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Electrical maturation of the murine oocyte: an increase in calcium current coincides withacquisition of meiotic competence

Published online by Cambridge University Press:  26 September 2008

Joan M. Murnane  and
Louis J. DeFelice
Joan M. Murnane
Affiliation:
Emory University School of Medicine, Atlanta, Georgia, USA
Louis J. DeFelice*
Affiliation:
Emory University School of Medicine, Atlanta, Georgia, USA
*
Louis J. DeFelice, Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, GA 30322, USA.
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Summary

We have used the whole-cell recording technique to compare three stages of primary and secondary oocytes from F1 hybrid mice (C57BL/6J x SJL/J):neonatal germinal vesicle (NGV) stage primary oocytes from 10- to 20-day-old, prepubescent mice; mature germinal vesicle (MGV) stage primary oocytes from 12-week-old, post-pubescent, superovulated mice; first polar body (FPB) stage secondary oocytes from 12-week-old, post-pubescent mice during the normal oestrus cycle or following superovulation. NGV, MGV and FPB oocytes all exhibit two voltage-dependent currents: an inward, rapidly activating/inactivating current, and an outward, slowly activating/non-inactivating current. In 1.5 mmol/1 external Ca the average peak inward current is − 2.9, − 12.4 and − 13.8 μA/cm2 in NGV, MGV and FPB oocytes, respectively. In 20 mmol/1 Ca these currents increase and the reversal potential shifts to the right. The outward current decreases slightly with growth and development: at 40 mV test potentials, NGV oocytes have average outward currents of 8.9 μA/cm2, and MGV and FPB oocytes have currents of 5.0 and 5.5 μA/cm2, respectively. Thus, MGV oocytes express FPB current patterns. The reversal potentials, kinetics and pharmacology of the currents indicate that Ca channels carry the inward current and K channels carry the outward current. During growth in vivo a gradual depolarisation accompanies maturation. Resting potentialsranged from − 45 to − 30 mV in NGV oocytes to − 35 to − 17 mV in MGV oocytes to − 20 mV to − 3 mV in FPB oocytes. These data suggest that a selective increase occurs in the number of Ca channels during oocyte growth. This increase precedes nuclear maturation and coincides with the acquisition of meiotic competence.

Keywords

Oocyte maturationcalcium channelswhole-cell voltage clampmeiotic competence
Type
Article
Information
Zygote , Volume 1 , Issue 1 , February 1993 , pp. 49 - 60
Copyright
Copyright © Cambridge University Press 1993

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References

Anderson, E. & Albertini, D.F. (1976). Gap junction between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 71, 680–6.CrossRefGoogle ScholarPubMed
Ayalon, D.A., Tsafriri, A., Linder, H.R., Cordova, T. & Harell, A. (1972). Serum gonadotrophin levels in pro-oestrus rats in relation to the resumption of meiosis by the oocytes J. Reprod. Fert. 317, 51–8.CrossRefGoogle Scholar
Bae, I.-H. & Channing, C. (1985). Effects of Ca ion on the maturation of cumulus-enclosed pig follicular oocytes isolated from medium-sized Graafian follicles. Biol.Reprod. 33, 79–87.CrossRefGoogle Scholar
Bar-Ami, S. & Tsafriri, A. (1981). Acquisition of meiotic competence in the rat: role of gonadotrophin and estrogen. Gamete Res. 4, 463–72.CrossRefGoogle Scholar
Batta, S.K. & Knudsen, J.F. (1980). Ca concentration in cumulus enclosed oocytes of rats after treatment with pregnant mare's serum. Biol. Reprod. 22, 243–6.CrossRefGoogle Scholar
Bornslaeger, E.A., Poueymirou, W.T., Mattei, P. & Schultz, R.M. (1986). Effects of protein kinase C activator on germinal vesicle breakdown and polar body emission of mouse oocytes. Exp. Cell Res. 165, 507–17.CrossRefGoogle ScholarPubMed
Chambers, et al. (1974). The activation of sea urchin eggs by the divalent ionophore A23187 and X-537a. Biochem. Biophys. Res. Commun. 60, 126–132.CrossRefGoogle ScholarPubMed
Channing, C.P. & Tsafriri, A. (1977). Mechanisms of action of luteinizing hormone and follicle stimulating hormone on the ovary in vitro. Metabolism 26, 413–68.CrossRefGoogle ScholarPubMed
Cho, W.K., Stern, S. & Biggars, J.D. (1974). Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187, 383–6.CrossRefGoogle ScholarPubMed
Clapham, D.E. & DeFelice, L.J. (1984). Voltage-gated K channels in embryonic chick heart. Biophys. J. 43, 38–9.Google Scholar
Cross, M.H., Cross, P.C. & Brinster, R.L. (1973). Changes in membrane potential during mouse egg development. Dev. Biol. 33, 412–16.CrossRefGoogle ScholarPubMed
Dawson, J.E. & Conrad, J.T. (1972). The effect of human chorionic gonadotrophin and luteinizing hormone upon the membrane potential of unovulated frog oocytes. Biol.Reprod. 6, 58–66.CrossRefGoogle ScholarPubMed
DeFelice, L.J., Mazzanti, J., Murnane, J. & Cohen, J. (1988). Patch-clamp and whole-cell recording from human oocytes. Biophys. J. 53, 547a.Google Scholar
DeFelici, M. & Siracusa, G. (1982). Survival of isolated, fully grown mouse ovarian oocytes in strictly dependent on external Ca2+. Dev. Biol. 92, 539–43.CrossRefGoogle Scholar
Dekel, N. & Beers, W.H. (1980). Development of the rat oocyte in vitro: inhibition and induction of maturation in the presence or absence of the cumulus oophorus. Dev.Biol. 75, 247–54.CrossRefGoogle ScholarPubMed
Dekel, N., Aberdam, E. & Sherizly, I. (1984). Spontaneous maturation in vitro of cumulus-enclosed rat oocytes is inhibited by forskolin. Biol. Reprod. 31, 244–50.CrossRefGoogle ScholarPubMed
Donahue, R.P. (1968). Maturation of the mouse oocyte in vitro. I. Sequence and timing of nuclear progression. Exp. Zool. 169, 237–301.CrossRefGoogle ScholarPubMed
Downs, S.M. & Eppig, J.J. (1986). The role of purines in the maintenance of meiotic arrest in mouse oocytes. Tokai J. Exp. Clin. Med. 11, 463–9.Google ScholarPubMed
Downs, S.M., Daniel, S.A. & Eppig, J.J. (1988). Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool., 245, 86–96.CrossRefGoogle ScholarPubMed
Ducibella, T.A., Anderson, D.F., Albertini, F., Aalberg, J. & Rangarajan, S. (1988). Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during maturation. Dev. Biol. 130, 184–97.CrossRefGoogle ScholarPubMed
Dullart, J.,Kent, J. & Ryle, M. (1975). Serum gonadotrophin concentration in infantile mice. J. Reprod. Fertil. 43, 189–92.CrossRefGoogle Scholar
Edwards, R.G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–51.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1977). Mouse development in vitro with various culture systems. Dev. Biol. 60, 371–88.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1979). A comparison between oocytes grown in co-culture with granulosa cells and oocytes with granulosa cell-oocyte junctional contact maintained in vitro. J. Exp. Zool. 209, 345–53.CrossRefGoogle Scholar
Eppig, J.J. (1982). The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev. Biol. 119, 313–21.CrossRefGoogle Scholar
Eppig, J.J. & Downs, S.M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biol. Reprod. 30, 1–11.CrossRefGoogle ScholarPubMed
Eppig, J.J., Freter, R.R., Ward-Bailey, F. & Schultz, R.M. (1983). Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones, and a putative maturation-inhibitory factor. Dev. Biol. 100, 39–49.CrossRefGoogle Scholar
Erickson, G.F. & Sorensen, R.A. (1974). In vitro maturation of mouse oocytes isolated from late, middle and preantral Graafian follicles. J. Exp. Zool. 190, 123–7.CrossRefGoogle ScholarPubMed
Eusebi, F., Colonna, R. & Mangia, F. (1983). Development of membrane excitability in mammalian oocytes and early embryos. Gamete Res. 7, 39–47.CrossRefGoogle Scholar
Franchimont, P., Demoulin, A. & Valcke, J.C. (1988). Endocrine, paracrine and autocrine control of follicular development. Horm. Metab. Res. 20, 193–203.CrossRefGoogle ScholarPubMed
Fulton, B.F. & Whittingham, B.G. (1978). Activation of mammalian oocytes by intracellular injection of Ca. Nature 273, 149–51.CrossRefGoogle Scholar
Georgiou, P., Bountra, C., Bland, K.P. & House, C.R. (1984). Ca action potentials in unfertilized eggs of mice and hamsters. Exp. Physiol. 69, 365–80.CrossRefGoogle Scholar
Gilula, N.B., Epstein, M.L. & Beers, W.H. (1978). Cell-to-cell communication and ovulation. J. Cell Biol. 78, 58–75.CrossRefGoogle ScholarPubMed
Hasimoto, N. & Kishimoto, T. (1986). Cell cycle dynamic of maturation-promoting factor during mouse oocyte maturation. Tokai J. Exp. Med. 11, 471–7.Google Scholar
Heller, D.T. & Schultz, R.M. (1980). Ribonucleoside metabolism in mouse oocytes: metabolic cooperativity between fully-grown oocyte and cumulus cells. Exp. Zool. 214, 355–64.CrossRefGoogle ScholarPubMed
Heller, D.T., Cahill, D.M. & Schultz, R.M. (1981). Biochemical studies of mammalian oogenesis: metabolic cooperativity between granulosa cells and growing mouse oocytes. Dev. Biol. 84, 455–64.CrossRefGoogle ScholarPubMed
Hillensjo, T., Barnia, A., Nilsson, L., Herlitz, H. & Ahrin, K. (1974). Temporal relationship between serum LH levels and oocyte maturation in prepubertal rats injected with pregnant mare's serum gonadotropin. Endocrinology 95, 1762–6.CrossRefGoogle ScholarPubMed
Hillensjo, T., Channing, C.P., Pomerantz, S.H. & Schwartz-Kriporer, A. (1979). Intrafollicular control of oocyte maturation in the pig. In Vitro 15, 32–9.CrossRefGoogle ScholarPubMed
Igusa, Y., Miyazaki, S. & Yamashita, N. (1983). Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm. J. Physiol. (Lond.) 340, 633–47.CrossRefGoogle ScholarPubMed
Jagiello, G., Ducayen, M.B., Downey, R. & Jonassen, A. (1982). Alterations of mammalian oocyte meiosis I with divalent cations and calmodulin. Cell Ca 3, 153–62.CrossRefGoogle ScholarPubMed
Kaplan, R., Dekel, N. & Kracier, P.F. (1978). Acceleration of onset of oocyte maturation in vitro by luteinizing hormone. Gamete Res. 1, 59–63.CrossRefGoogle Scholar
Kline, D. (1988). Ca-dependent events at fertilization of the frog egg: injection of a Ca buffer blocks ion channel opening, exocytosis, and formation of pronuclei. Dev. Biol. 126, 346–61.CrossRefGoogle Scholar
Kubiak, J.Z. (1989). Mouse oocytes gradually develop the capacity for activation during the metaphase II arrest. Dev. Biol. 136, 537–5.CrossRefGoogle ScholarPubMed
Lawrence, T.S., Beers, W.H. & Gilula, N.B. (1978). Transmission of hormonal stimulation by cell-to-cell communication. Nature 272, 501–7.CrossRefGoogle ScholarPubMed
Magnusson, C. & Hillensjo, T. (1977). Inhibition of maturation and metabolism in rat oocytes by cyclic AMP. J. Exp. Zool. 201, 139–41.CrossRefGoogle ScholarPubMed
Maller, J.L. & Krebs, E.G. (1980). Regulation of oocyte maturation.. Curr. Top. Cell Regul. 16, 271–311.CrossRefGoogle ScholarPubMed
Martin, R.B. and Richardson, F.S. (1979). Lanthanum as probes for calcium in biological systems. Quart. Rev. Biophys. 12, 181–209.CrossRefGoogle Scholar
Maruska, D.V., Leibfreid, M.L. & First, N.L. (1984). Role of Ca and Ca–calmodulin complex in resumption of meiosis, Electrical maturation of the murine oocyte 59 cumulus expansion, viability, and hyaluronidase sensitivity of bovine cumulus–oocyte complexes. Biol. Reprod. 31, 1–6.CrossRefGoogle Scholar
Masui, Y. & Clarke, H.J. (1979). Oocyte maturation. Int. J. Cytol. 57, 185–282.CrossRefGoogle ScholarPubMed
Masui, Y., Meyerhof, P.G., Miller, M.A. & Wasserman, W.J. (1977). Roles of divalent cations in maturation and activation of vertebrate oocytes. Differentiation 9, 49–57.CrossRefGoogle ScholarPubMed
Moor, R.M., Smith, M.W. & Dawson, R.M.C. (1980). Measurement of intracellular coupling between oocytes and cumulus cells using intracellular markers. Exp. Cell Res. 126, 15–29.CrossRefGoogle ScholarPubMed
Moor, R.M., Osborn, J.C., Cran, D.G. & Walters, D.E. (1981). Selective effect of gonadotrophins on cell coupling, nuclear maturation, and protein synthesis in mammalian oocytes. Embryol. Exp. Morphol. 61, 347–65.Google ScholarPubMed
Moreau, M.P., Doree, M. & Guerrier, P. (1976). Electrophoretic introduction of Ca ions into the cortex of Xenopus laevis oocytes triggers meiosis reinitiation. J. Exp. Zool. 197, 443–9.CrossRefGoogle Scholar
Okamoto, H., Takahashi, K. & Yamashita, N. (1977). Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J. Physiol. (Lond.) 7, 465–95.CrossRefGoogle Scholar
Paleos, G.A. & Powers, R.D. (1981). The effect of Ca on the first meiotic division of the mammalian oocyte. J. Exp. Zool. 217, 409–16.CrossRefGoogle Scholar
Pedersen, T. & Peters, H. (1968). Proposal for a classification of oocytes and folliclesin the mouse ovary. J. Reprod. Fert. 17, 555–7.CrossRefGoogle Scholar
Peres, A. (1986). Resting membrane potential and inward current properties of mouse ovarian oocytes and eggs. Pflugers Arch. 407, 534–40.CrossRefGoogle ScholarPubMed
Peres, A. (1987). The Ca current of mouse egg measured in physiological Ca and temperature conditions. J. Physiol. (Lond.) 391, 573–88.CrossRefGoogle Scholar
Peters, H. (1962). The development of the mouse ovary from birth to puberty. Acta Endocrinol. (Copenh.) 62, 98–116.Google Scholar
Pincus, G. & Enzmann, E.V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro. I. The activation of ovarian eggs. J. Exp. Med. 62, 665–75.CrossRefGoogle ScholarPubMed
Powers, R.D. (1982). Changes in mouse oocyte membrane potential and permeability during meiotic maturation. J. Exp. Zool. 221, 365–71.CrossRefGoogle ScholarPubMed
Powers, R.D. & Biggers, J.D. (1976). Inhibition of mouse oocyte maturation by cell membrane potential hyperpolarization. J. Cell Biol. 70, 352a.Google Scholar
Powers, R.D. & Paleos, G.A. (1982). The combined effects of Ca and dibutyryl cyclic AMP on germinal vesicle breakdown in the mouse oocyte. Reprod. Fert. 66, 1–8.CrossRefGoogle Scholar
Powers, R.D. & Tupper, J.T. (1977). Developmental changes in membrane transport and permeability properties in the early mouse embryo. Dev. Biol. 56, 306–15.CrossRefGoogle Scholar
Preston, S.L., Parmer, T.G. & Behrman, H.R. (1987). Adenosine reverses Ca-dependent inhibition of follicle-stimulating hormone action and induction of maturation in cumulus-enclosed rat oocytes. Endocrinology 120, 1356–64.CrossRefGoogle Scholar
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during maturation in vivo and in vitro. Dev. Biol. 108, 191–202.CrossRefGoogle ScholarPubMed
Rasmussen, H. (1982). Ca as intracellular messenger in hormone action. Adv. Exp. Med. Biol. 151, 473–91.CrossRefGoogle Scholar
Reed, P.W. & Lardy, H.A. (1972). A23187: a divalent cation ionophore. Biol. Chem. 247, 6870–7.CrossRefGoogle ScholarPubMed
Reuter, H. (1973). Divalent cations as charge carriers in excitable membranes. Prog. Biophy. Mol. Biol. 26, 1–43.CrossRefGoogle ScholarPubMed
Richards, J.S. & Midgley, A.R. (1976). Protein hormone action: a key to understanding ovarian follicular and luteal cell development. Biol. Reprod. 14, 82–94.CrossRefGoogle Scholar
Salustri, A. & Siracusa, G. (1983). Metabolic coupling, cumulus expansion and meiotic resumption in mouse cumuli oophori cultured in vitro in the presence of FSH or cAMP, or stimulated in vivo by hCG. J. Reprod. Fert. 68, 335–41.CrossRefGoogle ScholarPubMed
Salustri, A.. Petrungaro, S., DeFelici, M., Conti, M. & Siracusa, G. (1985). Effect of follicle-stimulating hormone on cyclic adenosine monophosphate level and on meiotic maturation in mouse cumulus cell-enclosed oocytes cultured in vitro. Biol. Reprod. 33, 777–82.CrossRefGoogle ScholarPubMed
Schorderet-Slatkine, S. & Urner, F. (1986). Pharmacological manipulation of meiotic maturation in vitro: a comparative study between amphibian (Xenopus) and the mammalian (mouse) oocyte. Tokai J. Exp. Clin. Med. 6, 453–62.Google Scholar
Schuetz, A.W. (1974). Role of hormones in oocyte maturation. Biol. Reprod. 10, 150–78.CrossRefGoogle ScholarPubMed
Schuetz, A.W. (1975). Induction of nuclear breakdown and meiosis in Spisula solidissima oocytes by Ca ionophore. Exp. Zool. 191, 433–40.CrossRefGoogle Scholar
Schultz, R.M., Montgomery, R.R.Ward-Bailey, P.F. & Eppig, J.J. (1983). Regulation of oocyte maturation in the mouse: possible roles of intracellular cAMP and testosterone. Dev. Biol. 95, 294–304.CrossRefGoogle Scholar
Sorenson, R. & Wasserman, P.M. (1976). Relationship between growth and meiotic maturation of the mouse oocyte. Dev. Biol. 50, 531–6.CrossRefGoogle Scholar
Spitzer, N.C. (1979). Ion channels in development. Annu. Rev. Neurosci. 2, 363–97CrossRefGoogle ScholarPubMed
Steinhardt, R.A.Epel, D., Carroll, E.F. & Yanagimachi, R. (1974). Is Ca ionophore a universal activator for unfertilized eggs? Nature 252, 41–3.CrossRefGoogle Scholar
Szbek, K. (1972). In vitro maturation of oocytes from sexually immature mice. J. Endocrinol. 54, 527–8.CrossRefGoogle Scholar
Thibault, C. (1977). Are follicular maturation and oocyte maturation independent processes?. J. Reprod. Fert. 51, 1–15.CrossRefGoogle ScholarPubMed
Thibault, C. & Gerard, M. (1973). Cytoplasmic and nuclear maturation of rabbit oocyte in vitro. Annu. Rev. Anim. Biochem. Biophys. 13, 145–6.CrossRefGoogle Scholar
Thibault, C., Szollosi, D. & Gerard, M. (1987). Mammalian oocyte maturation. Reprod. Nutr. Dev. 27, 865–96.CrossRefGoogle ScholarPubMed
Tombes, R.M., Simerly, C., Borisk, G.C. & Shatten, G. (1992). Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca, whereas germinal vesicle breakdown is Ca independent in the mouse oocyte. J. Cell Biol. 117, 799–811.CrossRefGoogle ScholarPubMed
Tsafriri, A. & Channing, C.P. (1975 a).An inhibitory influence of granulosa cells and follicular fluid upon porcine oocyte meiosis in vitro. Endocrinology 96, 922–7.CrossRefGoogle ScholarPubMed
Tsafriri, A. & Channing, C.P. (1975 b). Influence of follicular maturation and culture conditions on the meiosis of pig oocytes in vitro. J. Reprod. Fert. 43, 149–52.CrossRefGoogle ScholarPubMed
Tsafriri, A. & Kraicer, P.F. (1972). The time sequence of ovum maturation in the rat. Reprod. Fert. 29, 387–93.CrossRefGoogle ScholarPubMed
Tsafriri, A., Linder, H.R., Zor, U. & Lamprecht, S.A. (1972). In vitro induction of meiotic division in follicle-enclosed rat oocytes by LH, cyclic AMP, and prostaglandin E2. Reprod. Fert. 31, 39–50.CrossRefGoogle Scholar
Tsafriri, A., Pomerantz, S. & Channing, C.P. (1976). Inhibition of oocyte maturation by porcine follicular fluid: partial characterization of the inhibitor. Biol. Reprod. 14, 511–16.CrossRefGoogle ScholarPubMed
Tupper, J.T. (1974). Inhibition of increased K permeability following fertilization of the echinoderm embryo: its relationship to the initiation of protein synthesis and K exchangeability. Dev. Biol. 38, 332–5.CrossRefGoogle Scholar
Tupper, J.T. & Powers, R.D. (1973). Na and K permeability during early echinoderm development: electrophysiological and tracer-flux determination. J. Exp. Zool. 184, 356–64.CrossRefGoogle Scholar
Umezu, M., Hashizume, K. & Masaki, J. (1978). Follicular and oocyte maturation during the period of ovulation in immature rats pretreated with PMS. Jpn. J. Anim. Reprod. 24, 69–72.CrossRefGoogle Scholar
Wasserman, P.M., Josefowicz, W.J. & Letourneau, S.A. (1976). Meiotic maturation of mouse oocytes in vitro: inhibition of maturation at specific stages of nuclear progression. J. Cell Sci. 22, 532–45.Google Scholar
Wasserman, W.J. & Masui, Y. (1975). Initiation of meiotic maturation in Xenopus laevis oocytes by the combination of divalent cations and ionophore A23187. J. Exp. Zool. 193, 369–75.CrossRefGoogle ScholarPubMed
Weisenseel, M.H. & Jaffe, L.F. (1972). Membrane potential and impedance of developing fucoid eggs. Dev. Biol. 27, 555–74.CrossRefGoogle ScholarPubMed
Whitefield, J.F., Boyton, A.L., Macmanus, J.P., Sikorska, M. & Tsang, B.K. (1979). The regulation of cell proliferation by Ca and cyclic AMP. Mol. Cell. Biochem. 27, 155–79.CrossRefGoogle Scholar
Williams, (1976). Calcium chemistry and its relation to biological function. In Calcium in Biological Systems (Duncan, C.J., Eds.), pp. 1–17, Cambridge University Press, Cambridge.Google Scholar
Yamashita, N. (1982). Enhancement of ionic currents through voltage-gated channels in the mouse after fertilization. J. Physiol. (Lond.) 329, 263–80.CrossRefGoogle ScholarPubMed
Yoshida, S. (1982). Na and Ca spikes produced by ions passing through Ca channels in mouse ovarian oocytes. Pflugers Arch. 395, 84–6.CrossRefGoogle ScholarPubMed
Yoshida, S. (1983). Permeation of divalent and monovalent cations through the ovarian oocyte membrane of the mouse. J. Physiol. (Lond.) 339, 631–42.CrossRefGoogle ScholarPubMed