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Involvement of GABAA receptor in Bufo arenarum oocyte maturation

Published online by Cambridge University Press:  01 May 2008

G. Sánchez Toranzo
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.
J. Oterino
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. 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 4248025. e-mail: mbuhler@fbqf:unt.edu.ar

Summary

Amphibian oocytes meiotic arrest is released under the stimulus of progesterone; this hormone interacts with the oocyte surface and starts a cascade of events leading to the activation of a cytoplasmic maturation promoting factor (MPF) that induces germinal vesicle breakdown (GVBD), chromosome condensation and extrusion of the first polar body.

The aim of this work was to determine whether the activation of a GABAA receptor is able to induce GVBD in fully grown denuded oocytes of Bufo arenarum and to analyse its possible participation in progesterone-induced maturation. We also evaluated the role of purines and phospholipids in the maturation process induced by a GABAA receptor agonist such as muscimol.

Our results indicated that the activation of the GABAA receptor by muscimol induces maturation in a dose- and time-dependent manner and that this activation is a genuine maturation that enables oocytes to form pronuclei. Assays with a receptor antagonist, picrotoxine, showed that the maturation induced by muscimol was inhibited. Treatment with picrotoxine, however, shows that the participation of GABAA receptor in progesterone-induced maturation is not significant.

In addition, our results indicate that high intracellular levels of purines obtained by the use of db-AMPc and theophylline or the inhibition of the phosphatidylinositol 4,5-bisphosphate (PIP2 hydrolysis by neomycin and PIP2 turn over by LiCl, respectively, inhibited the maturation induced by muscimol. Treatment with H-7 indicated, however, that PKC activation is not necessary for GVBD induced by the GABAA receptor agonist. Results suggest that the transduction pathway used by the GABAA receptor to induce maturation is different from those used by progesterone.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

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References

Berridge, M.J. & Irvine, R.F. (1989). Inositol phosphates and cell signaling. Nature 341, 197205.CrossRefGoogle Scholar
Bühler, M.I., Petrino, T. & Legname, A. (1987). Sperm nuclear transformation and aster formation related to metabolic behavior in amphibian eggs. Dev. Growth Diff. 29, 177–84.CrossRefGoogle ScholarPubMed
Covey, D.F., Evers, A.S., Mennerick, S., Zorumski, C.F. & Purdy, R.H. (2001). Recent developments in structure–activity relationships for steroid modulators of GABAA receptors. Brain Res. Rev. 37, 91–7.CrossRefGoogle Scholar
Downes, C.P. (1989). G protein-dependent regulation of phospholipase C. Trends Pharmacol. Sci. Suppl, 3942.Google ScholarPubMed
Elinson, R.P. (1973). Fertilization of frog body cavity eggs enhanced by treatments affecting the vitelline coat. J. Exp. Zool. 183, 291302.CrossRefGoogle Scholar
Eppig, J.J. (1991). Maintainance 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
Ferrell, J.E. (1999). Xenopus oocytes maturation: new lessons from a good egg. BioEssays 21, 833–42, 866–70.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Fissore, R.A, Reis, M.M. & Palermo, G.D. (1999). Isolation of the Ca2+ releasing component(s) of mammalian sperm extracts: the search continues. Mol. Hum. Reprod. 5, 189–92.CrossRefGoogle ScholarPubMed
Fortune, J.E., Concannon, P.W. & Hansel, W. (1975). Ovarian progesterone levels during in vitro oocyte maturation and ovulation in Xenopus laevis. Biol. Reprod. 13, 561–7.CrossRefGoogle ScholarPubMed
Hanson, B.A. (1991). The effects of lithium on the phosphoinositides and inositol phosphates of Neurospora crassa. Exp. Mycol. 15, 7690.CrossRefGoogle Scholar
Kwon, H.B. & Schuetz, A.W. (1986). Role of cAMP in modulating intrafollicular progesterone levels and oocytes maturation in amphibians. Dev. Biol. 117, 354–64.CrossRefGoogle ScholarPubMed
Kwon, H.B., Lin, Y.P., Choi, M.J. & Ahn, R.S. (1989). Spontaneous maturation of follicular oocytes in Rana dybowski in vitro: seasonal influences, progesterone production and involvement of cAMP. J. Exp. Zool. 252, 190–9.CrossRefGoogle Scholar
Laszlo, A., Villanyi, P., Zsolnai, B. & Erdo, S.L. (1989). Gamma-aminobutyric acid, its related enzymes and receptor-binding sites in the human ovary and fallopian tube. Gynecol. Obstet. Invest. 28, 94–7.CrossRefGoogle ScholarPubMed
Lin, Y.P. & Schuetz, A.W. (1985). Spontaneous oocyte maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 1128.CrossRefGoogle Scholar
Meizel, S. (1997). Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol. Reprod. 56, 569–74.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
Nishizuka, Y. (1984). The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308, 693–8.CrossRefGoogle ScholarPubMed
Pesty, A., Lefevre, B., Kubiak, J., Geraud, G., Tesarik, J. & Maro, B. (1994). Mouse oocyte maturation is affected by lithium via the polyphosphoinositide metabolism and the microtubule network. Mol. Reprod. Dev. 38, 187–99.CrossRefGoogle ScholarPubMed
Picard, A. & Doreé, M. (1983). Lithium inhibits amplification or action of the maturation-promoting factor (MPF) in meiosis maturation of starfish oocytes. Exp. Cell Res. 147, 4150.CrossRefGoogle ScholarPubMed
Rorsman, P., Berggren, P.O., Bokvist, K., Ericson, H., Mohler, H., Ostenson, C.G. & Smith, P.A. (1989). Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels. Nature 341, 233–6.CrossRefGoogle ScholarPubMed
Sadler, S.E. & Maller, J.L. (1980). Progesterone prevents activation of adenylate cyclase by cholera toxin in Xenopus oocytes. J. Cell Biol. 87, 169.Google Scholar
Sadler, S.E. & Maller, J.L. (1981). Progesterone inhibits adenylate cyclase in Xenopus oocytes: Action on the guanine nucleotide regulatory protein. J. Biol. Chem. 256, 6368–73.CrossRefGoogle ScholarPubMed
Sadler, S.E. & Maller, J.L. (1982). Identification of a steroid receptor on the surface of Xenopus oocytes by photoaffinity labeling. J. Biol. Chem. 247, 355–61.CrossRefGoogle Scholar
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L., Oterino, J., Bühler, M.I. (2004). Effect of insulin on spontaneous and progesterone-induced GVBD on Bufo arenarum denuded oocytes. Zygote 12, 111.Google ScholarPubMed
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L., Oterino, J. & Bühler, M.I. (2006). Activation of the maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents. Zygote 14, 306–16.Google Scholar
Schmitt, A. & Nebreda, A.R. (2002). Signaling pathways in oocyte meiotic maturation. J. Cell Sci. 115, 2457–9.CrossRefGoogle ScholarPubMed
Schuetz, A.W. (1985). Local control mechanisms during oogenesis and folliculogenesis. In Oogenesis In Developmental Biology: A Comprehensive Synthesis, vol. I (ed. Browder, L.W.), pp. 383. New York: Plenum Press.CrossRefGoogle Scholar
Sih, Q.X. & Roldán, E.R. (1995). Evidence that a GABAA-like receptor is involved in progesterone-induced acrosomal exocytosis in mouse spermatozoa. Biol. Reprod. 52, 373–81.Google Scholar
Smith, L.D. (1989). The induction of oocyte maturation: transmembrane signaling events and regulation of the cell cycle. Development 107, 685–99.CrossRefGoogle ScholarPubMed
Taraskevich, P.S. & Douglas, W.W. (1985). Pharmacological and ionic features of gamma-aminobutyric acid receptors influencing electrical properties of melanotrophs isolated from the rat pars intermedia. Neuroscience 14, 301–8.CrossRefGoogle ScholarPubMed
Voronina, E. & Wessel, G.M. (2004). Regulatory contribution of heterotrimeric G-proteins to oocyte maturation in the sea urchin. Mech. Dev. 121, 247–59.CrossRefGoogle ScholarPubMed
Webb, R.J., Bains, H., Cruttwell, C. & Carroll, J. (2002). Gap-junctional communication in mouse cumulus–oocyte complex: implications for the mechanism of meiotic maturation. Reproduction 123, 4152.CrossRefGoogle ScholarPubMed
Wistrom, C.A. & Meizel, S. (1993). Evidence suggesting involvement of a unique human sperm steroid receptor/Cl channel complex in the progesterone-initiated acrosome reaction. Dev. Biol. 159, 679–90.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