Hostname: page-component-745bb68f8f-d8cs5 Total loading time: 0 Render date: 2025-01-12T09:06:01.685Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcium and cell cycle control in early embryos

Published online by Cambridge University Press:  26 September 2008

Martin Wilding
Martin Wilding*
Affiliation:
Stazione Zoologica, Naples, Italy
*
M. Wilding, Stazione Zoologica, Villa Comunale, 80121 Naples, Italy Telephone: +39-81-583-3288. Fax: +39-81-583-3260.
Get access Rights & Permissions [Opens in a new window]

Extract

Over the past few years, we have witnessed a burgeoning series of papers addressing the role of calcium signalling in cell cycle control. In this review I will attempt to bring together all the diverse threads and discuss new concepts that have arisen from the most recent data. Because the major part of the data concerns mitosis/meiosis entry and exit, I have focused on these areas. I will jointly refer to meiotic and mitotic phases of the cell cycle as M-phase because these phases are highly comparable. Studies of the cell cycle involve a huge range of species, from plants to humans. I will, however, restrict this review to the work performed in early embryos. I apologise in advance to contributors to this field whose names I do not mention because they do not work on embryos.

Type
Commentary
Information
Zygote , Volume 4 , Issue 1 , February 1996 , pp. 1 - 6
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baitinger, C., Alderton, J., Peonie, M., Schulman, H. & Steinhardt, R.A. (1990). Multifunctional Ca2+/calmodulindependent protein kinase is necessary for nuclear envelope breakdown. J. Cell Biol. 111, 1763–73.CrossRefGoogle ScholarPubMed
Browne, C.L., Miller, A.L., Palazzo, R.E. & Jaffe, L.F. (1992). On the calcium pulse proceeding nuclear envelope breakdown in early sea urchin embryos. Biol. Bull. 177, 370–1.CrossRefGoogle Scholar
Ciapa, B., Pesando, D., Wilding, M., & Whitaker, M. (1994). Cell-cycle calcium transients driven by cyclic changes in inositol triphosphate levels. Nature 368, 875–8.CrossRefGoogle Scholar
Clothier, G., & Timourian, H. (1972). Calcium uptake and release by dividing sea urchin eggs. Exp. Cell Res. 78, 105–10.CrossRefGoogle Scholar
Cuthbertson, K. & Cobbold, P. (1985). Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell calcium. Nature 316, 541–2.CrossRefGoogle Scholar
Dorée, M. (1990). Control of M-phase by maturation promoting factor. Curr. Opin. Cell Biol. 2, 269–73.CrossRefGoogle ScholarPubMed
Finch, E., Turner, T., & Goldin, S. (1991). Calcium as a coagonist of inositol 1,4,5-trisphosphate induced calcium release. Science 252, 443–6.CrossRefGoogle ScholarPubMed
Forer, A. & Sillers, P.J. (1987). The role of the phosphatidyl-inositol cycle in mitosis in sea urchin zygotes. Exp. Cell Res. 170, 42–55.CrossRefGoogle ScholarPubMed
Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N. & Mikoshiba, K. (1989). Primary structure and functional expression of the inositol 1,4,5-trisphosphate binding protein P400. Nature 342, 32–8.CrossRefGoogle ScholarPubMed
Galione, A., & White, A. (1994). Calcium release induced by cyclic ADP ribose. Trends Cell Biol. 4, 431–6.CrossRefGoogle Scholar
Galione, A., Lee, H.C., & Busa, W.B. (1991). Calcium-induced calcium release in sea urchin egg homogenates: modulation by cyclic ADP ribose. Science 253, 1143–6.CrossRefGoogle ScholarPubMed
Gilkey, J.C., Jaffe, L.F., Ridgway, E.B., & Reynolds, G.T. (1978). A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J. Cell Biol. 76, 448–66.CrossRefGoogle ScholarPubMed
Grandin, N., & Charbonneau, M. (1991). Intracellular free calcium oscillates during cell division of Xenopus embryos. J. Cell Biol. 112, 711–18.CrossRefGoogle ScholarPubMed
Hafner, M. & Petzelt, C. (1987). Inhibition of mitosis by an antibody to the mitotic calcium transport system. Nature 330, 264–6.CrossRefGoogle Scholar
Han, J.-K., Fukami, K. & Nuccitelli, R. (1992). Reducing inositol lipid hydrolysis, Ins(1,4,5)P3 receptor availability, or Ca2+ gradients lengthens the duration of the cell cycle in Xenopus laevis blastomeres. J. Cell Biol. 116, 147–56.CrossRefGoogle ScholarPubMed
Heald, R., McLoughlin, M., & McKeon, F. (1993). Human weel maintains mitotic timing by protecting the nucleus from cytoplasmically activated cdc2 kinase. Cell 74, 463–74.CrossRefGoogle Scholar
Hepler, P.K. (1989). Calcium transients during mitosis: observations in flux. J. Cell Biol. 109, 2567–73.CrossRefGoogle ScholarPubMed
Hepler, P.K. (1992). Calcium and mitosis. Int. Rev. Cytol. 138, 239–68.CrossRefGoogle ScholarPubMed
Hepler, P.K. (1994). The role of calcium in cell division. Cell Calcium 16, 322–30.CrossRefGoogle ScholarPubMed
Igusa, Y. & Miyazaki, S. (1986). Periodic increase of cytoplasmic free calcium in fertilised hamster eggs measured with calcium-sensitive electrodes. J. Physiol.(Lond). 377, 193–205.CrossRefGoogle ScholarPubMed
Izant, J.G. (1983). The role of calcium ions during mitosis: calcium participates in the anaphase trigger. Chromosoma 88, 101–7.CrossRefGoogle ScholarPubMed
Jones, K., Carrol, J., Merriman, J., Whittingham, D. & Kono, T. (1995 a). Repetitive sperm-induced calcium transients in mouse oocytes are cell cycle-dependent. Development 121, 3259–66.CrossRefGoogle ScholarPubMed
Jones, K., Carrol, J. & Whittingham, D. (1995 b). Ionomycin, thapsigargin, ryanodine and sperm-induced calcium release during meiotic maturation of mouse oocytes. J. Biol. Chem. 270, 6671–7.CrossRefGoogle ScholarPubMed
Keating, T.J., Cork, R.J., & Robinson, K.R. (1994). Intracellular free calcium oscillations in normal and cleavage-blocked embryos and artificially activated eggs of Xenopus laevis. J. Cell Sci. 107, 2229–37.CrossRefGoogle ScholarPubMed
Kline, D. & Kline, J. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. FASEB J. A214, no.717.Google Scholar
Lai, F., Erickson, H., Rousseau, E., Liu, Q. & Meissner, G. (1988). Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331, 315–19.Google ScholarPubMed
Lohka, M.J. & Maller, J.L. (1985). Induction of nuclear envelope breakdown, chromosome condensation and spindle fromation in cell-free extracts. J. Cell Biol. 101, 518–23.CrossRefGoogle Scholar
Lorca, T., Fesquet, D., Galas, S., Devault, A., Cavadore, J.-E. & Dorée, M. (1991). Degradation of the proto-oncogene product p39mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca2+ calmodulin-dependent event. EMBO J. 10, 2087–93.CrossRefGoogle Scholar
Lorca, T., Cruzalegui, F.H., Fesquet, D., Cavadore, J.E., Méry, J., Means, A. & Dorée, M. (1993). Calmodulindependent protein kinase II mediates inactivation of MPF and CSF upon fertilisation of Xenopus eggs. Nature 366, 270–3.CrossRefGoogle ScholarPubMed
Lorca, T., Abrieu, A., Means, A., Dorée, M. (1994). Ca2+ is involved through type II calmodulin-dependent protein kinase in cyclin degradation and exit from metaphase. Biochim. Biophys. Acta 1223, 325–32.CrossRefGoogle ScholarPubMed
Masui, Y. & Markert, C. (1971). Cytoplasmic control of nuclear behaviour during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129–46.CrossRefGoogle ScholarPubMed
Mazia, D., Petzelt, C., Williams, R.O. & Meza, I. (1972). A Ca2+-activated ATPase in the mitotic apparatus of the sea urchin egg (isolated by a new method). Exp. Cell Res. 70, 325–32.CrossRefGoogle Scholar
Mignery, G., Sudhof, T., Takei, K. & De Camilli, P. (1998). Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature 342, 192–5.CrossRefGoogle Scholar
Minshull, J., Blow, J.J. & Hunt, T. (1989). Translation of cyclin mRNA is necessary for extracts of activated Xenopus eggs to enter mitosis. Cell 56, 947–56.CrossRefGoogle ScholarPubMed
Miyazaki, S., Hashimoto, N., Yoshimoto, Y., Kishimoto, T., Igusa, Y., & Hiramoto, Y. (1986). Temporal and spatial dynamics of the peridic increase in intracellular calcium at fertilisation of golden hamster eggs. Dev. Biol. 118, 259–67.CrossRefGoogle Scholar
Miyazaki, S., Shirakawa, H., Nakada, K., Honda, Y., Yuzaki, M., Nakade, S., & Mikoshiba, K. (1992 a). Antibody to the inositol trisphosphate receptor blocks thimerosalenhanced Ca2+-induced Ca2+ release and Ca2+ oscillations in hamster eggs. FEBS Lett. 309, 180–4.CrossRefGoogle Scholar
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakade, S., & Mikoshiba, K. (1992 b). Block of calcium wave and calcium oscillation by antibody to the inositol, 1,4,5-trisphosphate receptor in fertilised hamster eggs. Science 257, 251–5.CrossRefGoogle Scholar
Morgan, D. (1995). Principles of CDK regulation. Nature 374, 131–4.CrossRefGoogle ScholarPubMed
Morin, N., Abrieu, A., Lorca, T., Martin, F. & Dorée, M. (1994). The proteolysis-dependent metaphase to anaphase transition; calcium/calmodulin–dependent protein kinase II mediates onset of anaphase in extracts prepared from unfertilised Xenopus eggs. EMBO J. 13, 4343–52.CrossRefGoogle Scholar
Murray, A.W., & Kirschener, M.W. (1989). Cyclin synthesis drives the early embryonic cell cycle. Nature 339, 275–80.CrossRefGoogle ScholarPubMed
Murray, A.W., Solomon, M.J., & Kirschner, M.W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280–6.CrossRefGoogle ScholarPubMed
NewPort, J., & Kirschener, M.W. (1982). A major developmental transition in early Xenopus embryos. I. Characterisation and timing of cellular changes at the midblastula stage. Cell 30, 675–86.CrossRefGoogle Scholar
Nurse, P. (1990). Universal contorl mechanism regulating onset of M-phase. Nature 344, 503–8.CrossRefGoogle Scholar
Patel, R., Twigg, J., Crossley, I., Golsteyn, R. & Whitaker, M.J. (1989). Calcium-induced chromatin condensation and cyclin phosphorylation during chromatin condensation cycles in ammonia-activated sea urchin eggs. J. Cell Sci. Suppl. 12, 129–44.CrossRefGoogle ScholarPubMed
Patel, R., Twigg, J., Sheppard, B. & Whitaker, M. (1990). Calcium, cyclin and cell cycle control in sea urchin embryos. Dev. Biol. 125, 21–35.Google Scholar
Petzelt, C. (1972). Ca2+ activated ATPase during the cell cycle of the sea urchin Stronglyocentrotus purpuratus. Exp. Cell Res. 70, 333–9.CrossRefGoogle Scholar
Petzelt, C. & Auel, D. (1978). Purification and some properties of the mitotic Ca2+/ATPase. In Cell Reproduction, ed. Dirksen, E.R., Prescott, D.M. & Fox, C.F. pp. 487–94. New York: Academic Press.CrossRefGoogle Scholar
Petzelt, C. & Von Lederbur-Villiger, M. (1973). Ca2+-stimulated ATPase during the early development of parthenogenetically activated eggs of the sea urchin Paracentrotus lividus. Cell Res. 81, 87–94.CrossRefGoogle ScholarPubMed
Poenie, M., Alderton, J., Tsien, R.Y. & Steinhardt, R.A. (1985). Changes of free calcium levels with stages of the cell division cycle. Nature 315, 147–9.CrossRefGoogle ScholarPubMed
Poenie, M., Alderton, J., Steinhardt, R.A. & Tsien, R.Y. (1986). Calcium rises abruptly and briefly throughout the cell at the onset of anaphase. Science 233, 886–9.CrossRefGoogle ScholarPubMed
Rink, T.J., Tsien, R.Y., & Warner, A.E. (1980). Free calcium in Xenopus embryos measured with ion-selective microelectordes. Nature 283, 658–60.CrossRefGoogle Scholar
Ross, C., Meldolesi, J., Milner, T., Satoh, T., Suppattapone, S. & Sayder, S. (1989). Inositol 1,4,5-trisphosphate receptor localised to endoplasmic reticulum in cerebellar Purkinje neurons. Nature 339, 468–70.CrossRefGoogle ScholarPubMed
Schantz, A. (1985). Cytosolic free calcium-ion concentration in cleaving embryonic cells of Oryzias latipes measured with calcium-selective microelectrodes. J. Cell Biol. 100, 947–54.CrossRefGoogle ScholarPubMed
Silver, R.B. (1986). Mitosis in sand dollar embryos is inhibited by antibodies directed against the calcium transport enzyme of muscle. Proc. Natl. Acad. Sci. USA 83, 4302–6.CrossRefGoogle ScholarPubMed
Speksnijder, A., Sardet, C. & Jaffe, L. (1990). Periodic calcium waves cross ascidian eggs after fertilisation. Dev. Biol. 142, 246–9.CrossRefGoogle Scholar
Steinhardt, R.A. (1990). Intracellular free calcium and the first cell cycle of the sea urchina embryo. (Lytechinus pictus). J. Reprod. Fertil. Suppl. 42, 191–7.Google ScholarPubMed
Steinhardt, R.A. & Alderton, J., (1988). Intracellular free calcium rise triggers nuclear envelope breakdown in the sea urchin embryo. Nature 332, 364–6.CrossRefGoogle ScholarPubMed
Stricker, S. (1995). Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev. Biol. 170, 496–518.CrossRefGoogle ScholarPubMed
Sudhof, T., Newton, C., Archer, B., Ushkaryov, Y. & Mignery, G. (1991). Structure of a novel IP3 receptor. EMBO J. 10, 3199–206.CrossRefGoogle Scholar
Sun, F., Bradshaw, J., Galli, C. & Moor, R. (1994). Changes in intracellular calcium concentration in bovine oocytes following penetration by spermatozoa. J. Reprod. Fertil. 101, 713–19.CrossRefGoogle ScholarPubMed
Taylor, C., Lawrence, Y., Kingsland, C., Biljan, M. & Cuthbertson, K. (1993). Oscillations in intracellular free calcium induced by spermatozoa in human oocytes at fertilisation. Hum. Reprod. 8, 2174–9.CrossRefGoogle Scholar
Tombes, R.M., & Borisy, G.G. (1989). Intracellular free calcium and mitosis in mammalian cells: anaphase onset is calcium modulated, but is not triggered by a brief transient. J. Cell Biol. 109, 627–36.CrossRefGoogle Scholar
Tombes, R.M., Simerly, C., Borisy, G.G. & Schatten, G. (1992).Intracelluar free calcium and mitosis in mammalian dells: anaphase oneset is calcium modulated, but is not triggered by a brief transient,J. Cell Biol. 8. 2174–9.Google Scholar
Tombes, R.M., Simerly, C., Borisy, G.G. & Schatten, G. (1992). Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca2+ wherease germinal vesicle breakdown is Ca2+ independent in the mouse oocyte. J. Cell Biol. 117, 799–811.CrossRefGoogle Scholar
Twigg, J., Patel, R. & Whitaker, M. (1988). Translational control of InsP3-induced chromatin condensation during the early cell cycles of sea urchin embroyos. Nature 332, 366–9.CrossRefGoogle Scholar
Whitaker, M.J. (1995). Regulation of the cell division cycle by inositol trisphosphate and the calcium signalling pathway. Adv. Second Messenger Phosphoprotein Res. 30, 299–310.CrossRefGoogle Scholar
Whitaker, M. & Patel, R. (1990). Calcium and cell cycle control. Development 108, 525–42.CrossRefGoogle ScholarPubMed
Whitaker, M. & Steinhardt, R.A. (1982). Ionic regulation of egg activation. Q. Rev. Biophys. 15, 593–666.CrossRefGoogle ScholarPubMed
Whitaker, M. & Swann, K. (1993). Lighting the fuse at fertilisation. Development 117, 1–12.CrossRefGoogle Scholar