KT Jones, A Bos-Mikich, DG Whittingham and J Carroll
Medical Research Council Experimental Embryology and Teratology Unit, St. George's Hospital Medical School, London, England.

We have used Ca2+-sensitive fluorescent dyes to monitor intracellular Ca2+ during mitosis in one-cell mouse embryos. We find that fertilized embryos generate Ca2+ transients at nuclear envelope breakdown (NEBD) and during mitosis. In addition, fertilized embryos arrested in metaphase using colcemid continue to generate Ca2+ transients. In contrast, parthenogenetic embryos produced by a 2-h exposure to strontium containing medium do not generate detectable Ca2+ transients at NEBD or in mitosis. However, when parthenogenetic embryos are cultured continuously in strontium containing medium Ca2+ transients are detected in mitosis but not in interphase. This suggests that mitotic Ca2+ transients are detected in the presence of an appropriate stimulus such as fertilization or strontium. The Ca2+ transient detected in fertilized embryos is not necessary for inducing NEBD since parthenogenetic embryos undergo nuclear envelope breakdown (NEBD). Also the first sign that NEBD is imminent occurs several minutes before the Ca2+ transient. The Ca2+ transient at NEBD appears to be associated with the nucleus since nuclear transfer experiments show that the presence of a karyoplast from a fertilized embryo is essential. Finally, we show that the intracellular Ca2+ chelator Bapta inhibits NEBD in fertilized and parthenogenetic embryos in a dose-dependent manner. These studies show that during mitosis there is an endogenous increase in Ca2+ releasing activity that leads to the generation of Ca2+ transients specifically during mitosis. The ability of Ca2+ buffers to inhibit NEBD regardless of the presence of global Ca2+ transients suggests that the underlying cell cycle-associated Ca2+ releasing activity may take the form of localized Ca2+ transients.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Li, Y., O'Neill, C., Day, M. L. (2009). Activation of a Chloride Channel by a Trophic Ligand Is Required for Development of the Mouse Preimplantation Embryo In Vitro. Biol. Reprod. 81: 759-767 [Abstract] [Full Text]
Whitaker, M. (2008). Calcium signalling in early embryos. Phil Trans R Soc B 363: 1401-1418 [Abstract] [Full Text]
Yoon, S.-Y., Fissore, R. A (2007). Release of phospholipase C {zeta}and [Ca2+]i oscillation-inducing activity during mammalian fertilization. Reproduction 134: 695-704 [Abstract] [Full Text]
Lee, B., Vermassen, E., Yoon, S.-Y., Vanderheyden, V., Ito, J., Alfandari, D., De Smedt, H., Parys, J. B., Fissore, R. A. (2006). Phosphorylation of IP3R1 and the regulation of [Ca2+]i responses at fertilization: a role for the MAP kinase pathway. Development 133: 4355-4365 [Abstract] [Full Text]
Kuroda, K., Ito, M., Shikano, T., Awaji, T., Yoda, A., Takeuchi, H., Kinoshita, K., Miyazaki, S. (2006). The Role of X/Y Linker Region and N-terminal EF-hand Domain in Nuclear Translocation and Ca2+ Oscillation-inducing Activities of Phospholipase C{zeta}, a Mammalian Egg-activating Factor. J. Biol. Chem. 281: 27794-27805 [Abstract] [Full Text]
Madgwick, S., Hansen, D. V., Levasseur, M., Jackson, P. K., Jones, K. T. (2006). Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. JCB 174: 791-801 [Abstract] [Full Text]
Whitaker, M. (2006). Calcium at Fertilization and in Early Development. Physiol. Rev. 86: 25-88 [Abstract] [Full Text]
Larman, M. G, Sheehan, C. B, Gardner, D. K (2006). Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 131: 53-61 [Abstract] [Full Text]
Zhang, D., Pan, L., Yang, L.-H., He, X.-K., Huang, X.-Y., Sun, F.-Z. (2005). Strontium promotes calcium oscillations in mouse meiotic oocytes and early embryos through InsP3 receptors, and requires activation of phospholipase and the synergistic action of InsP3. Hum Reprod 20: 3053-3061 [Abstract] [Full Text]
FitzHarris, G., Larman, M., Richards, C., Carroll, J. (2005). An increase in [Ca2+]i is sufficient but not necessary for driving mitosis in early mouse embryos. J. Cell Sci. 118: 4563-4575 [Abstract] [Full Text]
Philipova, R., Larman, M. G., Leckie, C. P., Harrison, P. K., Groigno, L., Whitaker, M. (2005). Inhibiting MAP Kinase Activity Prevents Calcium Transients and Mitosis Entry in Early Sea Urchin Embryos. J. Biol. Chem. 280: 24957-24967 [Abstract] [Full Text]
Larman, M. G., Saunders, C. M., Carroll, J., Lai, F. A., Swann, K. (2004). Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLC{zeta}. J. Cell Sci. 117: 2513-2521 [Abstract] [Full Text]
Marangos, P., FitzHarris, G., Carroll, J. (2003). Ca2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130: 1461-1472 [Abstract] [Full Text]
Krivokharchenko, A., Popova, E., Zaitseva, I., Vil'ianovich, L., Ganten, D., Bader, M. (2003). Development of Parthenogenetic Rat Embryos. Biol. Reprod. 68: 829-836 [Abstract] [Full Text]
FitzHarris, G., Marangos, P., Carroll, J. (2003). Cell Cycle-dependent Regulation of Structure of Endoplasmic Reticulum and Inositol 1,4,5-Trisphosphate-induced Ca2+ Release in Mouse Oocytes and Embryos. Mol. Biol. Cell 14: 288-301 [Abstract] [Full Text]
Hirooka, K., Bertolesi, G. E., Kelly, M. E. M., Denovan-Wright, E. M., Sun, X., Hamid, J., Zamponi, G. W., Juhasz, A. E., Haynes, L. W., Barnes, S. (2002). T-Type Calcium Channel alpha 1G and alpha 1H Subunits in Human Retinoblastoma Cells and Their Loss After Differentiation. J. Neurophysiol. 88: 196-205 [Abstract] [Full Text]
Gordo, A. C., Kurokawa, M., Wu, H., Fissore, R. A. (2002). Modifications of the Ca2+ release mechanisms of mouse oocytes by fertilization and by sperm factor. Mol Hum Reprod 8: 619-629 [Abstract] [Full Text]
Li, X., Morris, L. H.-A., Allen, W.R. (2002). In Vitro Development of Horse Oocytes Reconstructed with the Nuclei of Fetal and Adult Cells. Biol. Reprod. 66: 1288-1292 [Abstract] [Full Text]
Fenwick, J., Platteau, P., Murdoch, A.P., Herbert, M. (2002). Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro. Hum Reprod 17: 407-412 [Abstract] [Full Text]
Ogonuki, N., Sankai, T., Yagami, K., Shikano, T., Oda, S., Miyazaki, S., Ogura, A. (2001). Activity of a Sperm-Borne Oocyte-Activating Factor in Spermatozoa and Spermatogenic Cells from Cynomolgus Monkeys and Its Localization after Oocyte Activation. Biol. Reprod. 65: 351-357 [Abstract] [Full Text]
Tang, T., Dong, J., Huang, X., Sun, F. (2000). Ca(2+) oscillations induced by a cytosolic sperm protein factor are mediated by a maternal machinery that functions only once in mammalian eggs. Development 127: 1141-1150 [Abstract]
Levasseur, M, McDougall, A (2000). Sperm-induced calcium oscillations at fertilisation in ascidians are controlled by cyclin B1-dependent kinase activity. Development 127: 631-641 [Abstract]
Wang, J, Mayernik, L, Schultz, J., Armant, D. (2000). Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development 127: 33-44 [Abstract]
Goud, P.T., Goud, A.P., Van Oostveldt, P., Dhont, M. (1999). Presence and dynamic redistribution of type I inositol 1,4,5-trisphosphate receptors in human oocytes and embryos during in-vitro maturation, fertilization and early cleavage divisions. Mol Hum Reprod 5: 441-451 [Abstract] [Full Text]
Pey, R., Vial, C., Schatten, G., Hafner, M. (1998). Increase of intracellular Ca2+ and relocation of E-cadherin during experimental decompaction of mouse embryos. Proc. Natl. Acad. Sci. USA 95: 12977-12982 [Abstract] [Full Text]
Emerson, M., Travis, A. R., Bathgate, R., Stojanov, T., Cook, D. I., Harding, E., Lu, D. P., O'Neill, C. (2000). Characterization and Functional Significance of Calcium Transients in the 2-Cell Mouse Embryo Induced by an Autocrine Growth Factor. J. Biol. Chem. 275: 21905-21913 [Abstract] [Full Text]
Sotomaru, Y., Kawase, Y., Ueda, T., Obata, Y., Suzuki, H., Domeki, I., Hatada, I., Kono, T. (2001). Disruption of Imprinted Expression of U2afbp-rs/U2af1-rs1 Gene in Mouse Parthenogenetic Fetuses. J. Biol. Chem. 276: 26694-26698 [Abstract] [Full Text]