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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Anti-Müllerian hormone reduces growth rate without altering follicular survival in isolated caprine preantral follicles cultured in vitro

R. M. P. Rocha A D , L. F. Lima A , I. R. Brito A , G. M. Silva A , H. H. V. Correia A , N. A. Ribeiro de Sá A , A. C. A. Ferreira A , A. D. Sales A , C. H. Lobo A , C. C. Campello A , J. Smitz B , M. B. Wheeler C and J. R. Figueiredo A
+ Author Affiliations
- Author Affiliations

A Laboratory of Manipulation of Oocytes and Preantral Follicles -LAMOFOPA, Faculty of Veterinary Medicine, State University of Ceará, Av. Paranjana 1700, Campus do Itaperi, Fortaleza, 60740-903 CE, Brazil.

B Follicle Biology Laboratory, Vrije Universiteit Brussel (VUB), Laarbeeklaan 101, B-1090 Brussels, Belgium.

C Department of Animal Sciences, University of Illinois, 1207 West Gregory Drive, Urbana, IL 61801, USA.

D Corresponding author. Email: rebeca_mpr@yahoo.com.br

Reproduction, Fertility and Development 29(6) 1144-1154 https://doi.org/10.1071/RD15290
Submitted: 17 July 2015  Accepted: 13 March 2016   Published: 11 May 2016

Abstract

The aim of the present study was to evaluate the effect of anti-Müllerian hormone (AMH), with and without FSH, on the in vitro development of isolated caprine preantral follicles, as well as follicular steroid production and mRNA levels of AMH, hormone receptors (AMH and FSH), CYP19A1 (cytochrome P450, family 19, subfamily A, polypeptide 1), CYP17 (cytochrome P450, family 17, subfamily A, polypeptide 1), HSD3B (3-beta-hydroxysteroid dehydrogenase) and Myc (myelocytomatosis oncogene). Isolated secondary follicles were cultured in minimum essential medium alpha (α-MEM+) alone or supplemented with 50 ng mL–1 AMH and/or 100 ng mL–1 FSH added sequentially on different days of culture. Follicles were cultured for a total of 18 days, with different media during the first (Days 0–9) and second (Days 10–18) halves of the culture period, resulting in six treatment groups, as follows: α-MEM+/α-MEM+, FSH/FSH, AMH/AMH, AMH+FSH/AMH+FSH, AMH/FSH, and FSH/AMH. Follicle development was evaluated on the basis of follicular growth, oocyte maturation and steroid secretion. There was a decrease in follicular growth rate in the AMH, AMH + FSH and AMH/FSH treatment groups compared with α-MEM+ and FSH treatment groups (P < 0.05). However, the different culture conditions had no effect on rates of meiotic resumption and steroid secretion (P > 0.05). Moreover, follicles cultured in the presence of FSH had lower levels of AMH receptor type II (AMHRII) mRNA compared with non-cultured control (freshly isolated follicles), and the AMH and AMH/FSH treatment groups. In conclusion, AMH reduces the follicular growth rate of isolated goat preantral follicles in vitro without affecting follicular survival.

Additional keywords: cell culture, folliculogenesis, goats.


References

Almeida, A. P., Magalhães-Padilha, D. M., Araújo, V. R., Costa, S. L., Chaves, R. N., Lopes, C. A. P., Donato, M. A., Peixoto, C. A., Campello, C. C., Junior, J. B., and Figueiredo, J. R. (2015). Effect of sequential medium with fibroblast growth factor-10 and follicle stimulating hormone on in vitro development of goat preantral follicles. Anim. Reprod. Sci. 152, 32–38.
Effect of sequential medium with fibroblast growth factor-10 and follicle stimulating hormone on in vitro development of goat preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFShs73N&md5=d7a89c94f288568541f25ef5f94e0429CAS | 25496673PubMed |

Alves, A. M. C. V., Chaves, R. N., Rocha, R. M. P., Lima, L. F., Andrade, P. M., Lopes, C. A. P., Souza, C. E., Moura, A. A., Campello, C. C., Báo, S. N., Smitz, J., and Figueiredo, J. R. (2013). Dynamic medium containing growth differentiation factor-9 and FSH maintains survival and promotes in vitro growth of caprine preantral follicles after long-term in vitro culture. Reprod. Fertil. Dev. 25, 955–965.
Dynamic medium containing growth differentiation factor-9 and FSH maintains survival and promotes in vitro growth of caprine preantral follicles after long-term in vitro culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrtrzN&md5=93a90b9026383cf779dfd9a2ba986772CAS |

Araújo, V. R., Silva, G. M., Duarte, A. B., Magalhães, D. M., Almeida, A. P., Gonçalves, R. F., Bruno, J. B., Silva, T. F., Campello, C. C., Rodrigues, A. P., and Figueiredo, J. R. (2011). Vascular endothelial growth factor-A(165) (VEGF-A(165)) stimulates the in vitro development and oocyte competence of goat preantral follicles. Cell Tissue Res. 346, 273–281.
Vascular endothelial growth factor-A(165) (VEGF-A(165)) stimulates the in vitro development and oocyte competence of goat preantral follicles.Crossref | GoogleScholarGoogle Scholar | 21987221PubMed |

Campbell, B. K., Clinton, M., and Webb, R. (2012). The role of anti-mullerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology 153, 4533–4543.
The role of anti-mullerian hormone (AMH) during follicle development in a monovulatory species (sheep).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtlagtb%2FJ&md5=fb24f22fe5e3cbd794d502c5870c3986CAS | 22778215PubMed |

Chaves, R. N., Duarte, A. B. G., Rodrigues, G. Q., Celestino, J. J. H., Silva, G. M., Lopes, C. A. P., Almeida, A. P., Donato, M. A. M., Peixoto, C. A., Moura, A. A., Lobo, C. H., Locatelli, Y., Mermillod, P., Campello, C. C., and Figueiredo, J. R. (2012). The effects of insulin and follicle stimulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles. Biol. Reprod. 87, 69.
The effects of insulin and follicle stimulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles.Crossref | GoogleScholarGoogle Scholar | 22811569PubMed |

Crozet, N., Dahirel, M., and Gall, L. (2000). Meiotic competence of in vitro grown goat oocytes. J. Reprod. Fertil. 118, 367–373.
Meiotic competence of in vitro grown goat oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitlCqu74%3D&md5=aaa4bc637c7629ca06d0f1a6ebae6baaCAS | 10864802PubMed |

Demeestere, I., Streiff, A. K., Suzuki, J., Al-Khabouri, S., Mahrous, E., Tan, S. L., and Clarke, H. J. (2012). Follicle-stimulating hormone accelerates mouse oocyte development in vivo. Biol. Reprod. 87, 3.
Follicle-stimulating hormone accelerates mouse oocyte development in vivo.Crossref | GoogleScholarGoogle Scholar | 22517620PubMed |

Diaz, F. J., Wigglesworth, K., and Eppig, J. J. (2007). Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev. Biol. 305, 300–311.
Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksV2lu7Y%3D&md5=51c8ba2aac9177d845a7a0823d3f0d07CAS | 17368609PubMed |

Dorphin, B., Prades-Borio, M., Anastacio, A., Rojat, P., Coussieu, C., and Poirot, C. (2012). Secretion profiles from in vitro cultured follicles, isolated from fresh prepubertal and adult mouse ovaries or frozen–thawed prepubertal mouse ovaries. Zygote 20, 181–192.
Secretion profiles from in vitro cultured follicles, isolated from fresh prepubertal and adult mouse ovaries or frozen–thawed prepubertal mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVCrtLc%3D&md5=6d7b6453eab52f4c912c2920aebe7992CAS | 21729379PubMed |

Durlinger, A. L., Kramer, P., Karels, B., De Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (1999). Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 140, 5789–5796.
Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12htLc%3D&md5=66dffd2acf3e3c99f3e4d6df5ffeb5fdCAS | 10579345PubMed |

Durlinger, A. L., Gruijters, M. J., Kramer, P., Karels, B., Kumar, T. R., Matzuk, M. M., Rose, U. M., De Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (2001). Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 142, 4891–4899.
Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGqu78%3D&md5=fdd52662583cb8d529e9cf204dc606d3CAS | 11606457PubMed |

Hsueh, A. J., Kawamura, K., Cheng, Y., and Fauser, B. C. (2015). Intraovarian control of early folliculogenesis. Endocr. Rev. 36, 1–24.
Intraovarian control of early folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Shsrg%3D&md5=0585a6978e818c68a2b76f6b6a2d56dbCAS | 25202833PubMed |

Lima, I. M. T., Celestino, J. J. H., Faustino, L. R., Magalhães-Padilha, D. M., Rossetto, R., Brito, I. R., Donato, M. A. M., Lopes, C. A. P., Campello, C. C., Peixoto, C. A., Figueiredo, J. R., and Rodrigues, A. P. R. (2012). Dynamic medium containing kit ligand and follicle-stimulating hormone promotes follicular survival, activation, and growth during long-term in vitro culture of caprine preantral follicles. Cells Tissues Organs 195, 260–271.
Dynamic medium containing kit ligand and follicle-stimulating hormone promotes follicular survival, activation, and growth during long-term in vitro culture of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVGiu7Y%3D&md5=88f004dfff68b3f25305b53514232ae7CAS |

Magalhães-Padilha, D. M., Andrade, P. M., Sales, E. T., Araujo, V. R., Lima, I. M. T., Castro, S. V., Faustino, L. R., Lopes, C. A. P., Campello, C. C., Báo, S. N., Gastal, M. O., Gastal, E. L., and Figueiredo, J. R. (2012). Effect of sequential medium on in vitro culture of goat ovarian cortical tissue. Anim. Reprod. Sci. 132, 159–168.
Effect of sequential medium on in vitro culture of goat ovarian cortical tissue.Crossref | GoogleScholarGoogle Scholar | 22727672PubMed |

Magalhães-Padilha, D. M., Geisler-Lee, J., Wischral, A., Gastal, M. O., Fonseca, G. R., Eloy, Y. R., Geisler, M., Figueiredo, J. R., and Gastal, E. L. (2013). Gene expression during early folliculogenesis in goats using microarray analysis. Biol. Reprod. 89, 19.
Gene expression during early folliculogenesis in goats using microarray analysis.Crossref | GoogleScholarGoogle Scholar |

McGee, E. A., Smith, R., Spears, N., Nachtigal, M. W., Ingraham, H., and Hsueh, A. J. (2001). Müllerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol. Reprod. 64, 293–298.
Müllerian inhibitory substance induces growth of rat preantral ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCkuw%3D%3D&md5=b55ae47167bbea5a4ea43ec8c83f05beCAS | 11133686PubMed |

Nilsson, E., Rogers, N., and Skinner, M. K. (2007). Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 134, 209–221.
Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrfO&md5=e7e1caec180feb12d68555fb555a3bedCAS | 17660231PubMed |

Palma, G. A., Argañaraz, M. E., Barrera, A. D., Rodler, D., Mutto, A. Á., and Sinowatz, F. (2012). Biology and biotechnology of follicle development. ScientificWorldJournal 2012, 938138.
Biology and biotechnology of follicle development.Crossref | GoogleScholarGoogle Scholar | 22666170PubMed |

Park, J. H., Maclaughlin, D. T., and Teixeira, J. M. (2011). The rate of in vitro maturation of primary follicles from adult mice and the quality of oocytes is improved in the absence of anti-mullerian hormone. Reprod. Sci. 18, 334–341.
The rate of in vitro maturation of primary follicles from adult mice and the quality of oocytes is improved in the absence of anti-mullerian hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVGqu7w%3D&md5=514ba4a39ecd30cf87d21b9ec4ebb209CAS | 21098214PubMed |

Rocha, R. M. P., Lima, L. F., Carvalho, A. A., Chaves, R. N., Bernuci, M. P., Rosa-E-Silva, A. C. J. S., Rodrigues, A. P. R., Campello, C. C., and Figueiredo, J. R. (2016). Immunolocalization of the anti-Müllerian hormone (AMH) in caprine follicles and the effects of AMH on in vitro culture of caprine pre-antral follicles enclosed in ovarian tissue. Reprod. Domest. Anim. 51, 212–219.
Immunolocalization of the anti-Müllerian hormone (AMH) in caprine follicles and the effects of AMH on in vitro culture of caprine pre-antral follicles enclosed in ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XjvFGhu7g%3D&md5=3caba881fa3ebd9cc07fa2674f8be5d2CAS |

Rodrigues, G. Q., Bertoldo, M. J., Brito, I. R., Silva, C. M., Sales, A. D., Castro, S. V., Duffard, N., Locatelli, Y., Mermillod, P., Lobo, C. H., Campello, C. C., Rodrigues, A. P., Freitas, V. J., and Figueiredo, J. R. (2014). Relative mRNA expression and immunolocalization for transforming growth factor-beta (TGF-β) and their effect on in vitro development of caprine preantral follicles. In Vitro Cell. Dev. Biol. Anim. 50, 688–699.
Relative mRNA expression and immunolocalization for transforming growth factor-beta (TGF-β) and their effect on in vitro development of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpsVagtLs%3D&md5=6b7e771c1507eb7be9ec6833734d98f8CAS | 24879083PubMed |

Sánchez, F., and Smitz, J. (2012). Molecular control of oogenesis. Biochim. Biophys. Acta 1822, 1896–1912.
Molecular control of oogenesis.Crossref | GoogleScholarGoogle Scholar | 22634430PubMed |

Sánchez, F., Adriaenssens, T., Romero, S., and Smitz, J. (2010). Different follicle-stimulating hormone exposure regimens during antral follicle growth alter gene expression in the cumulus–oocyte complex in mice. Biol. Reprod. 83, 514–524.
Different follicle-stimulating hormone exposure regimens during antral follicle growth alter gene expression in the cumulus–oocyte complex in mice.Crossref | GoogleScholarGoogle Scholar | 20592308PubMed |

Sánchez, F., Romero, S., and Smitz, J. (2011). Oocyte and cumulus cell transcripts from cultured mouse follicles are induced to deviate from normal in vivo conditions by combinations of insulin, follicle-stimulating hormone, and human chorionic gonadotropin. Biol. Reprod. 85, 565–574.
Oocyte and cumulus cell transcripts from cultured mouse follicles are induced to deviate from normal in vivo conditions by combinations of insulin, follicle-stimulating hormone, and human chorionic gonadotropin.Crossref | GoogleScholarGoogle Scholar | 21565993PubMed |

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., and Figueiredo, J. R. (2010). Dynamic medium produces caprine embryo from preantral follicles grown in vitro. Reprod. Sci. 17, 1135–1143.
Dynamic medium produces caprine embryo from preantral follicles grown in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1akt77F&md5=043e64316bcb4dcdde226d683436d95dCAS |

Stubbs, S. A., Hardy, K., Da Silva-Buttkus, P., Stark, J., Webber, L. J., Flanagan, A. M., Themmen, A. P., Visser, J. A., Groome, N. P., and Franks, S. (2005). Anti-Mullerian hormone protein expression is reduced during the initial stages of follicle development in human polycystic ovaries. J. Clin. Endocrinol. Metab. 90, 5536–5543.
Anti-Mullerian hormone protein expression is reduced during the initial stages of follicle development in human polycystic ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFWjt7zN&md5=0e355db7e95fafe1bf6334437fbcce97CAS | 16030171PubMed |

Xu, J., Bernuci, M. P., Lawson, M. S., Yeoman, R. R., Fisher, T. E., Zelinski, M. B., and 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, 685–697.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfK&md5=d87449419fbad20d7d1f4e01d4867b15CAS | 20729335PubMed |