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Expression of angiotensin II receptors in the caprine ovary and improvement of follicular viability in vitro

Published online by Cambridge University Press:  14 October 2015

J.B. Bruno*
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. Fortaleza, CEBrasilCEP 60740 903.
I.B. Lima-Verde
Affiliation:
Institute for Technology and Research, Tiradentes University, Aracaju-SE, Brazil.
J.J.H. Celestino
Affiliation:
Institute of Health Sciences, University of International Integration Lusophone African-Brazilian, Acarape-CE, Brazil.
L.F. Lima
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
M.H.T. Matos
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
L.R. Faustino
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
M.A.M. Donato
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife-PE, Brazil.
C.A. Peixoto
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife-PE, Brazil.
C.C. Campello
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
J.R.V. Silva
Affiliation:
Biotechnology Nucleus of Sobral (NUBIS), Federal University of Ceara, Sobral-CE, Brazil.
J.R. Figueiredo
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
*
All correspondence to: J.B. Bruno. 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. Fortaleza, CE Brasil CEP 60740 903. Tel.: +55.85.3101.9852. Fax: +55.85.3101.9840. E-mail: [email protected]

Summary

This study aimed to evaluate mRNA levels of angiotensin II (ANG II) receptors (AGTR1 and AGTR2) in caprine follicles and to investigate the influence of ANG II on the viability and in vitro growth of preantral follicles. Real-time polymerase chain reaction (PCR) was used to quantify AGTR1 and AGTR2 mRNA levels in the different follicular stages. For culture, caprine ovaries were collected, cut into 13 fragments and then either directly fixed for histological and ultrastructural analysis (fresh control) or placed in culture for 1 or 7 days in α-minumum essential medium plus (α-MEM+) with 0, 1, 5, 10, 50 or 100 ng/ml ANG II. Then, the fragments were destined to morphological, viability and ultrastructural analysis. The results showed that primordial follicles had higher levels of AGTR1 and AGTR2 mRNA than secondary follicles. Granulosa/theca cells from antral follicles had higher levels of AGTR1 mRNA than their respective cumulus–oocyte complex (COCs). After 7 days of culture, ANG II (10 or 50 ng/ml) maintained the percentages of normal follicles compared with α-MEM+. Fluorescence and ultrastructural microscopy confirmed follicular integrity in ANG II (10 ng/ml). In conclusion, a high expression of AGTR1 and AGTR2 is observed in primordial follicles. Granulosa/theca cells from antral follicles had higher levels of AGTR1 mRNA. Finally, 10 ng/ml ANG II maintained the viability of caprine preantral follicles after in vitro culture.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

Acosta, T.J., Berisha, B., Ozawa, T., Sato, K., Schams, D. & Miyamoto, A. (1999). Evidence for a local endothelin-angiotensin-atrial natriuretic peptide systemin bovine mature follicles in vitro: effects on steroid hormones and prostaglandin secretion. Biol. Reprod. 61, 1419–25.Google Scholar
Barreta, M.H., Oliveira, J.F.C., Ferreira, R., Antoniazzi, A.Q., Gasperin, B.G., Sandri, L.R. & Gonçalves, P.B.D. (2008). Evidence that the effect of angiotensin II on bovine oocyte nuclear maturation is mediated by prostaglandins E2 and F2a. Reproduction 136, 733–40.CrossRefGoogle Scholar
Berisha, B., Schams, D. & Miyamoto, A. (2002). The mRNA expression of angiotensin and endothelin system members in bovine ovarian follicles during final follicular growth. J. Reprod. Dev. 48, 573–82.Google Scholar
Chaves, R.N., Martins, F.S., Saraiva, M.V.A., Celestino, J.J.H., Lopes, C.A.P., Correia, J.C., Lima-Verde, I.B., Matos, M.H.T., Báo, S.N., Name, K.P.O., Campello, C.C., Silva, J.R.V. & Figueiredo, J.R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro . Reprod. Fertil. Dev. 20, 640–7.Google Scholar
Desai, N., Alex, A., Abdel Hafez, F., Calabro, A., Goldfarb, J., Fleischman, A. & Falcone, T. (2010). Three-dimensional in vitro follicle growth: overview of culture models, biomaterials, design parameters and future directions. Reprod. Biol. Endocrinol. 119, 112.Google Scholar
Feral, C., Le Gall, S. & Leymarie, P. (1995). Angiotensin II modulates steroidogenesis in granulosa and theca in the rabbit ovary: Its possible involvement in atresia. Eur. J. Endocrinol. 133, 747–53.Google Scholar
Ferreira, R., Oliveira, J.F., Fernandes, R., Moraes, J.F. & Gonçalves, P.B. (2007). The role of angiotensin II in the early stages of bovine ovulation. Reproduction 134, 713–9.CrossRefGoogle ScholarPubMed
Ferreira, R., Gasperin, B., Santos, J., Rovani, M., Santos, R.A., Gutierrez, K., Oliveira, J.F., Reis, A.M. & Gonçalves, P.B. (2011a). Angiotensin II profile and mRNA encoding RAS proteins during bovine follicular wave. J. Renin-Angiotensin-Aldosterone Syst. 12, 475–82.CrossRefGoogle ScholarPubMed
Ferreira, R., Gasperin, B., Rovani, M., Santos, J., Barreta, M., Bohrer, R., Price, C. & Gonçalves, P.B.D. (2011b). Angiotensin II signaling promotes follicle growth and dominance in cattle. Endocrinology 152, 4957–65.Google Scholar
Frota, I.M., Leitão, C.C., Costa, J.J., Brito, I.R., van den Hurk, R. & Silva, J.R. (2011). Stability of housekeeping genes and expression of locally produced growth factors and hormone receptors in goat preantral follicles. Zygote 19, 7183.CrossRefGoogle ScholarPubMed
Garor, R., Abir, R., Erman, A., Felz, C., Nitke, S., Fisch, B. (2009). Effects of basic fibroblast growth factor on in vitro development of human ovarian primordial follicles. Fertil. Steril. 91, 1967–75.Google Scholar
Giometti, I.C., Bertagnolli, A.C., Ornes, R.C., Da Costa, L.F.S., Carambula, S.F., Reis, A.M., De Oliveira, J.F.C., Emanuelli, I.P. & Gonçalves, P.B.D. (2005). Angiotensin II reverses the inhibitory action produced by theca cells on bovine oocyte nuclear maturation. Theriogenology 63, 1014–25.Google Scholar
Hartshorne, G. (1997). In vitro culture of ovarian follicles. Rev. Reprod. 2, 94104.CrossRefGoogle ScholarPubMed
Husain, A., Bumpus, F.M., Silva, P. & Speth, R.C. (1987). Localization of angiotensin II receptors in ovarian follicles and the identification of angiotensin II in rat ovaries. Proc. Natl. Acad. Sci. USA 84, 2489–93.Google Scholar
Itoh, H., Mukoyama, M., Pratt, R.E., Gibbons, G.H. & Dzau, V.J. (1993). Multiple autocrine growth factors modulate vascular smooth muscle cell growth response to angiotensin II. J. Clin. Invest. 91, 2268–74.Google Scholar
Lerer-Serfaty, G., Samara, N., Fisch, B., Shachar, M., Kossover, O., Seliktar, D., Ben-Haroush, A. & Abir, R. (2013). Attempted application of bioengineered/biosynthetic supporting matrices with phosphatidylinositol-trisphosphate-enhancing substances to organ culture of human primordial follicles. J. Assist. Reprod. Genet. 30, 1279–88.Google Scholar
Li, Y.H., Jiao, L.H., Liu, R.H., Chen, X.L., Wang, H. & Wang, W.H. (2004). Localization of angiotensin II in pig ovary and its effects on oocyte maturation in vitro . Theriogenology 61, 447–59.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
Lucci, C.M., Amorim, C.A., Báo, S.N., Figueiredo, J.R., Rodrigues, A.P.R., Silva, J.R. & Gonçalves, P.B.D. (1999). Effect of the interval of serial sections of ovarian in the tissue chopper on the number of isolated caprine preantral follicles. Anim. Reprod. Sci. 56, 3949.Google Scholar
Lucci, C.M., Silva, J.R., Carvalho, C.A., Figueiredo, J.R. & Báo, S.N. (2001). Light microscopical and ultrastructural characterization of goat preantral follicles. Small Rumin. Res. 41, 61–9.Google Scholar
Paul, M., Mehr, A.P. & Kreutz, R. (2006). Physiology of local renin–angiotensin systems. Physiol. Rev. 86, 747803.CrossRefGoogle ScholarPubMed
Portela, V.M., Gonçalves, P.B.D., Veiga, A.M., Nicola, E., Buratini, J.J. & Price, C.A. (2008). Regulation of angiotensin type 2 receptor in bovine granulosa cells. Endocrinology 149, 5004–11.CrossRefGoogle ScholarPubMed
Portela, V.M., Zamberlam, G., Gonçalves, P.B.D., de Oliveira, J.F.C. & Price, C.A. (2011). Role of angiotensin II in the periovulatory epidermal growth factor like cascade in bovine granulosa cells in vitro . Biol. Reprod. 85, 1167–74.Google Scholar
SAS Institute, Inc. (2002). Sas/STAT1 9.0 User's Guide. Cary, NC: SAS Institute Inc.Google Scholar
Shuttleworth, G., Broughton Pipkin, F.B. & Hunter, M.G. (2002). In vitro development of pig preantral follicles cultured in a serum-free medium and the effect of angiotensin II. Reproduction 123, 807–18.Google Scholar
Silva, J.R.V., van den Hurk, R., Costa, S.H.F., Andrade, E.R., Nunes, A.P.A., Ferreira, F.V.A., Lôbo, R.N.B. & Figueiredo, J.R. (2004). Survival and growth of goat primordial follicles after in vitro culture of ovarian cortical slices in media containing coconut water. Anim. Reprod. Sci. 81, 273–86.Google Scholar
Steel, R.G.D., Torrie, J.H. & Dickey, D.A. (1997). Principles and procedures of statistics: a biometrical approach. New York, NY: McGraw-Hill.Google Scholar
Stefanello, J.R., Barreta, M.H., Porciuncula, P.M., Arruda, J.N., Oliveira, J.F., Oliveira, M.A. & Gonçalves, P.B. (2006). Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068–76.Google Scholar
van Tol, H.T. & Bevers, M.M. (1998). Theca cells and theca-cell conditioned medium inhibit the progression of FSH-induced meiosis of bovine oocytes surrounded by cumulus cells connected to membrane granulosa. Mol. Reprod. Dev. 51, 315–21.Google Scholar
Yoon, S-J., Kim, K-H., Chung, H-M., Choi, D-H., Lee, W-S., Cha, K-Y. & Lee, K-A. (2006). Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fert. Steril. 85, 193203.Google Scholar
Yoshimura, Y. (1997). The ovarian renin–angiotensin system in reproductive physiology. Front. Neuroendocrinol. 18, 247–91.Google Scholar
Yoshimura, Y., Karubc, M., Koyama, N., Shiokawa, S., Nanno, T. & Nakamura, Y. (1992). Angiotensin II directly induces follicle rupture and oocyte maturation in the rabbit. FEBS Lett. 307, 305–8.Google Scholar
Yoshimura, Y., Karube, M., Oda, T., Koyama, N., Shiokawa, S., Akiba, M., Yoshinaga, A. & Nakamura, Y. (1993). Locally produced angiotensin II induces ovulation by stimulating prostaglandin production in vitro perfused rabbit ovaries. Endocrinology 133, 1609–16.Google Scholar
Yoshimura, Y., Karube, M., Aoki, H., Oda, T., Koyama, N., Nagai, A., Akimoto, Y., Hirano, H. & Nakamura, Y. (1996). Angiotensin II induces ovulation and oocyte maturation in rabbit ovaries via the AT2 receptor subtype. Endocrinology 137, 1204–11.Google Scholar
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