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Activin-A promotes the development of goat isolated secondary follicles in vitro

Published online by Cambridge University Press:  13 August 2013

Cleidson Manoel Gomes da Silva ,
Simone Vieira Castro ,
Luciana Rocha Faustino ,
Giovanna Quintino Rodrigues ,
Ivina Rocha Brito ,
Rafael Rossetto ,
Márcia Viviane Alves Saraiva ,
Claudio Cabral Campello ,
Carlos Henrique Lobo  and
Carlos Eduardo Azevedo Souza
...Show all authors
Cleidson Manoel Gomes da Silva*
Affiliation:
Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Paranjana, 1700, Campus do Itaperi, CEP: 60740–000, Fortaleza–CE–Brasil.
Simone Vieira Castro
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Luciana Rocha Faustino
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Giovanna Quintino Rodrigues
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Ivina Rocha Brito
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Rafael Rossetto
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Márcia Viviane Alves Saraiva
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Claudio Cabral Campello
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Carlos Henrique Lobo
Affiliation:
Laboratory of Animal Physiology, Department of Animal Science, Federal University of Ceará, Fortaleza, CE, Brazil.
Carlos Eduardo Azevedo Souza
Affiliation:
Laboratory of Animal Physiology, Department of Animal Science, Federal University of Ceará, Fortaleza, CE, Brazil.
Arlindo de Alencar Araripe Moura
Affiliation:
Laboratory of Animal Physiology, Department of Animal Science, Federal University of Ceará, Fortaleza, CE, Brazil.
Mariana Aragão Matos Donato
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife, PE, Brazil.
Christina Alves Peixoto
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife, PE, Brazil.
José Ricardo de Figueiredo
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
*
All correspondence to: Cleidson Manoel Gomes da Silva. Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Paranjana, 1700, Campus do Itaperi, CEP: 60740–000, Fortaleza–CE–Brasil. Tel: +55 85 3101 9852. Fax: +55 85 3101 9840. e-mail: [email protected]
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Summary

The role of activin-A in follicular development and on the mRNA expression levels of different genes in goat secondary follicles was evaluated. Goat secondary follicles (≥150 μm) were cultured for 18 days under control conditions or with the addition of either 50 or 100 ng/ml activin-A (Experiment 1). The mRNA levels for the genes that code for activin-A, ActR-IA, ActR-IB, ActR-IIA, ActR-IIB, follicle stimulating hormone receptor (FSH-R) and P450 aromatase were measured in each condition (Experiment 2). We observed that after 6 days of culture, the antrum formation rate was higher in cultures with added activin-A than in the cultured control (P < 0.05). The addition of 50 ng/ml activin-A increased the follicular growth rate in the final third of the culture (days 12–18), resulting in a higher percentage of meiosis resumption (P < 0.05). On day 6, the addition of activin-A (50 ng/ml) increased the levels of ActR-IA mRNA compared with the cultured control (P < 0.05). After 18 days, the addition of 50 ng/ml activin-A significantly increased the levels of its own mRNA compared with the non-cultured control. Moreover, this treatment reduced the mRNA levels of P450 aromatase in comparison with the cultured control (P < 0.05). Higher levels of P450 aromatase mRNA were found for both activin-A treatments compared with the non-cultured control (P < 0.05). No difference in estradiol levels was detected among any of the tested treatments. In conclusion, the addition of activin-A to culture medium stimulated early antrum formation as well as an increase in the daily follicular growth rate and the percentage of meiosis resumption.

Keywords

Activin-AGoatIn vitro cultureP450 aromataseSecondary follicle
Type
Research Article
Information
Zygote , Volume 23 , Issue 1 , February 2015 , pp. 41 - 52
Copyright
Copyright © Cambridge University Press 2013 

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References

Alak, B.M., Coskun, S., Friedman, C.I., Kennard, E.A., Kim, M.H. & Seifer, D.B. (1998). Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil. Steril. 70, 1126–30.Google Scholar
Andreone, L., Velásquez, E.V., Abramovich, D., Ambao, V., Loreti, N., Croxatto, H.B., Parborell, F., Tesone, M. & Campo, S. (2009). Regulation of inhibin/activin expression in rat early antral follicles. Mol. Cell. Endocrinol. 309, 48–54.Google Scholar
Arunakumari, G., Shanmugasundaram, N. & Rao, V.H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.Google Scholar
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.CrossRefGoogle ScholarPubMed
Chaves, R.N., Alves, A.M.C.V., Faustino, L.R., Oliveira, K.P.L., Campello, C.C., Lopes, C.A.P., Báo, S.N. & Figueiredo, J.R. (2011). How the concentration of insulin affects the development of preantral follicles in goats. Cell Tissue Res. 346, 451–6.CrossRefGoogle ScholarPubMed
Cossigny, D.A., Findlay, J.K. & Drummond, A.E. (2012). The effects of FSH and activin-A on follicle development in vitro. Reproduction 143, 221–9.Google Scholar
Crozet, N., Dahirel, M. & Gall, L. (2000). Meiotic competence of in vitro grown goat oocytes. J. Reprod. Fertil. 118, 367–73.Google Scholar
Ethier, J. & Findlay, J.K. (2001). Roles of activin and its signal transduction mechanisms in reproductive tissues. Reproduction 121, 667–75.Google Scholar
Gupta, P.S.P., Ramesh, H.S., Manjunatha, B.M., Nandi, S. & Ravindra, J.P. (2008). Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16, 57–63.Google Scholar
Hulshof, S.C.J., Figueiredo, J.R., Beckers, J.F., Bevers, M.M., Vanderstichele, H. & van den Hurk, R. (1997). Bovine preantral follicles and activin: immunohistochemistry for activin and activin receptor and the effect of bovine activin A in vitro. Theriogenology 48, 133–42.Google Scholar
Knight, P.G. & Glister, C. (2001). Potential local regulatory functions of inhibins, activins and follistatin in the ovary. Reproduction 121, 503–12.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–8.Google Scholar
Magalhães, D.M., Duarte, A.B.G., Araújo, V.R., Brito, I.R., Soares, T.G., Lima, I.M.T., Lopes, C.A.P., Campello, C.C., Rodrigues, A.P.R. & Figueiredo, J.R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–8.Google Scholar
McLaughlin, M., Bromfield, J.J., Albertini, D.F. & Telfer, E.E. (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol. Hum. Reprod. 16, 644–53.Google Scholar
McNatty, K.P., Fidler, A.E., Juengel, J.L., Quirke, L.D., Smith, P.R., Heath, D.A., Lundy, T., O'Connell, A. & Tisdall, D.J. (2000). Growth and paracrine factors regulating follicular formation and cellular function. Mol. Cell. Endocrinol. 163, 11–20.Google Scholar
Miyano, T. & Manabe, N. (2007). Oocyte growth and acquisition of meiotic competence. Soc. Reprod. Fertil. Suppl. 63, 531–8.Google Scholar
Nottola, S.A., Cecconi, S., Bianchi, S., Motta, C., Rossi, G., Continenza, M.A. & Macchiarelli, G. (2011). Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod. Biol. Endocrinol. 9, 3–13.Google Scholar
O'Brien, M.J., Pendola, J.K. & Eppig, J.J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–6.Google Scholar
Pangas, S.A., Jorgez, C.J., Tran, M., Agno, J., Li, X., Brown, C.W., Kumar, T.R. & Matzuk, M.M. (2007). Intraovarian Activins are required for female fertility. Mol. Endocrinol. 21, 2458–71.Google Scholar
Rabinovici, J., Goldsmith, P.C., Roberts, V.J., Vaughan, J., Vale, W. & Jaffe, R.B. (1991). Localization and secretion of inhibin/activin subunits in the human and subhuman primate fetal gonads. J. Clin. Endocrinol. Metab. 73, 1141–9.CrossRefGoogle ScholarPubMed
Rabinovici, J., Spencer, S.J., Doldi, N., Goldsmith, P.C., Schwall, R. & Jaffe, R.B. (1992). Activin-A as an intraovarian modulator: actions, localization, and regulation of the intact dimer in human ovarian cells. J. Clin. Invest. 89, 1528–36.Google Scholar
Rossetto, R., Lima-Verde, I.B., Matos, M.H.T., Saraiva, M.V.A., Martins, F.S., Faustino, L.R., Araújo, V.R., Silva, C.M.G., Name, K.P.O., Báo, S.N., Campello, C.C., Figueiredo, J.R. & Blume, H. (2009). Interaction between ascorbic acid and follicle-stimulating hormone maintains follicular viability after long-term in vitro culture of caprine preantral follicles. Dom. Anim. Endocrinol. 37, 112–23.CrossRefGoogle ScholarPubMed
Saraiva, M.V.A., Celestino, J.J.H., Araújo, V.R., Chaves, R.N., Almeida, A.P., Lima-Verde, I.B., Duarte, A.B.G., Silva, G.M., Martins, F.S., Bruno, J.B., Matos, M.H.T., Campello, C.C., Silva, J.R.V. & Figueiredo, J.R. (2010a). Expression of follicle-stimulating hormone receptor (FSH-R) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles. Zygote 19, 205–14.Google Scholar
Saraiva, M.V.A., Rossetto, R., Brito, I.R., Celestino, J.J.H., Silva, C.M.G., Faustino, L.R., Almeida, A.P., Bruno, J.B., Magalhães, D.M., Matos, M.H.T., Campello, C.C. & Figueiredo, J.R. (2010b). Dynamic medium produces caprine embryo from preantral follicles grown in vitro. Reprod. Sci. 17, 1135–43.Google Scholar
Silva, C.C. & Knight, P.G. (1998). Modulatory actions of activin-A and follistatin on the developmental competence of in vitro-matured bovine oocytes. Biol. Reprod. 58, 558–65.Google Scholar
Silva, J.R.V., van den Hurk, R., van Tol, H.T.A., Roelen, B.A.J. & Figueiredo, J.R. (2004). Gene expression and protein localisation for activin-A, follistatin and activin receptors in goat ovaries. J. Endocrinol. 183, 405–15.Google Scholar
Silva, G.M., Araújo, V.R., Duarte, A.B.G., Chaves, R.N., Silva, C.M.G., Lobo, C.H., Almeida, A.P., Matos, M.H.T., Tavares, L.M.T., Campelo, C.C. & Figueiredo, J.R. (2011). Ascorbic acid improves the survival and in vitro growth of isolated caprine preantral follicles. Anim. Reprod. 8, 14–24.Google Scholar
Telfer, E.E., McLaughlin, M., Ding, C. & Thong, K.J. (2008). A two step serum free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23, 1151–8.Google Scholar
Thomas, F.H., Armstrong, D.G. & Telfer, E.E. (2003). Activin promotes oocyte development in ovine preantral follicles in vitro. Reprod. Biol. Endocrinol. 1, 1–76.Google Scholar
Xu, J., Bernuci, M.P., Lawson, M.S., Yeoman, R.R., Fisher, T.E., Zelinski, M.B. & Stouffer, R.L. (2010). Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 140, 685–97.Google Scholar
Zhao, J., Taverne, M.A.M., van der Weijden, G.C., Bevers, M.M. & van den Hurk, R. (2001). Effect of activin-A on in vitro development of rat preantral follicles and localization of activin-A and activin receptor II. Biol. Reprod. 65, 967–77.Google Scholar