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Spontaneous maturation in Bufo arenarum oocytes: participation of protein kinase C

Published online by Cambridge University Press:  26 September 2008

L. Zelarayán ,
J. Oterino  and
M.I. Bühler
L. Zelarayán
Affiliation:
Instituto Superior de Investigaciones Biolégicas (INSIBIO), Departamento de Biología del Desarrollo, Universidad Nacional Tucumán, Argentina.
J. Oterino
Affiliation:
Instituto Superior de Investigaciones Biolégicas (INSIBIO), Departamento de Biología del Desarrollo, Universidad Nacional Tucumán, Argentina.
M.I. Bühler*
Affiliation:
Instituto Superior de Investigaciones Biolégicas (INSIBIO), Departamento de Biología del Desarrollo, Universidad Nacional Tucumán, Argentina.
*
Marta Inés Bühler, Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina. Fax: 54-81-248025. e-mail: [email protected].
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Summary

Although progesterone is the maturation inducer in amphibians, it has been demonstrated that in Bufo arenarum oocytes resumed meiosis with no need of exogenous hormonal stimulus if derived of their enveloping, follicle cells. This phenomenon, called spontaneous maturation, is quite rare in amphibians. In B. arenarum, spontaneous maturation took place only in oocytes obtained during the reproductive period (spring-summer). During this period the oocytes also demonstrated a respiratory activity characteristic of mature oocytes. Interestingly, full-grown B. arenarum oocytes always responded to progesterone regardless of the season in which they were obtained and of their respiratory activity. The disposition of oocytes competent or not competent to mature spontaneously provides a useful system for the study of molecular mechanisms involved in the maturation process. The data presented here indicate that the activation of protein kinase C (PKC) induces germinal vesicle breakdown (GVBD) in denuded oocytes unable to mature spontaneously (winter oocytes) and is involved in the in vitro spontaneous maturation of B. arenarum full-grown oocytes. The inhibition of PKC by 1-(5-isoquinolynyl-sulphonyl-2-methyl-piperazine (H-7) impeded spontaneous maturation in a dose-dependent manner, thus supporting the participation of the PKC pathway during this process. Interestingly phorbol 12-myristate-13-acetate (PMA)-induced GVBD is inhibited by the incubation of the oocytes in dibutyryl cAMP (dbcAMP), indicating that both pathways, PKC and protein kinase A (PKA), are related at a certain point. However, spontaneous GVBD is less sensitive than PMA-induced GVBD to dbcAMP. This fact would support the suggestion that in spontaneous GVBD mechanisms different from activation of PKC are at work.

Keywords

AmphibianOocyteProtein kinase CSpontaneous maturation
Type
Article
Information
Zygote , Volume 4 , Issue 4 , November 1996 , pp. 257 - 262
Copyright
Copyright © Cambridge University Press 1996

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References

Refernces

Baulieu, E.E. (1983). Steroid-membrane-adenylate cyclase interaction during Xenopus laevis oocyte meiosis reinitiation: a new mechanism of steroid hormone action. Exp. Clin. Endocrinol. 81, 3–16.CrossRefGoogle ScholarPubMed
Bühler, M.I., Petrino, T. & Legname, A.H. (1987). Sperm nuclear transformation and aster formation related to metabolic behaviour in amphibian eggs. Dev. Growth Differ. 29, 177–84.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1991). Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte–granulosa cell complexes developed in vitro from preantral follicles. Blot. Keprod. 45, 824–30.Google ScholarPubMed
Eppig, J.J. & Downs, S.M. (1984). Chemical signals that regulate oocyte maturation. Blot. Reprod. 30, 1–11.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Ward-Bailey, 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
Kleis-San Francisco, S. & Schuetz, A.W. (1988). Role of protein kinase C activation in oocyte maturation and steroidogenesis in ovarian follicles of Rana pipiens: studies with phorbol 12-myristate-13-acetate. Gamete Res. 21, 323–34.CrossRefGoogle ScholarPubMed
Kwon, H.B. & Lee, W.K. (1991). Involvement of protein kinase C in the regulation of oocyte maturation in amphibians (Rana dybowskii). J. Exp. Zool. 257, 115–23.CrossRefGoogle ScholarPubMed
Kwon, H.B., Lin, Y.P., Choi, M.J. & Ahn, R.S. (1989). Spontaneous maturation of follicular oocytes in Rana dybowskii in vitro: seasonal influences, progesterone production and involvement of cAMP. J. Exp. Zool. 252, 190–9.CrossRefGoogle ScholarPubMed
Legname, A.H. & Böhler, M.I. (1978). Metabolic behaviour and cleavage capacity in the amphibian egg. J. Embryol. Exp. Morphol. 47, 161–8.Google ScholarPubMed
Legname, A.H. & Salomon de Legname, H. (1980). Changes in the oxidative metabolism during maturation of amphibian oocytes. J. Embryol. Exp. Morphol. 59, 175–86.Google ScholarPubMed
Lin, Y.P. & Schuetz, A.W. (1985). Spontaneous oocyte maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 11–28.CrossRefGoogle Scholar
Maller, J.L. (1983). Interaction of steroids with cyclic nucleotide system in amphibian oocytes. Adv. Cyclic Nucleotide Res. 15, 295–336.Google Scholar
Maller, J.L. & Krebs, E.G. (1980). Regulation of oocyte maturation. Curr. Top. Cell Reg. 16, 271–311.CrossRefGoogle ScholarPubMed
Maller, J.L., Butcher, F.R. & Krebs, E.G. (1979). Early effect of progesterone on levels of cyclic adenosine 3',5'–monophos–phate in Xenopus oocytes. J. Biol. Chem. 254, 579–82.CrossRefGoogle Scholar
Masui, Y. & Clarke, H.J. (1979). Oocyte maturation. Int. Rev. Cytol. 57, 185–282.CrossRefGoogle ScholarPubMed
Moor, R.M., Osborn, J.C., Cran, D.C. & Walters, D.F. (1981). Selective effect of gonadotropins on cell coupling, nuclear maturation and protein synthesis in mammalian oocytes. J. Embryol. Exp. Morphol. 61, 347–65.Google ScholarPubMed
Morril, G.A., Schatz, F., Kostellow, A.B. & Poupko, J.M. (1977). Changes in cyclic AMP levels in the amphibian ovarian follicle following progesterone induction of meiotic maturation. Differentiation 8, 97–104.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
Sadler, S.E. & Maller, J.L. (1983). Inhibition of Xenopus oocyte adenylate cyclase by progesterone and 2', 5'-didoxyadeno-sine is associated with slowing of guanine nucleotide exchange. J. Biol. Chem. 258, 7935–41.CrossRefGoogle ScholarPubMed
Schuetz, A.W. (1985). Local control mechanisms during oogenesis and folliculogenesis. In Developmental Biology, vol. 1, ed. L., Browder, pp. 3–83. New York: Plenum Press.Google Scholar
Smith, L.D. (1989). The induction of oocyte maturation: transmembrane signalling events and regulation of the cell cycle. Development 107, 685–99.CrossRefGoogle ScholarPubMed
Staigmiller, R.B & Moor, R.M. (1984). Effect of follicle cells on the maturation and developmental competence of ovine oocytes matured outside the follicle. Gamete Res. 9, 221–9.CrossRefGoogle Scholar
Stith, B.J. & Maller, J.L. (1987). Induction of meiotic maturation in Xenopus oocytes by 12-O-tetradecanoylphorbol 13-acetate. Exp. Cell Res. 169, 514–23.CrossRefGoogle Scholar
Varnold, R.L. & Smith, L.D. (1991). Protein kinase C and progesterone-induced maturation in Xenopus oocytes. Development 109, 597–604.CrossRefGoogle Scholar
Vilain, J.P., Moreau, M. & Guerrier, p. (1980). Uncoupling of oocyte follicle cells triggers reinitiation of meiosis in amphibian oocytes. Dev. Growth Differ. 22, 687–91.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J. & Buhler, 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