Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-27T21:26:49.208Z Has data issue: false hasContentIssue false

Involvement of G protein and purines in Rhinella arenarum oocyte maturation

Published online by Cambridge University Press:  02 February 2012

L.I. Zelarayán
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
M.T. Ajmat
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
F. Bonilla
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000- San Miguel de Tucumán, Argentina.
*
All correspondence to: Marta Bühler. Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000- San Miguel de Tucumán, Argentina. Fax: +54 381 4247752 (interno 7004). e-mail: [email protected]

Summary

We investigated the participation of Gαi protein and of intracellular cAMP levels on spontaneous and progesterone-mediated maturation in Rhinella arenarum fully grown follicles and denuded oocytes.

Although progesterone is the established maturation inducer in amphibians, Rhinella arenarum oocytes obtained during the reproductive period (competent oocytes) resume meiosis with no need for an exogenous hormonal stimulus if deprived of their enveloping follicular cells, a phenomenon called spontaneous maturation. In amphibian oocytes, numerous signalling mechanisms have been involved in the rapid, non-genomic, membrane effects of progesterone, but most of these are not fully understood.

The data presented here demonstrate that activation of the Gαi protein by Mas-7 induced maturation in non-competent oocytes and also an increase in GVBD (germinal vesicle breakdown) in competent oocytes. Similar results were obtained with intact follicles independent of the season. The activation of adenylyl cyclase (AC) by forskolin seems to inhibit both spontaneous and progesterone-induced GVBD. In addition, the high intracellular levels of cAMP caused by activation of AC by forskolin treatment or addition of db-cAMP inhibited maturation that had been induced by Mas-7 and in a dose-dependent manner. Treatment with H-89, a protein kinase A (PKA) inhibitor, was able to trigger GVBD in a dose-dependent manner in non-competent oocytes and increased the percentages of GVBD in oocytes competent to mature spontaneously. The results obtained with whole follicles and denuded oocytes were similar, which suggested that effects on AC and PKA were not mediated by follicle cells. The fact that Mas-7 was able to induce maturation in non-competent oocytes in a similar manner to progesterone and to increase spontaneous maturation suggests that Gαi activation could be an important step in meiosis resumption. Thus, the decrease in cAMP as a result of the regulation of the G proteins on AC and the inactivation of PKA by H-89 could contribute to the activation of MPF (maturation promoting factor) and induce maturation of the oocytes of Rhinella arenarum.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Cerdá, J., Petrino, T.R., Landin, A.M. & Lin, Y-W.P. (1997). Effects of isoquinolinesulfonamide H-8 on Fundulus heteroclitus ovarian follicles: role of cyclic nucleotide-dependent protein kinase on steroidogenesis and oocyte maturation in vitro. Comp. Biochem. Physiol. 117, 7581.Google ScholarPubMed
Cho, W.K, Stern, S. & Biggers, J.D. (1974). Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187, 383–6.CrossRefGoogle ScholarPubMed
Cicirelli, M.F. & Smith, L.D. (1985). Cyclic AMP levels during the maturation of Xenopus oocytes. Dev. Biol. 108, 254–8.CrossRefGoogle ScholarPubMed
Gallo, C.J., Hand, A.R., Jones, T.L. & Jaffe, L.A. (1995). Stimulation of Xenopus oocyte maturation by inhibition of G-protein alpha S subunit, a component of the plasma membrane and yolk platelets membrane. J. Cell Biol. 130, 275–84.CrossRefGoogle Scholar
Higashijima, T., Burnier, J. & Ross, E.M. (1990). Regulation of Gi and G0 by mastoparan, related amphiphilic peptides and hydrophobic amines. Mechanism and structural determinants of activity. J. Biol. Chem. 265, 14176–86.CrossRefGoogle Scholar
Kalinowsky, R.R., Berlot, C.H., Jones, T.L., Ross, L.F., Jaffe, L.A. & Mehlmann, L.M. (2004). Maintenance of the meiotic prophase arrest in vertebrate oocytes by a Gs protein mediated pathway. Dev. Biol. 267, 113.CrossRefGoogle Scholar
Kwon, H.B., Lin, Y.P., Choi, M.J. & Ahn, R.S. (1989). Spontaneous maturation of follicle oocytes in Rana dybowskii in vitro: seasonal influences, progesterone production and involvement of cAMP. J. Exp. Zool. 252, 190–9.CrossRefGoogle ScholarPubMed
Kwon, H.B., Park, H.J. & Schuetz, A.W. (1990). Induction of inhibition meiotic maturation of amphibian (Rana dybowskii) follicular oocytes by forskolin and cAMP in vitro. Mol. Reprod. Dev. 25, 147–54.CrossRefGoogle ScholarPubMed
Lin, Y.W. & Schuetz, A.W. (1985). Spontaneous maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 1128.CrossRefGoogle Scholar
Lutz, L., Khim, B., Jahani, D. & Hammes, S. (2000). G proteins subunits inhibited nongenomic progesterone-induced signaling and maturation in X. laevis oocytes. J. Biol. Chem. 275, 41512–20.CrossRefGoogle Scholar
Maller, J.L. & Krebs, E.G. (1977). Progesterone-stimulated meiotic cell division in Xenopus oocytes, induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3′:5′-monophosphate-dependent protein kinase. J. Biol. Chem. 252, 1712–8.CrossRefGoogle ScholarPubMed
Maller, J.L. (2001). The elusive progesterone receptor in Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 98, 810.CrossRefGoogle ScholarPubMed
Masui, Y. & Shibuya, E.K. (1987). Development of cytoplasmic activities that control chromosome cycles during maturation of amphibian oocytes. In: Molecular Regulation of Nuclear Events in Mitosis and Meiosis (eds Schlegel, R., Halleck, M.S. & Roa, P.N.), pp. 142. Orlando: Academic Press.Google Scholar
Morrill, G.A., Schatz, F., Kostellow, A.B. & Poupko, J.M. (1977). Changes cyclic AMP levels in the amphibian ovarian follicle following progesterone induction of meiotic maturation. Differentiation 8, 97104.CrossRefGoogle ScholarPubMed
Romo, S., Hinrichs, M.V., Guzmán, L. & Olate, J. (2002). Gαs levels regulate Xenopus laevis oocyte maturation. Mol. Reprod. Dev. 63, 104–9.CrossRefGoogle ScholarPubMed
Sadler, S.E. & Maller, J.L. (1982) Identification of steroid receptors on the surface of Xenopus oocytes by photoaffinity labelling. J. Biol. Chem. 247, 355–61.CrossRefGoogle Scholar
Sánchez Toranzo, G., Bonilla, F, Oterino, J., Zelarayán, LI. & Bühler, M.I. (2004). Effect of insulin on spontaneous and progesterone-induced GVBD in Bufo arenarum denuded oocyte. Zygote 12, 185–95.CrossRefGoogle Scholar
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L.I., Oterino, J. & Buhler, M.I. (2006). Activation of maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents. Zygote 14, 305–16.CrossRefGoogle Scholar
Seamond, K.B., Padgett, W. & Dally, J.W. (1981). Forkolin: a unique diterpene activator a adenylate cyclase in membranes and intact cells. Proc. Natl. Acad. Sci. USA 78, 3363–7.CrossRefGoogle Scholar
Sheng, Y., Tiberi, M., Booth, RA., Ma, C. & Liu, X.J. (2001). Regulation of Xenopus oocyte meiosis arrest by G protein betagamma subunits. Curr. Biol. 11, 405–16.CrossRefGoogle ScholarPubMed
Sheng, Y., Montplaisir, V. & Liu, X.J. (2004). Co-operation of Gsα and Gβγ in maintaining G2 arrest in Xenopus oocytes. J. Cell Physiol. 202, 3240.CrossRefGoogle Scholar
Thomas, P., Zhu, Y. & Pace, M. (2002). Progestin membrane receptors involved in the meiotic maturation of teleost oocytes: a review with some new findings. Steroids 67, 511–7.CrossRefGoogle ScholarPubMed
Vilain, J.P., Moreau, M. & Guerrier, P. (1980). Uncoupling of oocytes follicles cells triggers reinitiation meiosis in amphibian oocytes. Dev. Growth Differ. 22, 689–91.CrossRefGoogle ScholarPubMed
Voronina, E. & Wessel, G.M. (2000). Regulatory contribution of G-proteins to oocyte maturation in the sea urchin. Mech. Dev. 121, 247–59.CrossRefGoogle Scholar
Voronina, E. & Wessel, G. (2003). The regulation of oocytes maturation. Curr. Topics Dev. Biol. 58, 53110.CrossRefGoogle Scholar
Voronina, E. & Wessell, G. (2004). Regulatory contribution of heterotrimeric G-proteins to oocyte maturation in the sea urchin. Mech. Dev. 121, 247–59.CrossRefGoogle ScholarPubMed
Zelarayán, L.I., 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
Zelarayán, L.I., Oterino, J., Sánchez Toranzo, G. & Buhler, M.I. (2000). Involvement of purines and phosphoinositides in spontaneous and progesterone-induced nuclear maturation. J. Exp. Zool. 287, 151–7.3.0.CO;2-S>CrossRefGoogle ScholarPubMed