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Spontaneous and LH-induced maturation in Bufo arenarum oocytes: importance of gap junctions

Published online by Cambridge University Press:  01 February 2007

G. Sánchez Toranzo ,
J. Oterino ,
L. Zelarayán ,
F. Bonilla  and
M.I. Bühler
G. Sánchez Toranzo
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
J. Oterino
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
L. Zelarayán
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
F. Bonilla
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
*
All correspondence to: Marta I. Bühler, Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina. Fax: +54 381 424 8025. e-mail: [email protected]
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Summary

It has been demonstrated in Bufo arenarum that fully grown oocytes are capable of meiotic resumption in the absence of a hormonal stimulus if they are deprived of their follicular envelopes. This event, called spontaneous maturation, only takes place in oocytes collected during the reproductive period, which have a metabolically mature cytoplasm.

In Bufo arenarum, progesterone acts on the oocyte surface and causes modifications in the activities of important enzymes, such as a decrease in the activity of adenylate cyclase (AC) and the activation of phospholipase C (PLC). PLC activation leads to the formation of diacylglycerol (DAG) and inositol triphosphate (IP3), second messengers that activate protein kinase C (PKC) and cause an increase in intracellular Ca2+. Recent data obtained from Bufo arenarum show that progesterone-induced maturation causes significant modifications in the level and composition of neutral lipids and phospholipids of whole fully grown ovarian oocytes and of enriched fractions in the plasma membrane. In amphibians, the luteinizing hormone (LH) is responsible for meiosis resumption through the induction of progesterone production by follicular cells.

The aim of this work was to study the importance of gap junctions in the spontaneous and LH-induced maturation in Bufo arenarum oocytes. During the reproductive period, Bufo arenarum oocytes are capable of undergoing spontaneous maturation in a similar way to mammalian oocytes while, during the non-reproductive period, they exhibit the behaviour that is characteristic of amphibian oocytes, requiring progesterone stimulation for meiotic resumption (incapable oocytes).

This different ability to mature spontaneously is coincident with differences in the amount and composition of the phospholipids in the oocyte membranes. Capable oocytes exhibit in their membranes higher quantities of phospholipids than incapable oocytes, especially of PC and PI, which are precursors of second messengers such as DAG and IP3.

The uncoupling of the gap junctions with 1-octanol or halothane fails to induce maturation in follicles from the non-reproductive period, whose oocytes are incapable of maturing spontaneously. However, if the treatment is performed during the reproductive period, with oocytes capable of undergoing spontaneous maturation, meiosis resumption occurs in high percentages, similar to those obtained by manual defolliculation.

Interestingly, results show that LH is capable of inducing GVBD in both incapable oocytes and in oocytes capable of maturing spontaneously as long as follicle cells are present, which would imply the need for a communication pathway between the oocyte and the follicle cells. This possibility was analysed by combining LH treatment with uncoupling agents such as 1-octanol or halothane. Results show that maturation induction with LH requires a cell–cell coupling, as the uncoupling of the gap junctions decreases GVBD percentages. Experiments with LH in the presence of heparin, BAPTA/AM and theophylline suggest that the hormone could induce GVBD by means of the passage of IP3 or Ca2+ through the gap junctions, which would increase the Ca2+ level in the oocyte cytoplasm and activate phosphodiesterase (PDE), thus contributing to the decrease in cAMP levels and allowing meiosis resumption.

Keywords

Amphibian oocytesGap junctionsLH-induced maturationSpontaneous maturation
Type
Research Article
Information
Zygote , Volume 15 , Issue 1 , February 2007 , pp. 65 - 80
Copyright
Copyright © Cambridge University Press 2007

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References

Albertini, D. & Anderson, E. (1974). The appearance and structure of the intercellular connections during the ontogeny of the rabbit ovarian follicle with special reference to gap junctions. J. Cell Biol. 2, 234–50.CrossRefGoogle Scholar
Anderson, E. & Albertini, D. (1976). Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 7, 680–6.CrossRefGoogle Scholar
Alonso, T.S. (2000). Lipid involvement in amphibian maturation. Lipids 31, 651–6.Google Scholar
Allbriton, N.L., Meyer, T. & Stryer, L. (1992). Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812–5.CrossRefGoogle Scholar
Atef, A., Francois, P., Christian, V. & Marc-Andre, S. (2005). The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation. Mol. Reprod. Dev. 71, 358–67.CrossRefGoogle ScholarPubMed
Bandyopadhyay, A., Bandyopadhyay, J., Choi, H.H., Choi, H.S. & Kwon, H.B. (1998). Plasma membrane mediated action of progesterone in amphibian (Rana dybowskii) oocytes maturation. Gen. Comp. Endocrinol. 109, 293–301.CrossRefGoogle Scholar
Barber, M.L. & Foy, J.E. (1973). An enzymatic comparison of sea urchin eggs ghosts prepared before and after fertilization. J. Exp. Zool. 184, 157–66.CrossRefGoogle Scholar
Bolamba, D., Patiño, R., Yoshizaki, G. & Thomas, P. (2003). Changes in homologous and heterologous gap junction contacts during maturation-inducing hormone-dependent meiotic resumption in ovarian follicles Atlantic croaker. Gen. Comp. Endocrinol. 131, 291–5.CrossRefGoogle ScholarPubMed
Browne, C.L., Wiley, H.S. & Dumont, J.M. (1979). Oocyte–follicle cell gap junctions in Xenopus laevis and the effect of gonadotropins on their permeability. Science 203, 182–3.CrossRefGoogle ScholarPubMed
Browne, C.L. & Werner, W. (1984). Intercellular junctions between the follicle cells and oocytes of Xenopus laevis. J. Exp. Zool. 230, 105–13.CrossRefGoogle ScholarPubMed
Buccione, R., Schroeder, A.C. & Eppig, J.J. (1990). Interaction between somatic cells and germ cells throughout mammalians oogenesis. Biol. Reprod. 43, 543–7.CrossRefGoogle ScholarPubMed
Caldironi, H A. & Alonso, T. (1996). Lipidic characterization of full grown amphibian oocytes and their membrane-enriched fractions. Lipids 31, 651–6.CrossRefGoogle ScholarPubMed
Cerdá, J.L., Petrino, T. & Wallace, R. (1993). Functional heterologous gap junctions in Fundulus ovarian follicle maintain meiotic arrest and permit hydration during oocyte maturation. Dev. Biol. 160, 228–35.CrossRefGoogle ScholarPubMed
Chien, E., Morrill, G.A. & Kostellow, A.B. (1991). Progesterone-induced second messengers at the onset of meiotic maturation in the amphibian oocytes, interrelationships between phospholipid N-methylation, calcium and diacylglycerol release, and inositol phospholipid turnover. Mol. Cell. Endocrinol. 81, 53–67.CrossRefGoogle ScholarPubMed
Coskun, S. & Lin, Y.C. (1994). Effect of transforming growth factors and activin-A on in vitro porcine oocyte maturation. Mol. Reprod. Dev. 38, 153–9.CrossRefGoogle ScholarPubMed
Davis, JS, Farese, R. & Clark, MR. (1983). Stimulation of phospholipid synthesis by luteinizing hormone in isolated rat granulosa cells. Endocrinology 112, 2212–4.CrossRefGoogle ScholarPubMed
Davis, J.S., Weakland, L.L., West, L.A. & Farese, R.V. (1986). Luteinizing hormone stimulates the formation of inositol triphosphate and cyclic AMP ion rat granulose cells: Evidence for phospholipase C generated second messengers in the action of luteinizing hormone. Biochem. J. 238, 597–604.CrossRefGoogle Scholar
Davis, J.S. (1994). Mechanisms of hormone action: luteinizing hormone receptors and second-messenger pathways. Curr. Opin. Obstet. Gynecol. 6, 254–61.CrossRefGoogle ScholarPubMed
Dekel, N., Kraicer, P., Phillips, D., Sánchez, R. & Segal, S. (1978). Cellular associations in the rat oocytes–cumulus cell complex: morphology and ovulatory changes. Gamete Res. 1, 47–57.CrossRefGoogle Scholar
Dekel, N. & Beers, W. (1978) Rat oocytes maturation in vitro relief of cyclic AMP inhibition by gonadotropins. Proc. Natl. Acad. Sci. USA 75, 4369–73.CrossRefGoogle ScholarPubMed
Dekel, N. & Beers, W. (1980). Development of rat oocytes in vitro: inhibition and induction of maturation in the presence of cumulus–oophorus. Dev. Biol. 75, 247–54.CrossRefGoogle ScholarPubMed
Dekel, N., Galiani, D. & Sherizly, I. (1988). Dissociation between the inhibitory and the stimulatory action of cAMP on maturation of rat oocytes. Mol. Cell. Endocrinol. 56, 115–21.CrossRefGoogle ScholarPubMed
Dettlaff, T.A. (1988). Development of the mature egg organization in amphibians, fish, and starfish during the concluding stages of oogenesis, in the period of maturation. In Oocyte Growth and Maturation, (eds T.A. Dettlaff & S.G. Vassetzky), pp. 165–277. New York: Consultants Bureau.CrossRefGoogle Scholar
Dimino, M.J., Snitzer, J. & Brown, K.M. (1987). Inositol phosphate accumulation in ovarian granulose after stimu lation by luteinizing hormone. Biol. Reprod. 37, 1129–34.CrossRefGoogle Scholar
Down, S., Hudson, E. & Hardie, D. (2002). A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev. Biol. 245, 200–12.CrossRefGoogle Scholar
Downs, S.M. (2001). A gap-junction-mediated signal, rather than an external paracrine factor, predominates during meiotic induction in isolated mouse oocytes. Zygote 9, 71–82.CrossRefGoogle ScholarPubMed
Downs, S.M. & Eppig, JJ. (1987). Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol. Reprod. 36, 431–7.CrossRefGoogle ScholarPubMed
Downs, S.M. & 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
Epel, D. (1982). Membranes in growth and development. A. Liss, New York, p. 171.Google Scholar
Eppig, J.J. (1982). The relationship between cumulus cell–oocyte coupling, oocyte maturation, and cumulus expansion. Dev. Biol. 89, 268–72.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1991). Maintenance of meiotic arrest and induction of oocyte maturation in mouse oocyte–granulosa cell complex developed in vitro from preantral follicles. Biol. Reprod. 45, 824–30.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1993). Regulation of mammalian oocytes maturation. In The Ovary, (eds E.Y. Adashi & P.C.K. Leung), pp. 185–208. New York: Raven Press.Google Scholar
Eppig, J.J. & Downs, S.M. (1987). The effect of hypoxanthine on mouse oocytes growth and development in vitro: maintenance of meiotic arrest and gonadotropins-induced oocytes maturation. Dev. Biol. 119, 313–21.CrossRefGoogle Scholar
Eppig, J.J. & Downs, S.M. (1988). Gonadotropin-induced murine oocytes maturation in vivo in not associated with decreased cyclic adenosine monophosphate in the oocytes–cumulus cell complex. Gamete Res. 20, 125–31.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Ward Bailley, P.F. (1982). The mechanism of cumulus cell–oocyte uncoupling: evidence for the participation of both cumulus cells and oocytes. Gamete Res. 6, 145–54.CrossRefGoogle Scholar
Fagbohun, C.F. & Downs, S.M. (1990). Maturation of the mouse oocytes–cumulus cell complex: stimulation by lectins. Biol. Reprod. 42, 413–23.CrossRefGoogle Scholar
Fagbohun, C.D. & Downs, S.M. (1991). Metabolic and ligand-stimulated meiotic maturation in the mouse oocytes–cumulus cell complex. Biol. Reprod. 45, 851–9.CrossRefGoogle Scholar
Flores, J.A., Aguirre, C., Sharma, O.P. & Verdhuis, J.D. (1998). Luteinizing hormone (LH) stimulates both intracellular calcium ion mobilization and transmembrane cation influx in single ovarian (granulosa) cells: recruitment as a cellular mechanism of LH-(Ca2+), dose response. Endocrinology 139, 3606–12.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M.B. & Sloane-Stanley, G. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 487–509.CrossRefGoogle ScholarPubMed
Gilula, N.B., Epstein, M. & Brees, W. (1978). Cell-to-cell communication and ovulation: a study of the cell–oocyte complex. J. Cell Biol. 78, 58–75CrossRefGoogle Scholar
Godeau, F., Ishizaka, T. & Koide, S.S. (1985). Early stimulation of phospholipid methylation in Xenopus oocytes by progesterone. Cell Differ. 16, 35–41.CrossRefGoogle ScholarPubMed
Goren, S., Oron, Y. & Dekel, N. (1990). Rat oocyte maturation: role of calcium in hormone actino. Mol. Cell. Endocrinol. 72, 131–8.CrossRefGoogle Scholar
Greeley, M.S., Begovac, P.C. & Wallace, R.A. (1987). Removal of enveloping follicle cells can trigger resumption of meiotic maturation in Fundulus heteroclitus oocytes. J. Exp. Zool. 244, 177–80.CrossRefGoogle Scholar
Grondahl, C., Breinholt, J., Wahl, P., Murray, A., Hansen, T.H., Faerge, I. (2003). Physiology of meiosis-activating sterol: endogenous formation and mode of action. Hum. Reprod. 18, 122–9.CrossRefGoogle ScholarPubMed
Guderman, T., Birnbaumer, M. & Birnbaumer, L. (1992). Evidence for dual coupling of the murine luteinizing hormone receptor to adenylyl cyclase and phosphoinositide breakdown and Ca++ mobilization. Studies with the cloned murine luteinizing hormone receptor expressed in L cells. J. Biol. Chem. 267, 4479–88.CrossRefGoogle Scholar
Homa, S.T., Webster, S.D. & Russell, R.K. (1991). Phospholipid turnover and ultrastructural correlates during spontaneous germinal vesicle breakdown of the bovine oocytes: effects of a cyclic AMP phosphodiesterase inhibitor. Dev. Biol. 146, 461–72.CrossRefGoogle ScholarPubMed
Homa, S.T., Carroll, J. & Swann, K. (1993). The role of calcium in mammalian oocytes maturation and egg activation. Human Reprod. 8, 1274–81.CrossRefGoogle ScholarPubMed
Iwamatsu, T. & Ohta, T. (1981). On a relationship between oocyte and follicle cells around the time of ovulation in the medaka. Oryzias latipes. Annot. Zool. Japon 54, 17–29.Google Scholar
Jalabert, B., Breton, B., Brzuska, E., Fostier, A. & Wieniawski, J. (1977). A new tool for induced spawning: the use of 17α,20β-dihydroprogesterone to spawn carp at low temperature. Aquaculture 10, 353–64.CrossRefGoogle Scholar
Johnson, M.F., Simon, S.A. & Ramon, F. (1980). Interaction of anesthetics with electrical synapses. Nature 286, 498–500.CrossRefGoogle Scholar
Kahn, I.A. & Thomas, P. (1999). Ovarian cycle, teleost fish. In Encyclopaedia of Reproduction, (eds E. Knobil & J.D. Neill), pp. 552–64. San Diego: Academic Press.Google Scholar
Kim, J.W., Im, W., Choi, H. & Kwon, H.B. (1998). Seasonal fluctuations in pituitary gland and plasma levels of gonadotropic hormones in Rana. Gen. Comp. Endocrinol. 109, 13–23.CrossRefGoogle ScholarPubMed
Kobrinsky, E., Spielman, A.I., Rosenzweig, S., Marks, A.R. (1999). Ceramide triggers intracellular calcium release via the IP3 receptor in Xenopus laevis oocytes. Am. J. Physiol. 277 (4 Pt 1), C665–72.CrossRefGoogle ScholarPubMed
Kostellow, A.B., Ma, G.Y. & Morrill, G.A. (1993). Steroid action at the plasma membrane: progesterone stimulation of phosphatidylcholine-specific phospholipase C following release of the prophase block in amphibian oocytes. Mol. Cell. Endocrinol. 92, 33–44.CrossRefGoogle ScholarPubMed
Kronke, M. (1999). Involvement of sphingomyelinases in TNF signaling pathways. Chem. Phys. Lipids 102, 157–66.CrossRefGoogle ScholarPubMed
Larsen, W.J., Wert, S.E & Brunner, G.D. (1986). A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes. Dev. Biol. 113, 517–21.CrossRefGoogle ScholarPubMed
Lawrence, T.S., Dekel, N. & Beers, W.H. (1980). Binding of human chorionic gonadotrophin by rat cumuli oophori and granulose cells: a comparative study. Endocrinology 106, 1114–8.CrossRefGoogle Scholar
Lin, Y.P & Schuetz, A.W. (1985). Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: temporal relationship and locus of action. Gen. Comp. Endocrinol. 58, 421–35.Google ScholarPubMed
Mattioli, M. (1994). Transduction mechanisms for gonadotrophin-induced oocytes maturation in mammals. Zygote 2, 347–9.CrossRefGoogle ScholarPubMed
Mattioli, M. (1996). Molecular aspects of gonadotrophin-induced oocytes maturation. Arch. Animal Breeding 39, 31–41.Google Scholar
Mattioli, M., Galeati, G., Barboni, B. & Seren, E. (1994). Concentration of cyclic AMP during the maturation pig oocytes in vivo and in vitro. J. Reprod. Fertil. 100, 403–409.CrossRefGoogle ScholarPubMed
Mattioli, M., Lucidi, P. & Barboni, B. (1998). Expanded cumuli induce acrosome reaction in boar sperm. Mol. Reprod. Dev. 51, 445–53.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Mattioli, M. & Barboni, B. (2000). Signal transduction mechanism for LH in the cumulus–oocyte complex. Mol. Cell. Endocrinol. 161, 19–23.CrossRefGoogle ScholarPubMed
Masui, Y. & Clarke, H.J. (1979). Oocyte maturation. Int. Rev. Citol. 57, 185–282.CrossRefGoogle ScholarPubMed
Masui, Y. (1967). Relative roles of the pituitary, follicle cells, and progesterone in the induction of oocytes maturation in Rana pipiens. J. Exp. Zool. 166, 365.CrossRefGoogle ScholarPubMed
Meda, P. (1989). Gap junctional coupling and secretion in endocrine and exocrine pancreas. In Cell Interactions and Gap Junctions, vol. 1, (eds N. Speralakis & W.C. Cole), pp. 59–83. Boca Raton, Florida: CRC Press.Google Scholar
Meinecke, B. & Meinecke Tillmann, S. (1993). Effect of alfa-amanitin on nuclear maturation of porcine oocytes in vitro. J. Reprod. Fert. 98, 195–201.CrossRefGoogle Scholar
Moor, R., Smith, D. & Dawson, R. (1980). Measurement of intercellular coupling between oocytes and cumulus cell using intracellular markers. Exp. Cell Res. 126, 15–29.CrossRefGoogle ScholarPubMed
Morril, G.A. & Kostellow, A.B. (1999). Progesterone induces meiotic division in the amphibian oocytes by releasing lipid second messengers from the plasma membrane. Steroid 64, 157–67.CrossRefGoogle Scholar
Motlik, J., FulkaJ., Jr J., Jr, Prochazka, R., Rimkevicova, Z., Kubelka, M. & Fulka, J. (1989). RNA and protein synthesis requirements for the resumption of meiosis in rabbit oocytes: the role of cumulus cells. Reprod. Nutr. Dev. 29, 601–9.CrossRefGoogle ScholarPubMed
Nagahama, Y. (1987). Endocrine control of oocyte maturation. In Hormones and Reproduction in Fishes, Amphibians and Reptiles, (eds D.O. Norris & R.E. Jones), pp. 171–202. New York: Plenum.CrossRefGoogle Scholar
ODonnell, J., Hill, J. & Gross, DJ. (2004). Epidermal growth factor activates cytosolic Ca++ elevations and subsequent membrane permeabilization in mouse cumulus–oocyte complexes. Reproduction 127, 207–20.CrossRefGoogle ScholarPubMed
Park, J., Su, Y-Q., Ariga, M., Law, E., Jin, A-C. & Conti, M. (2004). EGF-like growth factors as mediators of LH actino in the ovulatory follicle. Science 303, 682–4.CrossRefGoogle Scholar
Patiño, R. & Kagawa, H. (1999). Regulation of gap junctions and oocyte maturational competence by gonadotropins and insulin-like growth factor-I in ovarian follicles of red sea bream. Gen. Comp. Endocrinol. 115, 454–62.CrossRefGoogle Scholar
Patiño, R., Chang, X., Yoshizaki, G., Thomas, P. & Kagawa, H.,(2000). Role and regulation of gap junctions during oocyte maturation in teleosts. In Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish, (eds Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E. & Stefansson, S.O.), pp. 292–4. Institute of Marine Research and University of Bergen, Bergen: University of Bergen Press.Google Scholar
Patiño, R., Yoshizaki, G., Thomas, P. & Kagawa, H. (2001). Gonadotropin control of ovarian follicle maturation: the two-stage concept and its mechanisms. Comp. Biochem. Physiol. B. 129, 427–39.CrossRefGoogle ScholarPubMed
Patiño, R., Yoshizaki, G. & Thomas, P. (2003). Ovarian follicle maturation and ovulation: an integrated perspective. Fish Physiol. Biochem. 28, 305–8.CrossRefGoogle Scholar
Peng, X.R, Hsueh, A.J., Lapolt, P.S., Bjersing, L. & Ny, T. (1991). Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129, 3200–7.CrossRefGoogle ScholarPubMed
Peracchia, C. (1991). Effects of the anesthetics heptanol, halothane and isoflurane on gap junction conductance in crayfish septate axons: a calcium- and hydrogen-independent phenomenon potentiated by caffeine and theophylline, and inhibited by 4-aminopyridine. J. Memb. Biol. 121, 67–78.CrossRefGoogle ScholarPubMed
Petrino, T., Bühler, M.I., Budeguer de Atenor, M.S. & Legname, A. (1983). Seasonal variations and metabolic behaviour during Bufo arenarum oogenesis. Acta Embryol. Morphol. Exper. 4, 17–26.Google ScholarPubMed
Racowsky, C. (1984). Effect of forskolin on the spontaneous maturation and cyclic AMP content of rat oocytes–cumulus complex. J. Reprod. Fertil. 72, 107–16.CrossRefGoogle Scholar
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and in vitro. Dev. Biol. 108, 191–202.CrossRefGoogle ScholarPubMed
Ramón, F., Zampighi, G.A. & Rivera, A. (1985). Control of junctional permeability. In Gap Junctions (eds Bennett, M.V.L. & Spray, D.). Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar
Redshaw, M.R (1972). The hormonal control of the amphibian ovary. Am. Zool. 12, 289–306.CrossRefGoogle Scholar
Reynhout, J.K., Taddei, C., Smith, L.D. & LaMarca, M.J. (1975). Response of large oocytes of Xenopus laevis to progesterone in vitro in relation to oocytes size and time after previous hCG-induced ovulation. Dev. Biol. 44, 375–9.CrossRefGoogle ScholarPubMed
Richards, C.D., Martin, K., Gregory, S., Keightley, C.A., Hesketh, T.R., Smith, G.A., Warren, G.B. & Metcalfe, J.C. (1978). Degenerate perturbations of protein structure as the mechanisms of anaesthetic action. Nature (Lond.) 276, 775–9.CrossRefGoogle ScholarPubMed
Rozental, R., Srinivas, M. & Spray, D.C. (2001). How to close a gap junction channel. Efficacies and potencies of uncoupling agents. Methods Mol. Biol. 154, 447–76.Google Scholar
Rouser, G., Fleischer, S. & Yamamoto, A. (1970). A two-dimensional thin-layer chromatographic separation of polar lipids and determination of phospholipids by phosphorous analysis of spots. Lipids 5, 494–6.CrossRefGoogle ScholarPubMed
Salustri, A. & Siracusa, G. (1983). Metabolic coupling, cumulus expansion and meiotic resumptions in mouse cumuli oophori cultured in vitro in the presence of FSH or db-AMP, or stimulated in vivo by hCG. J. Reprod. Fertil. 68, 335–41.CrossRefGoogle ScholarPubMed
Sánchez-Yague, J., Hipkin, R.W. & Ascoli, M. (1993). Biochemical properties of the agonist-induced desensitization of the follicle-stimulating hormone and luteinizing hormone/chorionic gonadotropins-responsive adenylyl cyclase in cells expressing the recombinant gonadotropin receptors. Endocrinology 132, 1007–16.CrossRefGoogle ScholarPubMed
Sandberg, K., Bor, M., Hong, J., Markwick, A., Millan, M.A. & Catt, K.J. (1990). Angiotensin II induced calcium mobilization in oocytes by signal transfer through gap junctions. Science 249, 298–301.CrossRefGoogle ScholarPubMed
Schuetz, A.W. (1974). Role of hormones in oocytes maturation. Biol. Reprod. 10, 150–178.CrossRefGoogle Scholar
Sela–Abramovich, S., Chorev, E., Galiani, D. & Dekel, N. (2005). Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocytes maturation in rat ovarian follicles. Endocrinology 146, 1236–44.CrossRefGoogle ScholarPubMed
Skoblina, M.N. (2004). Involvement of gap junctions in stimulation of in vitro maturation of common frog oocytes by low progesterone concentrations. Ontogenez 35, 350–5.Google ScholarPubMed
Smith, L.D. (1989). The induction of oocyte maturation: transmembrane signaling events and regulation of the cell cycle. Development 107, 685–99.CrossRefGoogle ScholarPubMed
Spiegel, S., Foster, D. & Kolesnik, R. (1996). Signal trans duction through lipid second messengers. Curr. Opin. Cell Biol. 8, 159–67.CrossRefGoogle Scholar
Stagg, R. & Fletcher, W.H. (1990). The hormone-induced regulation of contact-dependent cell–cell communication by phosphorylation. Endocrinol. Rev. 11, 302–25.CrossRefGoogle ScholarPubMed
Thomas, R., Armstrong, D. & Gilchrist, R. (2004). Bovine cumulus cell–oocyte gap junctions communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels. Biol. Reprod. 70, 548–56.CrossRefGoogle Scholar
Tsafriri, A., Dekel, N., Bar-Ami, S. (1982). The role of oocyte maturation inhibitor in follicular regulation of oocyte maturation. J. Reprod. Fertil. 64, 541–51.CrossRefGoogle ScholarPubMed
Tsafriri, A., Cao, X., Ashkenazi, H., Motola, S., Popliker, M. & Pomerantz, S.H. (2005). Resumption of oocyte meiosis in mammals: on models, meiosis activating sterols, steroids and EGF-like factors. Mol. Cell. Endocrinol. 29, 37–45.CrossRefGoogle Scholar
Van Den Hoef, M., Dictus, W.J., Hage, W.J. & Bluemink, J.G. (1984). The ultrastructural organization of gap junctions between follicle cells and the oocyte in Xenopus laevis. Eur. J. Cell Biol. 33, 242–7.Google ScholarPubMed
Vilain, J.P., Moreau, M., Guerrier, P. (1980). Uncoupling of oocytes follicle cells triggers reinitiation of meiosis in amphibian oocytes. Dev. Growth Differ. 22, 687–91.CrossRefGoogle ScholarPubMed
Villeco, E., Aybar, M., Genta, S., Sánchez, S. & Sánchez-Riera, A. (2000). Effect of gap junctions uncoupling in full-grown Bufo arenarum ovarian follicles: participation of cAMP in meiotic arrest. Zygote 8, 171–9.CrossRefGoogle Scholar
Warner, A. (1988). The gap junction. J. Cell Sci. 89, 1–7.CrossRefGoogle ScholarPubMed
Webb, R.J., Marshall, F., Swann, K. & Carroll, J. (2002). Follicle-stimulating hormone induced a gap junctions-dependent dynamic change in cAMP and protein kinase A in mammalian oocytes. Dev. Biol. 15, 441–54.CrossRefGoogle Scholar
Weber, G.M. & Sullivan, C.V. (2005). Insulin-like growth factor-I induces oocytes maturational competence but not meiotic resumption in white bass (Morone chrysops) follicles in vitro: evidence for rapid evolution of insulin-like growth factor action. Biol. Reprod. 72, 1177–86.CrossRefGoogle Scholar
York, W.S. (1993). Follicle cell–oocyte gap junctional coupling and oocytes maturation in sciaenic fishes. M.Sc. thesis, Texas Technological University, Lubbock, Texas.Google Scholar
Zelarayán, L., Oterino, J. & Bühler, M.I. (1995). Spontaneous maturation in Bufo arenarum oocytes: follicle wall involvement, respiratory activity and seasonal influences. J. Exp. Zool. 272, 356–62.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J. & Bühler, M.I. (1996) Spontaneous maturation in Bufo arenarum oocytes: participation of protein kinase C. Zygote 4, 257–62.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J., Sánchez Toranzo, G. & Bühler, M.I. (2000). Involvement of purines and phosphoinositides in spontaneous and progesterone-induced nuclear maturation of Bufo arenarum oocytes. J. Exp. Zool. 287, 151–7.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Zelenik, A.J., Schuler, H.M. & Reichert, L.E. (1981). Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropins to the preovulatory follicle. Endocrinology 109, 356–62.Google Scholar