Dose and administration protocol for FSH used for ovarian stimulation affect gene expression in sheep cumulus–oocyte complexes
Gláucia M. Bragança A D , Ribrio Ivan T. P. Batista A , Joanna Maria G. Souza-Fabjan A , Vivian A. P. Alfradique A , Eduardo K. N. Arashiro A , Isabel O. Cosentino A , Pedro Henrique N. Pinto A , Luiz Sérgio A. Camargo B , Jeferson F. da Fonseca C and Felipe Z. Brandão A
+ Author Affiliations
- Author Affiliations
A Faculdade de Veterinária, Universidade Federal Fluminense, Rua Vital Brazil, 64, CEP 24320-340, Niteroi, RJ, Brazil.
B Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa de Gado de Leite, Rua Eugênio do Nascimento, 610, CEP 36038-330, Juiz de Fora, MG, Brazil.
C Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa em Caprinos e Ovinos, Campo Experimental de Coronel Pacheco. Rodovia MG 133, km 42, CEP 36155-000, Coronel Pacheco, MG, Brazil.
D Corresponding author. Email: glauciaveterinaria@yahoo.com.br
Reproduction, Fertility and Development 30(9) 1234-1244 https://doi.org/10.1071/RD17337
Submitted: 26 August 2017 Accepted: 27 February 2018 Published: 27 March 2018
Abstract
The present study evaluated the effect of four ovarian stimulation protocols on the follicular population and molecular status of cumulus–oocyte complexes (COCs). Twelve Santa Inês ewes (in a cross-over design) received 80 or 120 mg FSH alone in a multiple-dose (MD80 and MD120) regimen or in combination with 300 IU equine chorionic gonadotrophin (eCG) in a one-shot (OS80 and OS120) protocol. The follicular population, COC recovery rate, mean COCs per ewe and the rate of brilliant Cresyl blue-positive (BCB+) COCs were similar among treatments (P > 0.05). The expression of markers of oocyte competence (ZAR1, zygote arrest 1; MATER, maternal antigen that embryo requires; GDF9, growth differentiation factor 9; BMP15, bone morphogenetic protein 15; Bcl-2, B-cell lymphoma 2; BAX, Bcl-2 associated X protein) and the steroidogenic pathway (ERα, oestrogen receptor α; LHr, LH receptor; FSHr, FSH receptor; STAR, steroidogenic acute regulatory protein) was affected by stimulation. Specifically, the expression of markers of the steroidogenic pathway was reduced with increasing FSH dose in the OS protocol. FSH at a dose of 80 mg reduced the expression of FSHr and ERα in the OS versus MD protocol. Conversely, in MD protocol, only LHr was affected by increasing FSH dose. In conclusion, 80 mg FSH in the MD or OS protocol was sufficient to promote the development of multiple follicles and obtain fully grown (BCB+) oocytes. The MD protocol may be more appropriate for the production of better-quality oocytes.
Additional keywords: brilliant Cresyl blue, ewe, molecular biology, oocyte, superstimulation.
References
Adams, G. P., Matteri, R. L., Kastelic, J. P., Ko, J. C., and Ginther, O. J. (1992). Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers. J. Reprod. Fertil. 94, 177–188.| Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhs1Kltr4%3D&md5=37ae68699abad5413e5a26da52ab1571CAS |
Almeida, K. C., Pereira, A. F., Alcântara Neto, A. S., Avelar, S. R. G., Bertolini, L. R., Bertolini, M., Freitas, V. J. F., and Melo, L. M. (2011). Real-time qRT-PCR analysis of EGF receptor in cumulus–oocyte complexes recovered by laparoscopy in hormonally treated goats. Zygote 19, 127–136.
| Real-time qRT-PCR analysis of EGF receptor in cumulus–oocyte complexes recovered by laparoscopy in hormonally treated goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFegsb8%3D&md5=9227f03ee8c2e7dbefbe15d20c8d8dafCAS |
Armstrong, D. T., Irvine, B. J., Earl, C. R., McLean, D., and Seamark, R. F. (1994). Gonadotropin stimulation regimens for follicular aspiration and in vitro embryo production from calf oocytes. Theriogenology 42, 1227–1236.
| Gonadotropin stimulation regimens for follicular aspiration and in vitro embryo production from calf oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1Giu7c%3D&md5=bd2ea96de41a9ce8b923208d1f3a1241CAS |
Avelar, S. R. G., Moura, R. R., Sousa, F. C., Pereira, A. F., Almeida, K. C., Melo, C. H. S., Teles-Filho, A. C. A., Baril, G., Melo, L. M., Teixeira, D. I. A., and Freitas, V. J. F. (2012). Oocyte production and in vitro maturation in Canindé goats following hormonal ovarian stimulation. Anim. Reprod. 9, 27–32.
Balaro, M. F. A., Fonseca, J. F., Barbosa, T. G. B., Souza-Fabjan, J. M. G., Figueira, L. M., Teixeira, T. A., Carvalheira, L. R., and Brandão, F. Z. (2016). Potential role for GnRH in the synchronization of follicular emergence before the superovulatory Day 0 protocol. Domest. Anim. Endocrinol. 54, 10–14.
| Potential role for GnRH in the synchronization of follicular emergence before the superovulatory Day 0 protocol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlGgtb7P&md5=e3b5aa391f58a6133265136d4d19aea1CAS |
Baldassarre, H. (2012). Practical aspects for implementing in vitro embryo production and cloning programs in sheep and goats. Anim. Reprod. 9, 188–194.
Baldassarre, H., Furnus, C. C., de Matos, D. G., and Pessi, H. (1996). In vitro production of sheep embryos using laparoscopic folliculocentesis: alternative gonadotrophin treatments for stimulation of oocyte donors. Theriogenology 45, 707–717.
| In vitro production of sheep embryos using laparoscopic folliculocentesis: alternative gonadotrophin treatments for stimulation of oocyte donors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisV2qs7s%3D&md5=8d531cadece7119cdb21d2006397e456CAS |
Baldassarre, H., Wang, B., Kafidi, N., Keefer, C., Lazaris, A., and Karatzas, C. N. (2002). Advances in the production and propagation of transgenic goats using laparoscopic ovum pick-up and in vitro embryo production technologies. Theriogenology 57, 275–284.
| Advances in the production and propagation of transgenic goats using laparoscopic ovum pick-up and in vitro embryo production technologies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fksl2ltg%3D%3D&md5=c9af22ab6ffc0a3684f13eab9b976740CAS |
Baldassarre, H., Keefer, C., Wang, B., Lazaris, A., and Kartazas, C. N. (2003). Nuclear transfer in goats using in vitro matured oocytes recovered by laparoscopic ovum pick-up. Cloning Stem Cells 5, 279–285.
| Nuclear transfer in goats using in vitro matured oocytes recovered by laparoscopic ovum pick-up.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislaqug%3D%3D&md5=b30cf06af21800d7d7f5c60833af01bbCAS |
Batista, R. I., Raposo, N. R., Campos-Junior, P. H., Pereira, M. M., Camargo, L. S., Carvalho, B. C., Gama, M. A., and Viana, J. H. (2014). Trans-10,cis-12 conjugated linoleic acid reduces neutral lipid content and may affect cryotolerance of in vitro-produced crossbred bovine embryos. J. Anim. Sci. Biotechnol. 5, 33.
| Trans-10,cis-12 conjugated linoleic acid reduces neutral lipid content and may affect cryotolerance of in vitro-produced crossbred bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G. G., Tore, S., Succu, S., Berlinguer, F., Naitana, S., and Ledda, S. (2008). Expression pattern of zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos. Reprod. Fertil. Dev. 20, 908–915.
| Expression pattern of zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Oks77K&md5=d67b889b419cc1f4360474c2b1793de6CAS |
Berlinguer, F., Leoni, G., Bogliolo, L., Pintus, P. P., Rosati, I., Ledda, S., and Naitana, S. (2004). FSH different regimes affect the developmental capacity and cryotolerance of embryos derived from oocytes collected by ovum pick-up in donor sheep. Theriogenology 61, 1477–1486.
| FSH different regimes affect the developmental capacity and cryotolerance of embryos derived from oocytes collected by ovum pick-up in donor sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVOlsrw%3D&md5=28973eeddea5bc96db6efaf6a12dcc78CAS |
Blondin, P., Bousquet, D., Herménégilde, T., Barnes, F., and Sirard, M. A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
| Manipulation of follicular development to produce developmentally competent bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1ylsA%3D%3D&md5=ae700fe746440a5f43269348ade8a0a0CAS |
Catalá, M. G., Izquierdo, D., Uzbekova, S., Marató, R., Roura, M., Romanguera, R., Papillier, P., and Paramio, T. (2011). Brilliant cresyl blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction 142, 517–527.
| Brilliant cresyl blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep.Crossref | GoogleScholarGoogle Scholar |
Chakravarthi, V. P., Kona, S. S., Siva Kumar, A. V., Bhaskar, M., and Rao, V. H. (2015). Quantitative expression of antiapoptotic and proapoptotic genes in sheep ovarian follicles grown in vivo or cultured in vitro. Theriogenology 83, 590–595.
| Quantitative expression of antiapoptotic and proapoptotic genes in sheep ovarian follicles grown in vivo or cultured in vitro.Crossref | GoogleScholarGoogle Scholar |
Couse, J. F., and Korach, K. S. (1999). Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20, 358–417.
| Estrogen receptor null mice: what have we learned and where will they lead us?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktVaqtLk%3D&md5=ac3c848d1093f5c74d4bf97131ebe9fcCAS |
Dias, F. C. F., Khan, M. I. R., Sirard, M. A., Adams, G. P., and Singh, J. (2013). Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reproduction 146, 181–191.
| Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlSnsb%2FM&md5=ac0d827d305105a8fe0a8c58b8d9a839CAS |
Dias, F. C. F., Khan, M. I. R., Sirard, M. A., Adams, G. P., and Singh, J. (2014). Granulosa cell function and oocyte competence: super-follicles, supper-moms and super-stimulation in cattle. Anim. Reprod. Sci. 149, 80–89.
| Granulosa cell function and oocyte competence: super-follicles, supper-moms and super-stimulation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2Fgt1Kitw%3D%3D&md5=c0250b754fb0b4bbc7febff90815c0bbCAS |
Gibbons, A., Pereyra Bonnet, F., Cueto, M., Catalá, M., Salamone, D., and González-Bulnes, A. (2007). Procedure for maximizing oocyte harvest for in vitro embryo production in small ruminants. Reprod. Domest. Anim. 42, 423–426.
| Procedure for maximizing oocyte harvest for in vitro embryo production in small ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlKns7g%3D&md5=ba7cfe222ebe1fdfec338b07b5b84a11CAS |
Hillier, S. G., Whitelaw, P. F., and Smyth, C. D. (1994). Follicular oestrogen synthesis: the ‘two-cell, two-gonadotrophin’ model revisited. Mol. Cell. Endocrinol. 100, 51–54.
| Follicular oestrogen synthesis: the ‘two-cell, two-gonadotrophin’ model revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVWisLk%3D&md5=89ec29a462ceb6b562f69ab4113cc93dCAS |
Hogg, K., McNeilly, A. S., and Duncan, W. C. (2011). Prenatal androgen exposure leads to alterations in gene and protein expression in the ovine fetal ovary. Endocrinology 152, 2048–2059.
| Prenatal androgen exposure leads to alterations in gene and protein expression in the ovine fetal ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVOjsrY%3D&md5=daf75c21fc1a8c12a18201e33e7d136dCAS |
Khan, D. R., Guillemette, C., Sirard, M. A., and Richard, F. J. (2015). Characterization of FSH signaling networks in bovine cumulus cells: a perspective on oocyte competence acquisition. Mol. Hum. Reprod. 21, 688–701.
| Characterization of FSH signaling networks in bovine cumulus cells: a perspective on oocyte competence acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsVGgsbzI&md5=336f4b08c98a0575297156ec1d5df2a0CAS |
Kona, S. S. R., Chakravarthi, V. P., Kumar, A. V. N. S., Srividya, D., Padmaja, K., and Rao, V. H. (2016). Quantitative expression patterns of GDF9 and BMP15 genes in sheep ovarian follicles grown in vivo or cultured in vitro. Theriogenology 85, 315–322.
| Quantitative expression patterns of GDF9 and BMP15 genes in sheep ovarian follicles grown in vivo or cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsF2gtr7O&md5=887c31bf34ca7d7a7102577800edb4f9CAS |
Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.
| The effect of oocyte quality on development.Crossref | GoogleScholarGoogle Scholar |
Lahoz, B., Alabart, J. L., Folch, J., Sànchez, P. S., Echegoyen, E., and Cocero, M. J. (2013). Influence of the FecXR allele in heterozygous ewes on follicular population and outcomes of IVP and ET using LOPU-derived oocytes. Reprod. Domest. Anim. 48, 717–723.
| Influence of the FecXR allele in heterozygous ewes on follicular population and outcomes of IVP and ET using LOPU-derived oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOgs7vM&md5=370ca04f8e6594d22ca499db1f1c7028CAS |
Lambrecque, R., Vigneault, C., Blondin, P., and Sirard, M. A. (2013). Gene expression analysis of bovine oocytes with high developmental competence obtainedfrom FSH-stimulated animals. Mol. Reprod. Dev. 80, 428–440.
| Gene expression analysis of bovine oocytes with high developmental competence obtainedfrom FSH-stimulated animals.Crossref | GoogleScholarGoogle Scholar |
Laster, D. B. (1972). Disappearance and uptake of [125I]FSH in the rat, rabbit, ewe and cow. J. Reprod. Fertil. 30, 407–415.
| Disappearance and uptake of [125I]FSH in the rat, rabbit, ewe and cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXhtFOrtw%3D%3D&md5=2a79e552cbac5c66cbe0217eb01ca130CAS |
Nivet, A. L., Bunel, A., Labrecque, R., Belanger, J., Vigneault, C., Blondin, P., and Sirard, M. A. (2012). FSH withdrawal improves developmental competence of oocytes in the bovine model. Reproduction 143, 165–171.
| FSH withdrawal improves developmental competence of oocytes in the bovine model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Kkt70%3D&md5=dea30204b832e7b409fc2bcf42b8cbccCAS |
Orozco-Lucero, E., and Sirard, M. A. (2014). Molecular markers of fertility in cattle oocytes and embryos: progress and challenges. Anim. Reprod. 11, 183–194.
Otsuka, F., Yamamoto, S., Erickson, G. F., and Shimasaki, S. (2001). Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH. J. Biol. Chem. 276, 11387–11392.
| Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGjt74%3D&md5=0d16bfac28238a7c372529623220ed08CAS |
Otsuka, F., Moore, R. K., Wang, X., Sharma, S., Miyoski, T., and Shimasaki, S. (2005). Essential role of the oocyte in estrogen amplification of follicle-stimulating hormone signaling in granulosa cells. Endocrinology 146, 3362–3367.
| Essential role of the oocyte in estrogen amplification of follicle-stimulating hormone signaling in granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVaitb0%3D&md5=a65cfdac0ffbe74c28a84a04444d7f22CAS |
Paramio, M. T., and Izquierdo, D. (2016). Recent advances in in vitro embryo production in small ruminants. Theriogenology 86, 152–159.
| Recent advances in in vitro embryo production in small ruminants.Crossref | GoogleScholarGoogle Scholar |
Pfaffl, M. W., Horgan, G. M., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
| Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar |
Pierson, J., Wang, B., Neveu, N., Sneek, L., Côté, F., Karatzas, N. C., and Baldassarre, H. (2004). Effects of repetition, interval between treatments and season on the results from laparoscopic ovum pick up in goats. Reprod. Fertil. Dev. 16, 795–799.
| Effects of repetition, interval between treatments and season on the results from laparoscopic ovum pick up in goats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7htFCmug%3D%3D&md5=d52aed471af8661a7579e31494ef4574CAS |
Pinto, P. H. N., Bragança, G. M., Balaro, M. F. A., Arashiro, E. K. N., Santos, G. B., Souza, G. N., Souza-Fabjan, J. M. G., Fonseca, J. F., and Brandão, F. Z. (2018). Colour-Doppler ultrasound imaging lutea in superovulated sheep. Reprod. Domest. Anim. , .
| Colour-Doppler ultrasound imaging lutea in superovulated sheep.Crossref | GoogleScholarGoogle Scholar |
Ramakers, C., Ruijter, J. M., Deprez, R. H. L., and Moorman, A. F. M. (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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=9eebf6befe2f42792657bfcc80921beaCAS |
Santos, J. D. R., Batista, R. I. T. P., Magalhães, L. C., Paula, A. R., Souza, S. S., Salamone, D. F., Bhat, M. H., Teixeira, D. I. A., Freitas, V. J. F., and Melo, L. M. (2016). Overexpression of hyaluronan synthase 2 and gonadotropin receptors in cumulus cells of goats subjected to one-shot eCG/FSH hormonal treatment for ovarian stimulation. Anim. Reprod. Sci. , .
| Overexpression of hyaluronan synthase 2 and gonadotropin receptors in cumulus cells of goats subjected to one-shot eCG/FSH hormonal treatment for ovarian stimulation.Crossref | GoogleScholarGoogle Scholar |
Shabankareh, H. K., Azimi, G., and Torki, M. (2014). Development competence of bovine oocytes selected based on follicle size and using the brilliant cresyl blue (BCB) test. Iran. J. Reprod. Med. 12, 771–778.
Shimasaki, S., Moore, R. K., Otsuka, F., and Erickson, G. F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72–101.
| The bone morphogenetic protein system in mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFOmt78%3D&md5=b95440997be7b1b41645b3223594c0a0CAS |
Sirard, M. A. (2010). Activation of the embryonic genome. Soc. Reprod. Fertil. Suppl. 67, 145–158.
| 1:STN:280:DC%2BC3MnosFeguw%3D%3D&md5=351f384e8f167d545caaca64e39a35c7CAS |
Sousa, F. C., Melo, C. H. S., Teles Filho, A. C. A., Avelar, S. R. G., Moura, A. A. A., Martins, J. A. M., Freitas, V. J. F., and Teixeira, D. I. A. (2011). Ovarian follicular response to different hormonal stimulation treatments in Canindé goats. Anim. Reprod. Sci. 125, 88–93.
| Ovarian follicular response to different hormonal stimulation treatments in Canindé goats.Crossref | GoogleScholarGoogle Scholar |
Souza-Fabjan, J. M. G., Pereira, A. F., Melo, C. H. S., Sanchez, J. D., Oba, E., Mermillod, P., Melo, L. M., Teixeira, D. I. A., and Freitas, V. J. F. (2013). Assessment of the reproductive parameters, laparoscopic oocyte recovery and the first embryos produced in vitro from endangered Canindé goats (Capra hircus). Reprod. Biol. 13, 325–332.
| Assessment of the reproductive parameters, laparoscopic oocyte recovery and the first embryos produced in vitro from endangered Canindé goats (Capra hircus).Crossref | GoogleScholarGoogle Scholar |
Souza-Fabjan, J. M. G., Locatelli, Y., Duffard, N., Corbin, E., Touzé, J. L., Perreau, C., Beckers, J. F., Freitas, V. J., and Mermillod, P. (2014a). In vitro embryo production in goats: slaughterhouse and laparoscopic ovum pick up-derived oocytes have different kinetics and requirements regarding maturation media. Theriogenology 81, 1021–1031.
| In vitro embryo production in goats: slaughterhouse and laparoscopic ovum pick up-derived oocytes have different kinetics and requirements regarding maturation media.Crossref | GoogleScholarGoogle Scholar |
Souza-Fabjan, J. M. G., Locatelli, Y., Freitas, V. J. F., and Mermillod, P. (2014b). Laparoscopic ovum pick up (LOPU) in goats: from hormonal treatment to oocyte possible destinations. R. Bras. Ci. Vet. 21, 3–11.
| Laparoscopic ovum pick up (LOPU) in goats: from hormonal treatment to oocyte possible destinations.Crossref | GoogleScholarGoogle Scholar |
Souza-Fabjan, J. M. G., Locatelli, Y., Duffard, N., Corbin, E., Batista, R. I. T. B., Freitas, V. J. F., Beckers, J. F., and Mermillod, P. (2016). Intrinsic quality of goats oocytes already found denuded at collection for in vitro embryo production. Theriogenology 86, 1989–1998.
| Intrinsic quality of goats oocytes already found denuded at collection for in vitro embryo production.Crossref | GoogleScholarGoogle Scholar |
Teixeira, P. P. M., Padilha, L. C., Oliveira, M. E. F., Motheo, T. F., Silva, A. S. L., Barros, F. F. P. C., Coutinho, L. M., Flôre, N. F., Lopes, M. C. S., Bandarra, M. B., Silva, M. A. M., Vasconcelos, R. O., Rodrigues, L. F. S., and Vicente, W. R. R. (2011). Laparoscopic ovum collection in sheep: Gross and microscopic evaluation of the ovary and influence on oocyte production. Anim. Reprod. Sci. 127, 169–175.
| Laparoscopic ovum collection in sheep: Gross and microscopic evaluation of the ovary and influence on oocyte production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbgvFaktg%3D%3D&md5=f4bc247ff4705f023924ccb58104b0aaCAS |
Tisdall, D. J., Watanabe, K., Hudson, N. L., Smith, P., and McNatty, K. P. (1995). FSH receptor gene expression during ovarian follicle development in sheep. J. Mol. Endocrinol. 15, 273–281.
| FSH receptor gene expression during ovarian follicle development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVGjtb4%3D&md5=536e422c5a84b7c50cd87090c7191842CAS |
Turner, H., Ghanem, N., Ambros, C., Hölker, M., Tomek, W., Phatsara, C., Alm, H., Sirard, M.-A., Kanitz, W., Schellander, K., and Tesfaye, D. (2008). Focus on mammalian embryogenomics molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197–212.
| Focus on mammalian embryogenomics molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity.Crossref | GoogleScholarGoogle Scholar |
Urrego, R., Herrera-Puerta, E., Chavarria, N. A., Camargo, O., Wrenzycki, C., and Rodriguez-Osorio, N. (2015). Follicular progesterone concentrations and messenger RNA expression of MATER and OCT-4 in immature bovine oocytes as predictors of developmental competence. Theriogenology 83, 1179–1187.
| Follicular progesterone concentrations and messenger RNA expression of MATER and OCT-4 in immature bovine oocytes as predictors of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosFKguw%3D%3D&md5=fc4647643c9f7b3d94642a73d4dc08b6CAS |
Vigone, G., Merico, V., Redi, C. A., Mazzini, G., Garagna, S., and Zuccotti, M. (2015). FSH and LH receptors are differentially expressed in cumulus cells surrounding developmentally competent and incompetent mouse fully grown antral oocytes. Reprod. Fertil. Dev. 27, 497–503.
| FSH and LH receptors are differentially expressed in cumulus cells surrounding developmentally competent and incompetent mouse fully grown antral oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXksVSltrk%3D&md5=c5b81f77755537b1a0851372a00a8727CAS |
Vitt, U. A., Hayashi, M., Klein, C., and Hsueh, A. J. W. (2000). Growth differentiation factor-9 stimulates proliferation but suppress the follicle-stimulating hormone-induced differentiation of cultured granulosa cell from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370–377.
| Growth differentiation factor-9 stimulates proliferation but suppress the follicle-stimulating hormone-induced differentiation of cultured granulosa cell from small antral and preovulatory rat follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOqsA%3D%3D&md5=1bc295b60ff7e1550c55f19406c26f2fCAS |
Wei, S. C., Gong, Z. D., Zhao, H. W., Liang, H. Q., Lai, L. J., and Deng, Y. Y. (2016). Equine chorionic gonadotropin influence on sheep oocyte in vitro maturation, apoptosis, and follicle-stimulating hormone receptor and luteinizing hormone receptor expression. Genet. Mol. Res. 15, 1–13.
| Equine chorionic gonadotropin influence on sheep oocyte in vitro maturation, apoptosis, and follicle-stimulating hormone receptor and luteinizing hormone receptor expression.Crossref | GoogleScholarGoogle Scholar |
Wood, J. R., and Strauss, J. F. (2002). Multiple signal transduction pathway regulate ovarian steroidogenesis. Rev. Endocr. Metab. Disord. 3, 33–46.
| Multiple signal transduction pathway regulate ovarian steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvFGht7k%3D&md5=e291990cd5e6479df534ce07c2bc8f93CAS |
Yang, M., Hall, J., Fan, Z., Regouski, M., Meng, Q., Rutigliano, H. M., Stott, R., Rood, K. A., Panter, K. E., and Polejaeva, I. A. (2016). Oocytes from small and large follicles exhibit similar development competence following goat cloning despite their differences in meiotic and cytoplasmic. Theriogenology 86, 2302–2311.
| Oocytes from small and large follicles exhibit similar development competence following goat cloning despite their differences in meiotic and cytoplasmic.Crossref | GoogleScholarGoogle Scholar |
Yu, Y., Li, W., Han, Z., Luo, M., Chang, Z., and Tan, J. (2003). The effect of follicle-stimulating hormone on follicular development, granulosa cell apoptosis and steirodogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology 60, 1691–1704.
| The effect of follicle-stimulating hormone on follicular development, granulosa cell apoptosis and steirodogenesis and its mediation by insulin-like growth factor-I in the goat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot12jsL0%3D&md5=6b1d949bd94b89a8d56c80d671044d71CAS |
Zheng, X., Prince, C. A., Tremblay, Y., Lussier, J. G., and Carrière, P. D. (2008). Role of transforming growth factor-β1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cell. Reproduction 136, 447–457.
| Role of transforming growth factor-β1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSrtr%2FI&md5=a4da64ec83ddb1aa0bedeeef5446c067CAS |
Zörnig, M., Hueber, A., Baum, W., and Evan, G. (2001). Apoptosis regulators and their role in tumorigenesis. Biochim. Biophys. Acta 1551, F1–F37.
| Apoptosis regulators and their role in tumorigenesis.Crossref | GoogleScholarGoogle Scholar |
