Summary
Progesterone initiates the resumption of the meiotic divisions in the amphibian oocyte. Depolarization of theRana pipiens oocyte plasma membrane begins 6–10 hr after exposure to progesterone (1–2 hr before nuclear breakdown). The oocyte cytoplasm becomes essentially isopotential with the medium by the end of the first meiotic division (20–22 hr). Voltage-clamp studies indicate that the depolarization coincides with the disappearance of an electrogenic Na+, K+-pump, and other electrophysiological studies indicate a decrease in both K+ and Cl− conductances of the oocyte plasma membrane. Measurement of [3H]-ouabain binding to the plasma-vitelline membrane complex indicates that there are high-affinity (K d-4.2×10−8 m), K+-sensitive ouabain-binding sites on the unstimulated (prophase-arrest) oocyte and that ouabain binding virtually disappears during membrane depolarization. [3H]-Leucine incorporation into the plasma-vitelline membrane complex increased ninefold during depolarization with no significant change in uptake or incorporation into cytoplasmic proteins or acid soluble pool(s). This together with previous findings suggests that progesterone acts at a translational level to produce a cytoplasmic factor(s) that down-regulates the membrane Na+, K+-ATPase and alters the ion permeability and transport properties of both nuclear and plasma membranes.
Similar content being viewed by others
References
Belanger, A.M., Schuetz, A.W. 1975. Precocious induction of activation responses in amphibian oocytes by divalent ionophore A23187.Dev. Biol. 48:378–381
Cross, M.H., Cross, P.C., Brinster, R.L. 1973. Changes in membrane potential during mouse egg development.Dev. Biol. 33:412–416
Dumont, J.N., Brummett, A.R. 1978. Oogenesis inXenopus laevis (Daudin): V. Relationships between developing oocytes and their investing follicular tissues.J. Morphol. 155:73–98
Erlij, D., Grinstein, S. 1976. The number of sodium ion pumping sites in skeletal muscle and its modification by insulin.J. Physiol. (London) 259:13–31
Godeau, J.F., Schorderet-Slatkine, S., Hubert, P., Baulieu, E. E. 1978. Induction of maturation inXenopus laevis oocytes by a steroid linked to a polymer.Proc. Natl. Acad. Sci. USA 75:2353–2357
Ishikawa, K., Hanaoka, Y., Kondo, Y., Imai, K. 1977. Primary action of steroid hormone at the surface of amphibian oocyte in the induction of germinal vesicle breakdown.Mol. Cell. Endocrinol. 9:91–100
Kalimi, M., Ziegler, D., Morrill, G.A. 1979. Characterization of a progestin-binding macromolecule in the amphibian oocyte cytosol.Biochem. Biophy. Res. Commun 86:560–567
Keynes, R.D., Swan, R.C. 1959. The permeability of frog muscle fibres to lithium ions.J. Physiol. (London) 147:626–638
Kostellow, A.B., Ziegler, D., Morrill, G.A. 1980. Regulation of Ca2+ and cyclic AMP during the first meiotic division in amphibian oocytes by progesterone.J. Cyclic Nucleotide Res. 6:347–358
Lee, S.C., Steinhardt, R.A. 1981. pH changes associated with meiotic maturation in oocytes ofXenopus laevis.Dev. Biol. 85:358–369
Masui, Y. 1967. Relative roles of the pituitary, follicle cells and progesterone in the induction of oocyte maturation inRana pipiens.J. Exp. Zool. 117:365–376
Masui, Y., Markert, C.L. 1971. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes.J. Exp. Zool. 177:129–146
Molinari, A.M., Medici, N., Moncharmont, B., Puca, C.A. 1977. Estradiol receptor of calf uterus: Interaction with heparin-agarose and purification.Proc. Natl. Acad. Sci. USA 74:4886–4890
Moreau, M., Guerrier, P., Dorée, M. 1976. Modifications précoces des proprietés électriques de la membrane plasmique des ovocytes deXenopus laevis au cours de la réiniation meiotique induite par la progestérone, la parachloromercuribenzoate (pCMB) ou l'ionophore A23187.C.R. Acad. Sci. Paris D. 282:1309–1312
Morrill, G.A., Kostellow, A.B., Murphy, J.B. 1971. Sequential forms of ATPase activity correlated with changes in cation binding and membrane potential from meiosis to first cleavage inR. pipiens.Exp. Cell Res. 66:289–298
Morrill, G.A., Kostellow, A.B., Murphy, J.B. 1975. Role of Na+, K+-ATPase in early embryonic development.Ann. N.Y. Acad. Sci. 242:543–559
Morrill, G.A., Schatz, F., Zabrenetzky, V.S. 1975. RNA and protein synthesis during progesterone-induced germinal vesicle breakdwon inR. pipiens ovarian tissue.Differentiation 4:143–152
Morrill, G.A., Watson, D.E. 1966. Transmembrane electropotential changes in amphibian eggs at ovulation, activation and first cleavage.J. Cell. Physiol. 67:85–92
Morrill, G.A., Ziegler, D. 1980. Na+ and K+ uptake and exchange by the amphibian oocyte during the first meiotic division.Dev. Biol. 74:216–223
Morrill, G.A., Ziegler, D.H., Kostellow, A.B. 1980. Kinetics of calcium efflux and exchange fromRana pipiens oocytes immediately following reiniation of the first meiotic division: Comparison of various meiotic agonists and antagonists.Cell Calcium 1:359–370
Petzelt, C., 1970. Ca2+-activated ATPase during the cell cycle of the sea urchinStrongylocentrotus purpuratus.Exp. Cell Res. 70:333–339
Smith, L.D., Ecker, R.E. 1969. Role of the oocyte nucleus in physiological maturation inRana pipiens.Dev. Biol. 19:281–309
Smith, L.D., Ecker, R.E., Subtelny, S. 1966. The initiation of protein synthesis in eggs ofRana pipiens.Proc. Natl. Acad Sci. USA 56:1724–1728
Wallace, R.A., Steinhardt, R.A. 1977. Maturation ofXenopus oocytes: II. Observations on the membrane potential.Dev. Biol. 57:305–316
Wasserman, W.J., Masui, Y. 1975. Effects of cycloheximide on a cytoplasmic factor initiating meiotic maturation inXenopus oocytes.Exp. Cell. Res. 91:381–388
Weinstein, S.P., Ziegler, D., Kostellow, A.B., Morrill, G.A. 1981. Sequential changes in plasma membrane properties ofRana oocytes during the first meiotic division.Fed. Proc. 40:611
Ziegler, D., Morrill, G.A. 1977. Regulation of the amphibian oocyte plasma membrane ion permeability by cytoplasmic factors during the first meiotic division.Dev. Biol. 60:318–325
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Weinstein, S.P., Kostellow, A.B., Ziegler, D.H. et al. Progesterone-induced down-regulation of an electrogenic Na+, K+-ATPase during the first meiotic division in amphibian oocytes. J. Membrain Biol. 69, 41–48 (1982). https://doi.org/10.1007/BF01871240
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01871240