Summary
Oocytes of Xenopus laevis were treated with agents which induce individual intracellular signals normally evoked during the process of meiotic maturation. Ultrastructural analysis of these oocytes allowed identification of specific second messengers that individually trigger single ultrastructural changes characteristic of the meiotic maturation process: Manipulation of intracellular cAMP levels induced changes in cortical granule position. Cytoplasmic alkalinization triggered a disruption of the annulate lamellae, a specialized organelle in the periphery of oocytes. Activation of protein kinase C caused rapid formation of a cortical endoplasmic reticulum and subsequent disruption of cortical granules. Manipulation of transmembrane calcium flux had varied results dependent upon the agent employed. Two of the treatments, Verapamil and zero external calcium, induced a reorganization in the oocyte periphery. The results indicate that these ultrastructural events are under the control of specific intracellular signals known to be elicited during meiotic maturation.
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References
Balinsky BI, Devis RJ (1963) Origin and differentiation of cytoplasmic structures in the oocytes of Xenopus laevis. Acta Morphol Embryol Exp 6:55–108
Baulieu E, Godeau F, Schorderet M, Schorderet-Slatkine S (1978) Steroid-induced meiotic division in Xenopus laevis oocytes: surface and calcium. Nature 275:593–598
Beebe SJ, Corbin JD (1987) Cyclic nucleotide-dependent protein kinases. In: Boyer PD, Krebs EG (eds) The Enzymes, Volume XVII, Control by Phosphorylation, Part A. Academic Press, New York, pp 44–113
Begg DA, Rehbun LI, Hyatt H (1982) Structural organization of actin in the sea urchin egg cortex: microvillar elongation in the absence of actin filament bundle formation. J Cell Biol 93:24–32
Berridge MJ (1984) Inositol trisphosphate and diacylglycerol as second messengers. Biochem J 220:345–360
Berridge MJ (1985) The molecular basis of communication within the cell. Sci Am 253(4):142–152
Bluemink JG (1972) Cortical woundhealing in the amphibian egg: and electron microscopical study. J Ultrastruct Res 41:95–114
Brachet J, Hanocq F, Van Gansen P (1970) A cytochemical and ultrastructural analysis of in vitro maturation in amphibian oocytes. Dev Biol 21:157–195
Bravo R, Otero C, Allende CC, Allende JE (1978) Amphibian oocyte maturation and protein synthesis: Related inhibition by cyclic AMP, theophylline, and papaverine. Proc Natl Acad Sci USA 75(3):1242–1246
Campanella C, Andreuccetti P (1977) Ultrastructural observations on cortical endoplasmic reticulum and on residual cortical granules in the egg of Xenopus laevis. Dev Biol 56:1–10
Campanella C, Andreuccetti P, Taddei C, Talevi R (1984) The modifications of cortical endoplasmic reticulum during in vitro maturation of Xenopus laevis oocytes and its involvement in cortical granule exocytosis. J Exp Zool 229:283–293
Capco DG, Mecca MD (1988) Analysis of proteins in the peripheral and central regions of amphibian oocytes and eggs. Cell Differ 23:155–164
Carafoli E (1987) Intracellular calcium homeostasis. Ann Rev Biochem 56:395–434
Carron CP, Longo FJ (1982) Relation of cytoplasmic alkalinization to microvillar elongation and microfilament formation in the sea urchin egg. Dev Biol 89:128–137
Charbonneau M, Grey RD (1984) The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis. Dev Biol 102:90–97
Charbonneau M, Webb DJ (1987) Weak bases partially activate Xenopus eggs and permit changes in membrane conductance whilst inhibiting cortical granule exocytosis. J Cell Sci 87:205–220
Cicirelli MF, Smith LD (1985) Cyclic AMP levels during the maturation of Xenopus oocytes. Dev Biol 108:254–258
Cicirelli MF, Robinson KR, Smith LD (1983) Internal pH of Xenopus oocytes: A study of the mechanism and role of pH changes during meiotic maturation. Dev Biol 100:133–146
Colombo R, Benedusi P, Valle G (1981) Actin in Xenopus development: Indirect immunofluorescence study of actin localization. Differentiation 20:45–51
Cork RJ, Cicirelli MF, Robinson KR (1987) A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. Dev Biol 121:41–47
Darnell J, Lodish H, Baltimore D (1986) Cell to cell signalling: hormones and receptors. In: Molecular Cell Biology. Scientific American Books, New York, pp 667–710
Gall L, Picheral B, Gounon P (1983) Cytochemical evidence for the presence of intermediate filaments and microfilaments in the egg of Xenopus laevis. Biol Cell 47:331–342
Gardiner DM, Grey RD (1983) Membrane junctions in Xenopus eggs: their distribution suggests a role in calcium regulation. J Cell Biol 96:1159–1163
Houle JG, Wasserman WJ (1983) Intracellular pH plays a role in regulating protein synthesis in Xenopus oocytes. Dev Biol 97:302–312
Imoh H, Okamoto M, Eguchi G (1983) Accumulation of annulate lamellae in the subcortical layer during progesterone-induced oocyte maturation in Xenopus laevis. Dev Growth Differ 25:1–10
Janis RA, Scriabine A (1983) Sites of action of Ca2+ channel inhibitors. Biochem Pharmacol 32:3499–3507
Kessel RG (1968) Annulate lamellae. J Ultrastruct Res [Suppl] 10:1–82
Kessel RG (1984) Annulate lamellae (porous cytomembranes): with particular emphasis on their possible role in differentiation of the female gamete. In: Browder LW (ed) Developmental Biology A Comprehensive Synthesis, Vol. 1, Oogenesis. Plenum, New York, pp 179–233
Kessel RG, Subtelny S (1981) Alteration of annulate lamellae in the in vitro progesterone-treated, full grown Rana pipiens oocyte. J Exp Zool 217:119–135
Larabell CA, Capco DG (1988) Role of calcium in the localization of maternal poly(A) + RNA and tubulin mRNA in Xenopus oocytes. Roux's Arch Dev Biol 197:175–183
Larabell CA, Chandler DE (1988) Freeze-fracture analysis of structural reorganization during meiotic maturation in oocytes of Xenopus laevis. Cell Tissue Res 251:129–136
Maller JL (1985) Regulation of amphibian oocyte maturation. Cell Differ 16:211–221
Maller JL, Butcher FR, Krebs EG (1979) Early effect of progesterone on levels of cyclic adenosine 3′:5′-monophosphate in Xenopus oocytes. J Biol Chem 254:579–582
Masui Y, Clark HJ (1979) Oocyte Maturation. Int Rev Cytol 57:185–282
Moreau M, Vilain JP, Guerrier P (1980) Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol 78:201–214
Nishizuka Y (1984) The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308:693–698
Nuccitelli R, Deamer D (Eds) (1982) Intracellular pH: Its measurement, regulation, and utilization in cellular functions. Kroc Found Ser 15: 1–586
O'Connor CM, Robinson KR, Smith LD (1977) Calcium, potassium, and sodium exchange by full grown and maturing Xenopus laevis oocytes. Dev Biol 61:28–40
Robinson KR (1979) Electrical currents through full-grown and maturing Xenopus oocytes. Proc Natl Acad Sci USA 76(2):837–841
Robinson KR (1985) Maturation of Xenopus oocytes is not accompanied by electrode-detectable calcium changes. Dev Biol 109:504–508
Schorderet-Slatkine S, Schorderet M, Baulieu EE (1982) Cyclic AMP-mediated control of meiosis: Effects of progesterone, cholera toxin and membrane-active drugs in Xenopus laevis oocytes. Proc Natl Acad Sci USA 79:850–854
Shiokawa K (1983) Mobilization of maternal mRNA in amphibian eggs with special reference to the possible role of membranous supramolecular structures. FEBS Lett 151(2):179–184
Speaker MG, Butcher FR (1977) Cyclic nucleotide fluctuations during steroid-induced meiotic maturation of frog oocytes. Nature 267:848–849
Stith BJ, Maller JL (1987) Induction of meiotic maturation in Xenopus oocytes by 12-O-tetradecanoylphorbol 13-acetate. Exp Cell Res 169:514–523
Tsutsui I, Ohkawa T, Nagai R, Kishimoto U (1987) Role of calcium ion in the excitability and electrogenic pump activity of the Chara corallina membrane: I. Effects of La3+, Verapamil, EGTA, W-7, and TFP on the action potential. J Membr Biol 96:65–73
Wallace RA, Jared D, Sega MW (1973) Protein incorporation by isolated amphibian oocytes III Optimum incubation conditions. J Exp Zool 184:321–334
Wasserman WJ, Houle JG (1984) The regulation of ribosomal protein S-6 phosphorylation in Xenopus oocytes: A potential role for intracellular pH. Dev Biol 101:436–445
Wasserman WJ, Penna MJ, Houle JG (1986) The regulation of Xenopus laevis oocyte maturation. In: Gall JG (ed) Gametogenesis and the Early Embryo. Alan R. Liss, Inc. New York, pp 111–130
Wasserman WJ, Pinto LH, O'Connor CM, Smith LD (1980) Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. Proc Natl Acad Sci USA 77(3):1534–1536
Yang C, Chou S, Taylor JD, Tchen TT (1987) Pigmentary organelle translocation in goldfish melanophores and xanthophores: Regulation by cAMP. J Cell Biol 105(4):35a
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Bement, W.M., Capco, D.G. Intracellular signals trigger ultrastructural events characteristic of meiotic maturation in oocytes of Xenopus laevis . Cell Tissue Res. 255, 183–191 (1989). https://doi.org/10.1007/BF00229080
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DOI: https://doi.org/10.1007/BF00229080