Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T19:15:20.707Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro steroid-induced meiosis in Rhinella arenarum oocytes: role of pre-MPF activation

Published online by Cambridge University Press:  26 May 2015

Ana Josefina Arias Torres ,
Marta Inés Bühler  and
Liliana Isabel Zelarayán
Ana Josefina Arias Torres
Affiliation:
Instituto de Biología, Facultad de Bioqca, Qca. y Farmacia, INSIBIO-UNT, Chacabuco 461, Tucumán, Argentina
Marta Inés Bühler
Affiliation:
Instituto de Biología, Facultad de Bioqca, Qca. y Farmacia, INSIBIO-UNT, Chacabuco 461, Tucumán, Argentina
Liliana Isabel Zelarayán*
Affiliation:
Instituto de Biología, Facultad de Bioqca, Qca. y Farmacia, INSIBIO-UNT, Chacabuco 461, 4000 San Miguel de Tucumán, Tucumán, Argentina
*
All correspondence to: Liliana Isabel Zelarayán. Instituto de Biología, Facultad de Bioqca, Qca. y Farmacia, INSIBIO-UNT, Chacabuco 461, 4000 San Miguel de Tucumán, Tucumán, Argentina. Tel: +549 381 4247752 Int. 7093. Fax: +549 381 4247752 Int. 7004. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In this work we showed the relationship between seasonal periods and the response of R. arenarum follicles and oocytes to different steroids. Using in vitro germinal vesicle breakdown (GVBD) assays, we demonstrated that P4 is the main steroid capable of inducing maturation in R. arenarum oocytes and follicles. In the second part of this work we showed that androgens can activate pre-maturation promoting factors (pre-MPFs) such as P4, by cytoplasm microinjection experiments. The results indicated that the steroids assayed induced oocyte and follicle maturation in a dose- and time-dependent manner. In oocytes, P4 was the most efficient steroid as a maturation inducer (EC50 of the reproductive period, 6 nM, EC50 of the non-reproductive period ≅ 30 nM). Androgens (DHEA, dehydroepiandrosterone; T, testosterone; and AD, androstenedione) were less efficient maturation inducers than P4 (EC50 reproductive period ≅ 50, 120 and 600 nM respectively). Similar results were obtained with intact follicles in both seasonal periods. Although the response of follicles to the different androgens was variable, in no case was it above the above the response induced by P4. Independently of the season, oocytes and follicles incubated in P4, P5 and T underwent GVBD after 6–10 h while oocytes and follicles incubated in DHEA and AD matured more slowly. Furthermore, we demonstrated that microinjection of mature cytoplasm from androgen-treated oocytes is sufficient to promote GVBD in immature recipient oocytes (DHEA, 57 ± 12%; AD, 60 ± 8%; T, 56 ± 13%). Thus, androgens such as DHEA, T and AD are as competent as P4 to activate pre-MPF.

Keywords

MPFOocyte maturationRhinella arenarumSeasonal changesSteroids
Type
Research Article
Information
Zygote , Volume 24 , Issue 2 , April 2016 , pp. 252 - 258
Copyright
Copyright © Cambridge University Press 2015 

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

Bühler, M.I. & Petrino, T.R. (1983). Simplified technique for the observation of asters in amphibian eggs stratified by centrifugation. Mikroskopie 40, 344–6.Google Scholar
Canario, A.V., Scott, A.P. & Flint, A.P. (1989). Radioimmunoassay investigations of 20 beta-hydroxylated steroids in maturing/ovulating female rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol. 74, 77–84.CrossRefGoogle ScholarPubMed
Cao, S., Xu, Q., Zhanng, Y., Zhao, Y., Wei, W. & Qin, Z. (2014). Enviromental (anti)androgenic chemical affect germinal vesicle breakdown (GVBD) of Xenopus laevis oocytes in vitro . Toxicology In Vitro 28, 426–31.Google Scholar
Deng, J., Carbajal, L., Evaul, K., Rasar, M., Jamnongjit, M. & Hammes, S.R. (2009). Nongenomic steroid-triggered oocyte maturation: of mice and frogs. Steroids 74, 595–601.Google Scholar
El-Zein, G., Boujard, D., Garnier, D.H. & Joly, J. (1988). The dynamics of the steroidogenic response of perfused Xenopus ovarian explants to gonadotropins. Gen. Comp. Endocrinol. 71, 132–40.Google Scholar
Gobbetti, A., Polzonetti-Magni, A., Zerani, M., Carnevali, O. & Botte, V. (1985). Vitellogenin hormonal control in the green frog, Rana esculenta. Interplay between estradiol and pituitary hormones. Comp. Biochem. Physiol. A Comp. Physiol. 82, 855–8.Google Scholar
Haccard, O. & Jessus, C. (2006). Oocyte maturation, Mos and cyclins—a matter of synthesis: two functionally redundant ways to induce meiotic maturation. Cell Cycle 5, 1152–9.Google Scholar
Haccard, O., Dupré, A., Liere, P., Pianos, A., Eychenne, B., Jessus, C. & Ozon, R. (2012). Naturally occurring steroids in Xenopus oocyte during meiotic maturation. Unexpected presence and role of steroid sulfates. Mol. Cell. Endocrinol. 362, 110–9.CrossRefGoogle ScholarPubMed
LaMarca, M.J., Westphal, L.M. & Rein, D.A. (1985). Gonadotropins and the timing of progesterone-induced meiotic maturation of Xenopus laevis oocytes. Dev. Biol. 109, 32–40.Google Scholar
Liu, X.S., Ma, C., Hamam, A.W. & Liu, X.J. (2005). Transcription-dependent and transcription-independent functions of the classical progesterone receptor in Xenopus ovaries. Dev. Biol. 283, 180–90.Google Scholar
Lutz, L.B., Cole, L.M., Grupta, M.K., Kwist, K.W., Auchus, R.J. & Hammes, S.R. (2001). Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation. Proc. Natl. Acad. Sci. USA 13, 728–33.Google Scholar
Maller, J.L. & Krebs, E.G. (1980). Regulation of oocyte maturation. Curr. Top. Cell Regul. 16, 271–311.Google Scholar
Masui, Y. (1982). Oscillatory activity of maturation promoting factor (MPF) in extracts of Rana pipiens eggs. J. Exp. Zool. 224, 389–99.Google Scholar
Medina, M., Ramos, I., Crespo, C.A., Gonzalez-Calvar, S. & Fernandez, S.N. (2004). Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. Gen. Comp. Endocrinol. 136, 143–51.Google Scholar
Ortiz, M.E., Buhler, M.I. & Zelarayán, L.I. (2013). Involvement of PLA2, COX and LOX in Rhinella arenarum oocyte maturation. Zygote 27, 516–23.Google Scholar
Ortiz, M.E., Arias-Torres, A.J. & Zelarayán, L.I. (2014). Role of arachidonic acid cascade in Rhinella arenarum oocyte maturation. Zygote 25, 1–12.Google Scholar
Pickford, D.B. & Morris, I.D. (1999). Effects of endocrine-disrupting contaminants on amphibian oogenesis: methoxychlor inhibits progesterone-induced maturation of Xenopus laevis oocytes in vitro . Environ. Health Perspect. 107, 285–92.CrossRefGoogle ScholarPubMed
Ponthier, J.L., Shackleton, C.H. & Trant, J.M. (1998). Seasonal changes in the production of two novel and abundant ovarian steroids in the channel catfish (Ictalurus punctatus). Gen. Comp. Endocrinol. 111, 141–55.CrossRefGoogle ScholarPubMed
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L., Oterino, J. & Bühler, M.I. (2006). Activation of maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents. Zygote 14, 305–16.Google Scholar
Sen, U., Mukherjee, S.P., Bhattacharyya, S.P. & Mukherjee, D. (2002). Seasonal changes in plasma steroids in Indian major carp Labeo rohita: influence of homologous pituitary extract on steroid production and development of oocytes maturational competence. Gen. Comp. Endocrinol. 128, 123–34.Google Scholar
Sheng, Y., Tiberi, M., Booth, R.A., Ma, C. & Liu, X.J. (2001). Regulation of Xenopus oocyte meiosis arrest by G protein betagamma subunits. Curr. Biol. 11, 405–16.Google Scholar
Smith, L.D., Ecker, R.E. & Subtelny, S. (1968). In vitro induction of physiological maturation in Rana pipiens oocytes removed from their ovarian follicles. Dev. Biol. 17, 627–43.Google Scholar
Thibier-Fouchet, C., Mulner, O. & Ozon, R. (1976). Progesterone biosynthesis and metabolism by ovarian follicles and isolated oocytes Xenopus laevis . Biol. Reprod. 14, 317–26.CrossRefGoogle ScholarPubMed
White, S., Jamnongjit, M., Gill, A., Lutz, L. & Hammes, S.R. (2005). Specific modulation of nongenomic androgens signaling in the ovary. Steroids 70, 352–60.Google Scholar
Zelarayán, L.I., 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.Google Scholar
Zelarayán, L.I., 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.Google Scholar
Zelarayán, L.I., Ajmat, M.T., Bonilla, F. & Buhler, M.I. (2012). Involvement of G protein and purines in Rhinella arenarum oocyte maturation. Zygote 2, 1–10.Google Scholar