Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of FSH on the expression of receptors for oocyte-secreted factors and members of the EGF-like family during in vitro maturation in cattle

Ester Siqueira Caixeta A , Mariana Fernandes Machado A , Paula Ripamonte B , Christopher Price C and José Buratini B D
+ Author Affiliations
- Author Affiliations

A Departamento de Farmacologia, Instituto de Biociências, Universidade Estadual Paulista Julio de Mesquita Filho, Rubião Junior, Botucatu, São Paulo, 18618-970, Brazil.

B Departamento de Fisiologia, Instituto de Biociências, Universidade Estadual Paulista Julio de Mesquita Filho, Rubião Junior, Botucatu, São Paulo, 18618-970, Brazil.

C Present address: Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Quebec J2S 7C6, Canada.

D Corresponding author. Email: buratini@ibb.unesp.br

Reproduction, Fertility and Development 25(6) 890-899 https://doi.org/10.1071/RD12125
Submitted: 18 April 2012  Accepted: 25 July 2012   Published: 1 October 2012

Abstract

FSH induces expansion of bovine cumulus–oocyte complexes (COCs) in cattle, which can be enhanced by oocyte-secreted factors (OSFs). In this study it was hypothesised that FSH stimulates COC expansion in part from direct stimulation of the epidermal growth factor (EGF)-like ligands amphiregulin (AREG), epiregulin (EREG) and betacellulin (BTC), but also in part through regulation of OSFs or their receptors in cumulus cells. Bovine COCs were cultured in defined medium with graded doses of FSH. In the absence of FSH, COCs did not expand. FSH caused cumulus expansion, and increased the abundance of AREG and EREG mRNA in a time- and dose-dependent manner, but decreased BTC mRNA levels. FSH had modest stimulatory effects on the levels of mRNA encoding the bone morphogenetic protein 15 (BMP15) receptor, BMPR1B, in cumulus cells, but did not alter mRNA expression of the growth and differentiation factor 9 (GDF9) receptor, TGFBR1. More interestingly, FSH dramatically stimulated levels of mRNA encoding two receptors for fibroblast growth factors (FGF), FGFR2C and FGFR3C, in cumulus cells. FSH also stimulated mRNA expression of FGFR1B, but not of FGFR2B in cumulus cells. Based on dose-response studies, FGFR3C was the receptor most sensitive to the influence of FSH. This study demonstrates that FSH stimulates the expression of EGF-like factors in bovine cumulus cells, and provides evidence that FSH differently regulates the expression of distinct receptors for OSFs in cumulus cells.

Additional keywords: cumulus expansion, EGF-like ligands.


References

Ashkenazi, H., Cao, X., Motola, S., Popliker, M., Conti, M., and Tsafriri, A. (2005). Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146, 77–84.
Epidermal growth factor family members: endogenous mediators of the ovulatory response.CrossRef | 1:CAS:528:DC%2BD2cXhtFGmt7jP&md5=a87fe4322f1300baf2981d5c7904eb44CAS | 15459120PubMed |

Assidi, M., Dieleman, S. J., and Sirard, M. A. (2010). Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction 140, 835–852.
Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence.CrossRef | 1:CAS:528:DC%2BC3MXisFKqtb4%3D&md5=eaaa6123b57916ef82f58bb42781b067CAS | 20724459PubMed |

Buratini, J., Teixeira, A. B., Costa, I. B., Glapinski, V. F., Pinto, M. G. L., Giometti, I. C., Barros, C. M., Cao, M., Nicola, E. S., and Price, C. A. (2005). Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles. Reproduction 130, 343–350.
Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles.CrossRef | 1:CAS:528:DC%2BD2MXhtFWisr3I&md5=730c9612e5bcfbaca375959958cbd36bCAS | 16123241PubMed |

Buratini, J., Pinto, M. G., Castilho, A. C., Amorim, R. L., Giometti, I. C., Portela, V. M., Nicola, E. S., and Price, C. A. (2007). Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles. Biol. Reprod. 77, 743–750.
Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles.CrossRef | 1:CAS:528:DC%2BD2sXhtFahsb3F&md5=9f0b07e7adc4f768bb8669065c37afa6CAS | 17582010PubMed |

Chen, A. Q., Yu, S. D., Wang, G. Z., Xu, Z. R., and Yang, Z. G. (2009). Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: effects of follicle-stimulating hormone on ovine antral follicles. Anim. Reprod. Sci. 111, 391–399.
Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: effects of follicle-stimulating hormone on ovine antral follicles.CrossRef | 1:CAS:528:DC%2BD1MXhsFKmtL8%3D&md5=f754ca7d869adabbf489bca8e88e8a56CAS | 18462895PubMed |

Child, T. J., Phillips, S. J., Abdul-Jalil, A. K., Gulekli, B., and Tan, S. L. (2002). A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries. Obstet. Gynecol. 100, 665–670.
A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries.CrossRef | 12383531PubMed |

Cho, J. H., Itoh, T., Sendai, Y., and Hoshi, H. (2008). Fibroblast growth factor 7 stimulates in vitro growth of oocytes originating from bovine early antral follicles. Mol. Reprod. Dev. 75, 1736–1743.
Fibroblast growth factor 7 stimulates in vitro growth of oocytes originating from bovine early antral follicles.CrossRef | 1:CAS:528:DC%2BD1cXhtlyqsrzO&md5=75677a3f4f4249def94c17b54cae12f8CAS | 18386286PubMed |

Choi, Y. H., Carnevale, E. M., Seidel, G. E., and Squires, E. L. (2001). Effects of gonadotrophins on bovine oocytes matured in TCM-199. Theriogenology 56, 661–670.
Effects of gonadotrophins on bovine oocytes matured in TCM-199.CrossRef | 1:CAS:528:DC%2BD3MXntlahtrg%3D&md5=c4fa268e8f3811e195e10aef53a43004CAS | 11572446PubMed |

Conti, M., Hsieh, M., Park, J. Y., and Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–723.
Role of the epidermal growth factor network in ovarian follicles.CrossRef | 1:CAS:528:DC%2BD28Xkt1Oqu78%3D&md5=f36eac7c48afc829a0d6d51d90a3d6e2CAS | 16051667PubMed |

Downs, S. M., and Chen, J. (2008). EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 75, 105–114.
EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes.CrossRef | 17549700PubMed |

Dragovic, R. A., Ritter, L. J., Schulz, S. J., Amato, F., Armstrong, D. T., and Gilchrist, R. B. (2005). Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 146, 2798–2806.
Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion.CrossRef | 1:CAS:528:DC%2BD2MXkslehsrg%3D&md5=7ceec3dee2ae8fc9479d6dc0f0668b98CAS | 15761035PubMed |

Elvin, J. A., Clark, A. T., Wang, P., Wolfman, N. M., and Matzuk, M. M. (1999). Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13, 1035–1048.
Paracrine actions of growth differentiation factor-9 in the mammalian ovary.CrossRef | 1:CAS:528:DyaK1MXjs1yns7c%3D&md5=d6b4e44ca53e2b7426ba8b13a0ab8419CAS | 10379900PubMed |

Fair, T., Carter, F., Park, S., Evans, A. C. O., and Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68, S91–S97.
Global gene expression analysis during bovine oocyte in vitro maturation.CrossRef | 1:CAS:528:DC%2BD2sXotlaiu74%3D&md5=1580c7e440a2ad9ee8cbb49932b2b9dbCAS | 17512044PubMed |

Fatehi, A. N., van den Hurk, R., Colenbrander, B., Daemen, A. J. J. M., van Tol, H. T. A., Monteiro, R. M., Roelen, B. A. J., and Bevers, M. M. (2005). Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–889.
Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development.CrossRef | 1:CAS:528:DC%2BD2MXjsVWr&md5=f07ae6f278b69c10125be64deb9c4d55CAS | 15629804PubMed |

Fru, K. N., Cherian-Shaw, M., Puttabyatappa, M., VandeVoort, C. A., and Chaffin, C. L. (2007). Regulation of granulosa cell proliferation and EGF-like ligands during the periovulatory interval in monkeys. Hum. Reprod. 22, 1247–1252.
Regulation of granulosa cell proliferation and EGF-like ligands during the periovulatory interval in monkeys.CrossRef | 1:CAS:528:DC%2BD2sXntlWmsrg%3D&md5=7ec7cfc30d07097987af719ff6b0d0d5CAS | 17293344PubMed |

Gilchrist, R. B., and Thompson, J. G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.
Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro.CrossRef | 17092551PubMed |

Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.CrossRef | 1:CAS:528:DC%2BD1cXisVKmurY%3D&md5=ea2826a49264b29c9302c4d90b63358cCAS | 18175787PubMed |

Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–521.
Oocyte-secreted factors enhance oocyte developmental competence.CrossRef | 1:CAS:528:DC%2BD28XotV2gsb4%3D&md5=0f9b6f0fe43b776d7f08409072e0f775CAS | 16854407PubMed |

Hussein, T. S., Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2011). Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM. Reprod. Fertil. Dev. 23, 576–584.
Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM.CrossRef | 1:CAS:528:DC%2BC3MXlsFKnsLw%3D&md5=5b6dd71548ece3251423d7edcec3abbcCAS | 21557924PubMed |

Itoh, N., and Ornitz, D. M. (2004). Evolution of the FGF and FGFR gene families. Trends Genet. 20, 563–569.
Evolution of the FGF and FGFR gene families.CrossRef | 1:CAS:528:DC%2BD2cXotlajsLo%3D&md5=79c3fff1175e15ea97b197499c57793cCAS | 15475116PubMed |

Izadyar, F., Zeinstra, E., and Bevers, M. M. (1998). Follicle-stimulating hormone and growth hormone act differently on nuclear maturation while both enhance developmental competence of in vitro-matured bovine oocytes. Mol. Reprod. Dev. 51, 339–345.
Follicle-stimulating hormone and growth hormone act differently on nuclear maturation while both enhance developmental competence of in vitro-matured bovine oocytes.CrossRef | 1:CAS:528:DyaK1cXmtlShtLc%3D&md5=44cf8cd1e4d6e700abb09df9fc9916d2CAS | 9771655PubMed |

Jayawardana, B. C., Shimizu, T., Nishimoto, H., Kaneko, E., Tetsuka, M., and Miyamoto, A. (2006). Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle. Reproduction 131, 545–553.
Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle.CrossRef | 1:CAS:528:DC%2BD28Xjs12jsLg%3D&md5=14e0bb26aeaea9214cda4611c267996cCAS | 16514197PubMed |

Kyasari, O. R., Valojerdi, M. R., Farrokhi, A., and Ebrahimi, B. (2012). Expression of maturation genes and their receptors during in vitro maturation of sheep COCs in the presence and absence of somatic cells of cumulus origin. Theriogenology 77, 12–20.
Expression of maturation genes and their receptors during in vitro maturation of sheep COCs in the presence and absence of somatic cells of cumulus origin.CrossRef | 1:CAS:528:DC%2BC3MXhsF2rt7rI&md5=4a327e187475246858f1381dfb2ed51bCAS | 21855989PubMed |

Lequarre, A. S., Traverso, J. M., Marchandise, J., and Donnay, I. (2004). Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors1. Biol. Reprod. 71, 425–431.
Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors1.CrossRef | 1:CAS:528:DC%2BD2cXmtFWgtLo%3D&md5=2970441176f26e58506e688eca708181CAS | 15056564PubMed |

Leyens, G., Verhaeghe, B., Landtmeters, M., Marchandise, J., Knoops, B., and Donnay, I. (2004). Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication. Biol. Reprod. 71, 1646–1651.
Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication.CrossRef | 1:CAS:528:DC%2BD2cXpt1yitr8%3D&md5=af51df45ff19ffeb410ec51a205f8c66CAS | 15240427PubMed |

Li, H. K., Kuo, T. Y., Yang, H. S., Chen, L. R., Li, S. S. L., and Huang, H. W. (2008). Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim. Reprod. Sci. 103, 312–322.
Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos.CrossRef | 1:CAS:528:DC%2BD2sXhsVSmtb7O&md5=b0116c08f18c18d47415ef3ac655c66aCAS | 17222994PubMed |

Lonergan, P., Gutiérrez-Adán, A., Rizos, D., Pintado, B., de la Fuente, J., and Boland, M. P. (2003). Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297–305.
Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge.CrossRef | 1:CAS:528:DC%2BD3sXotFOgtrY%3D&md5=5a5fa6eb9762f5d61d5c9d604036a29dCAS | 14502609PubMed |

Machado, M. F., Portela, V. M., Price, C. A., Costa, I. B., Ripamonte, P., Amorim, R. L., and Buratini, J. (2009). Regulation and action of fibroblast growth factor 17 in bovine follicles. J. Endocrinol. 202, 347–353.
Regulation and action of fibroblast growth factor 17 in bovine follicles.CrossRef | 1:CAS:528:DC%2BD1MXhtFahtLnN&md5=18af7f29f58392a4d4d51cd261c3839bCAS | 19535432PubMed |

Mazerbourg, S., Klein, C., Roh, J., Kaivo-Oja, N., Mottershead, D. G., Korchynskyi, O., Ritvos, O., and Hsueh, A. J. (2004). Growth differentiation factor-9 (GDF-9) signalling is mediated by the type I receptor, activin receptor-like kinase 5. Mol. Endocrinol. 18, 653–665.
Growth differentiation factor-9 (GDF-9) signalling is mediated by the type I receptor, activin receptor-like kinase 5.CrossRef | 1:CAS:528:DC%2BD2cXivFCqtrs%3D&md5=a6bf9340177ca8c018ab2978276fff3eCAS | 14684852PubMed |

Miyoshi, T., Otsuka, F., Inagaki, K., Otani, H., Takeda, M., Suzuki, J., Goto, J., Ogura, T., and Makino, H. (2007). Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly-regulated kinase signalling and oocyte actions in follicle-stimulating hormone-induced oestrogen production. Endocrinology 148, 337–345.
Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly-regulated kinase signalling and oocyte actions in follicle-stimulating hormone-induced oestrogen production.CrossRef | 1:CAS:528:DC%2BD2sXjsFSisQ%3D%3D&md5=2bc4e116fab2a2c4e5eeb014a8d315c9CAS | 17008391PubMed |

Moore, R. K., Otsuka, F., and Shimasaki, S. (2003). Molecular basis of bone morphogenetic protein-15 signalling in granulosa cells. J. Biol. Chem. 278, 304–310.
Molecular basis of bone morphogenetic protein-15 signalling in granulosa cells.CrossRef | 1:CAS:528:DC%2BD38XpvVWgtLc%3D&md5=b0b27d8b4559b942e3bb7faa781ab1b9CAS | 12419820PubMed |

Nakamura, E., Otsuka, F., Inagaki, K., Miyoshi, T., Yamanaka, R., Tsukamoto, N., Suzuki, J., Ogura, T., and Makino, H. (2010). A novel antagonistic effect of the bone morphogenetic protein system on prolactin actions in regulating steroidogenesis by granulosa cells. Endocrinology 151, 5506–5518.
A novel antagonistic effect of the bone morphogenetic protein system on prolactin actions in regulating steroidogenesis by granulosa cells.CrossRef | 1:CAS:528:DC%2BC3cXhsVKks7fI&md5=c9107e501241c67c83da06c3377bdf60CAS | 20810564PubMed |

Park, J. Y., Su, Y. Q., Ariga, M., Law, E., Jin, S. L., and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
EGF-like growth factors as mediators of LH action in the ovulatory follicle.CrossRef | 1:CAS:528:DC%2BD2cXmvVKlsg%3D%3D&md5=3cd08e1d965fb2c5268ba622152e142dCAS | 14726596PubMed |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
A new mathematical model for relative quantification in real-time RT-PCR.CrossRef | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=54b36b3c1054987092ad32dfe1b8f6acCAS | 11328886PubMed |

Portela, V. M., Zamberlam, G., Gonçalves, P. B. D., de Oliveira, J. F. C., and 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, 1167–1174.
Role of angiotensin II in the periovulatory epidermal growth factor-like cascade in bovine granulosa cells in vitro.CrossRef | 1:CAS:528:DC%2BC3MXhs1ShsLbJ&md5=a6b6fce80dc54bf75095ce127c8dd9e5CAS | 21849708PubMed |

Procházka, R., Petlach, M., Nagyová, E., and Nemcová, L. (2011). Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation and acquisition of developmental competence in vitro: comparison with gonadotrophins. Reproduction 141, 425–435.
Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation and acquisition of developmental competence in vitro: comparison with gonadotrophins.CrossRef | 21239527PubMed |

Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.CrossRef | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=e52aa9c386e7ff8008cfd9fb23cf2240CAS | 12618301PubMed |

Richards, J. S., Russell, D. L., Ochsner, S., and Espey, L. L. (2002). Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu. Rev. Physiol. 64, 69–92.
Ovulation: new dimensions and new regulators of the inflammatory-like response.CrossRef | 1:CAS:528:DC%2BD38XisFGms7Y%3D&md5=18578d3dcb76c7e5588bc3f75997575bCAS | 11826264PubMed |

Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.CrossRef | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=7e1cd9cffb7fc878404e93f2e0a29d94CAS | 11803560PubMed |

Sánchez, F., Adriaenssens, T., Romero, S., and Smitz, J. (2009). Quantification of oocyte-specific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro. Mol. Hum. Reprod. 15, 539–550.
Quantification of oocyte-specific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro.CrossRef | 19553355PubMed |

Su, Y. Q., Sugiura, K., Woo, Y., Wigglesworth, K., Kamdar, S., Affourtit, J., and Eppig, J. J. (2007). Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev. Biol. 302, 104–117.
Selective degradation of transcripts during meiotic maturation of mouse oocytes.CrossRef | 1:CAS:528:DC%2BD2sXntlOmsg%3D%3D&md5=82e1936aa0e7a4b83ef53097e1cb8875CAS | 17022963PubMed |

Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S. A., Sharma, S., Wigglesworth, K., O’Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells.CrossRef | 1:CAS:528:DC%2BD2sXpsFeju7k%3D&md5=24f7116ae5af6058d9b0e2c62c72fe7dCAS | 17553902PubMed |

Sutton-McDowall, M. E., Gilchrist, R. B., and Thompson, J. G. (2004). Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone.CrossRef | 1:CAS:528:DC%2BD2cXot1KitLk%3D&md5=cca0c749897e2e1e952e0bc3b98bcf73CAS |

Thibier, M. (2006). Transfers of both in vivo-derived and in vitro-produced embryos in cattle still on the rise and contrasted trends in other species in 2005. International Embryo Transfer Society Newsletter 24, 12–18.

Thompson, J. G., Gardner, D. K., Pugh, P. A., McMillan, W. H., and Tervit, H. R. (1995). Lamb birth-weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol. Reprod. 53, 1385–1391.
Lamb birth-weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos.CrossRef | 1:CAS:528:DyaK2MXpsVeisrs%3D&md5=5df20bf7e34820ebe5fb7f2535dd52d7CAS | 8562695PubMed |

Valve, E., Penttila, T. L., Paranko, J., and Härkönen, P. (1997). FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem. Biophys. Res. Commun. 232, 173–177.
FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development.CrossRef | 1:CAS:528:DyaK2sXhvVyltLs%3D&md5=426ebb12cee966b8d2f9bb5f54b2ffa4CAS | 9125125PubMed |

Vandesompele, J., Preter, K. D., Pattyn, F., Poppe, B., Roy, N. V., Paepe, A. D., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034–research0034.11.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef | 12184808PubMed |

Vanhoutte, L., Nogueira, D., Dumortier, F., and De Sutter, P. (2009). Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor. Hum. Reprod. 24, 1946–1959.
Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor.CrossRef | 1:CAS:528:DC%2BD1MXptVartLg%3D&md5=2ae3e1552ad21ca3b9848aeb5ddfccb3CAS | 19395363PubMed |

Yeo, C. X., Gilchrist, R. B., Thompson, J. G., and Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 67–73.
Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice.CrossRef | 1:CAS:528:DC%2BD2sXhsVWgsbzF&md5=c169a6fa48f54726380fc3324c35c050CAS | 17933754PubMed |

Yoshino, O., McMahon, H. E., Sharma, S., and Shimasaki, S. (2006). A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc. Natl. Acad. Sci. USA 103, 10 678–10 683.
A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse.CrossRef | 1:CAS:528:DC%2BD28XntFWmsL0%3D&md5=157cddfb3e3ae2e14ed4643ecb905098CAS |

Zhang, X., Ibrahimi, O. A., Olsen, S. K., Umemori, H., Mohammadi, M., and Ornitz, D. M. (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15 694–15 700.
Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family.CrossRef | 1:CAS:528:DC%2BD28Xlt1Cktrc%3D&md5=490b667006140f3d66b65e190b96e54dCAS |

Zhang, D. X., Cui, X. S., and Kim, N. H. (2009). Involvement of polyadenylation status on maternal gene expression during in vitro maturation of porcine oocytes. Mol. Reprod. Dev. 76, 881–889.
Involvement of polyadenylation status on maternal gene expression during in vitro maturation of porcine oocytes.CrossRef | 1:CAS:528:DC%2BD1MXptlehtL0%3D&md5=7752c4ddbbc8db952809a77644bd6eaaCAS | 19479986PubMed |

Zhang, K., Hansen, P. J., and Ealy, A. D. (2010a). Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro. Reproduction 140, 815–826.
Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro.CrossRef | 1:CAS:528:DC%2BC3MXisFKqtLY%3D&md5=df5b63c4dd620a87c20007e4b8a01b15CAS | 20876224PubMed |

Zhang, M., Su, Y. Q., Sugiura, K., Xia, G., and Eppig, J. J. (2010b). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–369.
Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.CrossRef | 1:CAS:528:DC%2BC3cXht1OisL7P&md5=f866b33d87d62442a6349fed2d92ae49CAS | 20947764PubMed |

Zhang, K., and Ealy, A. D. (). Disruption of fibroblast growth factor receptor signalling in bovine cumulus–oocyte complexes during in vitro maturation reduces subsequent embryonic development. Domest. Anim. Endocrinol. , .
Disruption of fibroblast growth factor receptor signalling in bovine cumulus–oocyte complexes during in vitro maturation reduces subsequent embryonic development.CrossRef |

Zhong, W., Wang, Q. T., Sun, T., Wang, F., Liu, J., Leach, R., Johnson, A., Puscheck, E. E., and Rappolee, D. A. (2006). FGF ligand family mRNA expression profile for mouse preimplantation embryos, early gestation human placenta and mouse trophoblast stem cells. Mol. Reprod. Dev. 73, 540–550.
FGF ligand family mRNA expression profile for mouse preimplantation embryos, early gestation human placenta and mouse trophoblast stem cells.CrossRef | 1:CAS:528:DC%2BD28Xjt1Kit7k%3D&md5=6d948506fa3385fc108d8701304b0419CAS | 16470835PubMed |

Zhu, G., Guo, B., Pan, D., Mu, Y., and Feng, S. (2008). Expression of bone morphogenetic proteins and receptors in porcine cumulus–oocyte complexes during in vitro maturation. Anim. Reprod. Sci. 104, 275–283.
Expression of bone morphogenetic proteins and receptors in porcine cumulus–oocyte complexes during in vitro maturation.CrossRef | 1:CAS:528:DC%2BD1cXhsVOmsb8%3D&md5=423e3a27a07ff8e161dded0a55ca090fCAS | 17368971PubMed |



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