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

Bovine oviductal and uterine fluid support in vitro embryo development

Meriem Hamdi A , Ricaurte Lopera-Vasquez A , Veronica Maillo A , Maria Jesus Sanchez-Calabuig A , Carolina Núnez A , Alfonso Gutierrez-Adan A and Dimitrios Rizos A B
+ Author Affiliations
- Author Affiliations

A Departamento de Reproduccion Animal, Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA), Ctra. de la Coruna KM 5.9 – 28040 Madrid, Spain.

B Corresponding author. Email: drizos@inia.es

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17286
Submitted: 21 July 2017  Accepted: 20 October 2017   Published online: 23 November 2017

Abstract

In order to mimic the maternal oviductal environment, we evaluated the effect of oviductal fluid (OF) and/or uterine fluid (UF) supplementation on in vitro embryo development and quality. In vitro-produced zygotes were cultured with 1.25% OF from Day 1 to Day 4 after insemination (OF group), 1.25% OF from Day 1 to Day 4 followed by 1.25% UF from Day 4 to Day 9 (OF+UF group) or 1.25% UF only from Day 4 to Day 9 (UF group). Control groups were cultured in the presence of synthetic oviduct fluid (SOF) supplemented with 3 mg mL−1 bovine serum albumin (BSA) or 5% fetal calf serum (FCS). Supplementation of the culture medium with OF and/or UF (both at 1.25%) supported embryo development (Day 9 blastocyst rate 28.2–30.6%). At 72 h after vitrification–warming, the survival of blastocysts from the OF and OF+UF groups was similar to that of blastocysts in the SOF+BSA group (61.0 ± 5.7% and 62.8 ± 6.4% vs 64.8 ± 6.4% respectively), but significantly higher than that of blastocysts from the SOF+FCS group (31.6 ± 4.9%; P < 0.001). Blastocysts from the OF group exhibited upregulation of epigenetic genes (i.e. DNA methyltransferase 3α (DNMT3A) and insulin-like growth factor 2 receptor (IGF2R)), compared with expression in the SOF+FCS group (P < 0.05). Whereas those from OF+UF and UF groups exhibited downregulation of oxidative stress genes compared to SOF+BSA and OF groups for glutathione peroxidase (GPX1) and to SOF+FCS, SOF+BSA and OF groups for chloride intracellular channel 1 (CLIC1) (P < 0.05). In addition, accumulation of reactive oxygen species was lower in blastocysts from the OF, OF+UF and UF groups. In conclusion, the use of low concentrations of OF and UF in in vitro serum-free culture supports embryo development, with OF providing a better control of embryo methylation, whereas UF may have antioxidant activity.

Additional keywords: culture medium, gene expression, in vitro fertilisation.


References

Aguilar, J., and Reyley, M. (2005). The uterine tubal fluid: secretion, composition and biological effects. Anim. Reprod. 2, 91–105.

Al-Gubory, K. H., and Garrel, C. (2012). Antioxidative signalling pathways regulate the level of reactive oxygen species at the endometrial–extraembryonic membranes interface during early pregnancy. Int. J. Biochem. Cell Biol. 44, 1511–1518.
Antioxidative signalling pathways regulate the level of reactive oxygen species at the endometrial–extraembryonic membranes interface during early pregnancy.CrossRef | 1:CAS:528:DC%2BC38XhtVeksLjO&md5=bc1257a8d47eeecd524a17064b6472e5CAS |

Auclair, G., Guibert, S., Bender, A., and Weber, M. (2014). Ontogeny of CpG island methylation and specificity of DNMT3 methyltransferases during embryonic development in the mouse. Genome Biol. 15, 545.
Ontogeny of CpG island methylation and specificity of DNMT3 methyltransferases during embryonic development in the mouse.CrossRef |

Averaimo, S., Milton, R. H., Duchen, M. R., and Mazzanti, M. (2010). Chloride intracellular channel 1 (CLIC1): sensor and effector during oxidative stress. FEBS Lett. 584, 2076–2084.
Chloride intracellular channel 1 (CLIC1): sensor and effector during oxidative stress.CrossRef | 1:CAS:528:DC%2BC3cXlvVaqsr8%3D&md5=5ddca385054bdfa66d1e3165b2d1ea05CAS |

Avilés, M., Gutiérrez-Adán, A., and Coy, P. (2010). Oviductal secretions: will they be key factors for the future ARTs? Mol. Hum. Reprod. 16, 896–906.
Oviductal secretions: will they be key factors for the future ARTs?CrossRef |

Balaban, R. S., Nemoto, S., and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483–495.
Mitochondria, oxidants, and aging.CrossRef | 1:CAS:528:DC%2BD2MXitVWnurg%3D&md5=63303f199bde0108d1555389dc19a1bbCAS |

Ballester, L., Romero-Aguirregomezcorta, J., Soriano-Úbeda, C., Matás, C., Romar, R., and Coy, P. (2014). Timing of oviductal fluid collection, steroid concentrations, and sperm preservation method affect porcine in vitro fertilization efficiency. Fertil. Steril. 102, 1762–1768.e1.
Timing of oviductal fluid collection, steroid concentrations, and sperm preservation method affect porcine in vitro fertilization efficiency.CrossRef | 1:CAS:528:DC%2BC2cXhs1SqurrM&md5=c6fe3adcc1f6970b928127cd0db70fd1CAS |

Barrera, A. D., Garcia, E. V., Hamdi, M., Sanchez-Calabuig, M. J., Lopez-Cardona, A. P., Balvis, N. F., Rizos, D., and Gutierrez-Adan, A. (2017). Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts. Reproduction 154, 1–12.
Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC2sXht1CqsL3L&md5=98a8b4e618f440585ad6992fd62db3d8CAS |

Batista, R. I. T. P., Moro, L. N., Corbin, E., Alminana, C., Souza-Fabjan, J. M. G., de Figueirêdo Freitas, V. J., and Mermillod, P. (2016). Combination of oviduct fluid and heparin to improve monospermic zygotes production during porcine in vitro fertilization. Theriogenology 86, 495–502.
Combination of oviduct fluid and heparin to improve monospermic zygotes production during porcine in vitro fertilization.CrossRef | 1:CAS:528:DC%2BC28XjtFChsbo%3D&md5=6cd788732e2d1c76449068cabbbabe0cCAS |

Bavister, B. D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update 1, 91–148.
Culture of preimplantation embryos: facts and artifacts.CrossRef | 1:STN:280:DC%2BD2M%2Fps1Cisw%3D%3D&md5=26f46e94362c1bdbc5e71a51102886e8CAS |

Bazer, F. W., Spencer, T. E., Johnson, G. A., Burghardt, R. C., and Wu, G. (2009). Comparative aspects of implantation. Reproduction 138, 195–209.
Comparative aspects of implantation.CrossRef | 1:CAS:528:DC%2BD1MXptlemt74%3D&md5=8c3cc60f5cf5365558bdd25f965af094CAS |

Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
Epigenetic differences between male and female bovine blastocysts produced in vitro.CrossRef | 1:CAS:528:DC%2BD1cXmt1Wjurw%3D&md5=af60d96bf152156d1913920ae1ebe746CAS |

Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC3cXjtFymtbo%3D&md5=aa937c7dba392dbde53b9e853f4d8ec7CAS |

Bhusane, K., Bhutada, S., Chaudhari, U., Savardekar, L., Katkam, R., and Sachdeva, G. (2016). Secrets of endometrial receptivity: some are hidden in uterine secretome. Am. J. Reprod. Immunol. 75, 226–236.
Secrets of endometrial receptivity: some are hidden in uterine secretome.CrossRef |

Binder, N. K., Evans, J., Gardner, D. K., Salamonsen, L. A., and Hannan, N. J. (2014). Endometrial signals improve embryo outcome: functional role of vascular endothelial growth factor isoforms on embryo development and implantation in mice. Hum. Reprod. 29, 2278–2286.
Endometrial signals improve embryo outcome: functional role of vascular endothelial growth factor isoforms on embryo development and implantation in mice.CrossRef | 1:CAS:528:DC%2BC2sXhs1ahsb7K&md5=3697649c500bc6bd586e00b4020d12c5CAS |

Block, J., Hansen, P. J., Loureiro, B., and Bonilla, L. (2011). Improving post-transfer survival of bovine embryos produced in vitro: actions of insulin-like growth factor-1, colony stimulating factor-2 and hyaluronan. Theriogenology 76, 1602–1609.
Improving post-transfer survival of bovine embryos produced in vitro: actions of insulin-like growth factor-1, colony stimulating factor-2 and hyaluronan.CrossRef | 1:CAS:528:DC%2BC3MXhsVanurzL&md5=e2e4010b0a585baced89482653bfdef1CAS |

Buhi, W. C. (2002). Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123, 355–362.
Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein.CrossRef | 1:CAS:528:DC%2BD38Xit1Clsr0%3D&md5=8b10f41489ba9d2f9f9db1ff95a82d8cCAS |

Cao, X. L., Zhao, M. F., Li, D. G., Xing, Y., Zhang, Y. C., Chen, J., He, X. Y., Cui, R., Meng, J. X., Xiao, X., Mu, J., Jiang, Y. Y., and Wu, R. M. (2016). [Establishment of macrophage model of iron overload in vitro and the injury induced by oxidative stress on macrophage with iron overload]. Zhonghua Yi Xue Za Zhi 96, 129–133.
| 1:CAS:528:DC%2BC28Xos1GgsLs%3D&md5=baf01037c734157af2dcf0c303b9a9bbCAS |

Carrasco, L. C., Coy, P., Avilés, M., Gadea, J., and Romar, R. (2008). Glycosidase determination in bovine oviducal fluid at the follicular and luteal phases of the oestrous cycle. Reprod. Fertil. Dev. 20, 808–817.
Glycosidase determination in bovine oviducal fluid at the follicular and luteal phases of the oestrous cycle.CrossRef | 1:CAS:528:DC%2BD1cXhtFWmsLfK&md5=bc7a2f8ef5696b1f4ac961078dce4ad7CAS |

Cebrian-Serrano, A., Salvador, I., García-Roselló, E., Pericuesta, E., Pérez-Cerezales, S., Gutierrez-Adán, A., Coy, P., and Silvestre, M. A. (2013). Effect of the bovine oviductal fluid on in vitro fertilization, development and gene expression of in vitro-produced bovine blastocysts. Reprod. Domest. Anim. 48, 331–338.
Effect of the bovine oviductal fluid on in vitro fertilization, development and gene expression of in vitro-produced bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC3sXmtlWqu7c%3D&md5=0f92996339632df550947675075cd416CAS |

Cordova, A., Perreau, C., Uzbekova, S., Ponsart, C., Locatelli, Y., and Mermillod, P. (2014). Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology 81, 1163–1173.
Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development.CrossRef | 1:CAS:528:DC%2BC2cXktlWmurc%3D&md5=d13e7d04109503090f3945e0c59b9392CAS |

Coy, P., Cánovas, S., Mondéjar, I., Saavedra, M. D., Romar, R., Grullón, L., Matás, C., and Avilés, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc. Natl Acad. Sci. USA 105, 15809–15814.
Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy.CrossRef | 1:CAS:528:DC%2BD1cXht1yitrjL&md5=9135ab8e9bef20d97b3ab660cc6d4dc0CAS |

Doherty, A. S., Mann, M. R. W., Tremblay, K. D., Bartolomei, M. S., and Schultz, R. M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–1535.
Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.CrossRef | 1:CAS:528:DC%2BD3cXjsF2hsrc%3D&md5=e5f2b402dfaafa7b724002d82ed29ed3CAS |

Duranthon, V., Watson, A. J., and Lonergan, P. (2008). Preimplantation embryo programming: transcription, epigenetics, and culture environment. Reproduction 135, 141–150.
Preimplantation embryo programming: transcription, epigenetics, and culture environment.CrossRef | 1:CAS:528:DC%2BD1cXit1yrt7Y%3D&md5=8e8f52dad269fe4c8ea7b8e0252ae3f8CAS |

Enright, B. P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F. A., Yang, X., and Boland, M. P. (2000). Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 54, 659–673.
Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality.CrossRef | 1:STN:280:DC%2BD3M%2FovVGrsg%3D%3D&md5=f85d23d60d8658a7d49449285b735d9dCAS |

Filant, J., and Spencer, T. E. (2014). Uterine glands: biological roles in conceptus implantation, uterine receptivity and decidualization. Int. J. Dev. Biol. 58, 107–116.
Uterine glands: biological roles in conceptus implantation, uterine receptivity and decidualization.CrossRef | 1:CAS:528:DC%2BC2cXhslSrsLzK&md5=a7f5e214fe71935b6740478c233a3891CAS |

Gad, A., Hoelker, M., Besenfelder, U., Havlicek, V., Cinar, U., Rings, F., Held, E., Dufort, I., Sirard, M.-A., Schellander, K., and Tesfaye, D. (2012). Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol. Reprod. 87, 100.
Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions.CrossRef |

Galli, C., Duchi, R., Crotti, G., Turini, P., Ponderato, N., Colleoni, S., Lagutina, I., and Lazzari, G. (2003). Bovine embryo technologies. Theriogenology 59, 599–616.
Bovine embryo technologies.CrossRef | 1:STN:280:DC%2BD38jjslKrsQ%3D%3D&md5=4158f68c6bea94935a9db6bd08c63f67CAS |

Gandolfi, F., and Moor, R. M. (1987). Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. J. Reprod. Fertil. 81, 23–28.
Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells.CrossRef | 1:STN:280:DyaL1c%2FjsFyhtg%3D%3D&md5=6261f3c0725b23aec95efb60773d31e0CAS |

Gómez, E., Correia-Álvarez, E., Caamaño, J. N., Díez, C., Carrocera, S., Peynot, N., Martín, D., Giraud-Delville, C., Duranthon, V., Sandra, O., and Muñoz, M. (2014). Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture. Reproduction 148, 353–365.
Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture.CrossRef |

Gopichandran, N., and Leese, H. J. (2006). The effect of paracrine/autocrine interactions on the in vitro culture of bovine preimplantation embryos. Reproduction 131, 269–277.
The effect of paracrine/autocrine interactions on the in vitro culture of bovine preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD28XisFalsL0%3D&md5=fd8a19c38a0d90d7e22a03bbb078fd66CAS |

Gray, C. A., Bartol, F. F., Taylor, K. M., Wiley, A. A., Ramsey, W. S., Ott, T. L., Bazer, F. W., and Spencer, T. E. (2000). Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle. Biol. Reprod. 62, 448–456.
Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle.CrossRef | 1:CAS:528:DC%2BD3cXotVyjsQ%3D%3D&md5=29623d110eddb0ed39ffdc8855e7384dCAS |

Guérin, P., Mouatassim, S. E., and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.
Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.CrossRef |

Heras, S., De Coninck, D. I. M., Van Poucke, M., Goossens, K., Bogado Pascottini, O., Van Nieuwerburgh, F., Deforce, D., De Sutter, P., Leroy, J. L. M. R., Gutierrez-Adan, A., Peelman, L., and Van Soom, A. (2016). Suboptimal culture conditions induce more deviations in gene expression in male than female bovine blastocysts. BMC Genomics 17, 72.
Suboptimal culture conditions induce more deviations in gene expression in male than female bovine blastocysts.CrossRef |

Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.
High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins.CrossRef | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=4b5bf1ef366000f0c309b3ada47205f5CAS |

Hugentobler, S. A., Diskin, M. G., Leese, H. J., Humpherson, P. G., Watson, T., Sreenan, J. M., and Morris, D. G. (2007). Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol. Reprod. Dev. 74, 445–454.
Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine.CrossRef | 1:CAS:528:DC%2BD2sXhvFCqtLg%3D&md5=6bb0db1194125461620e05c68ade8a0dCAS |

Ireland, J. J., Murphee, R. L., and Coulson, P. B. (1980). Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J. Dairy Sci. 63, 155–160.
Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum.CrossRef | 1:STN:280:DyaL3c7ot1yjsg%3D%3D&md5=10dd5fac037a21ad9544584cb52e103dCAS |

Johnson, M. H., and Nasr-Esfahani, M. H. (1994). Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays 16, 31–38.
Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro?CrossRef | 1:CAS:528:DyaK2cXivFGhu7c%3D&md5=871b3f4377314611c24f6724bc27dcceCAS |

Kalyanaraman, B., Darley-Usmar, V., Davies, K. J. A., Dennery, P. A., Forman, H. J., Grisham, M. B., Mann, G. E., Moore, K., Roberts, L. J., and Ischiropoulos, H. (2012). Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med. 52, 1–6.
Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations.CrossRef | 1:CAS:528:DC%2BC38Xitlyjtw%3D%3D&md5=eac4cfe6e0c188aaa896425f3eb7372fCAS |

Killian, G. J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim. Reprod. Sci. 82–83, 141–153.
Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development.CrossRef |

Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.CrossRef | 1:CAS:528:DC%2BD38XmsV2js7Y%3D&md5=ec0063763e3ac4f671eea9f305de86f1CAS |

Lazzari, G., Colleoni, S., Lagutina, I., Crotti, G., Turini, P., Tessaro, I., Brunetti, D., Duchi, R., and Galli, C. (2010). Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology 73, 748–757.
Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species.CrossRef | 1:STN:280:DC%2BC3c7ot1aksw%3D%3D&md5=818b77d5c074ebfaaa726c9fd2e28c42CAS |

Lloyd, R. E., Romar, R., Matás, C., Gutiérrez-Adán, A., Holt, W. V., and Coy, P. (2009). Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro. Reproduction 137, 679–687.
Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro.CrossRef | 1:CAS:528:DC%2BD1MXosl2ntbw%3D&md5=1f49799d790912d01fc5cdb57baa8940CAS |

Lopera-Vásquez, R., Hamdi, M., Fernandez-Fuertes, B., Maillo, V., Beltrán-Breña, P., Calle, A., Redruello, A., López-Martín, S., Gutierrez-Adán, A., Yañez-Mó, M., Ramirez, M. Á., and Rizos, D. (2016). Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 11, e0148083.
Extracellular vesicles from BOEC in in vitro embryo development and quality.CrossRef |

Lopera-Vasquez, R., Hamdi, M., Maillo, V., Gutierrez-Adan, A., Bermejo-Alvarez, P., Ramirez, M. A., Yanez-Mo, M., and Rizos, D. (2017a). Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro. Reproduction 153, 461–470.
Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro.CrossRef | 1:CAS:528:DC%2BC2sXhtVSlurzF&md5=71d4c64c97489404bbd07163f829bc4cCAS |

Lopera-Vasquez, R., Hamdi, M., Maillo, V., Lloreda, V., Coy, P., Gutierrez-Adan, A., Bermejo-Alvarez, P., and Rizos, D. (2017b). Effect of bovine oviductal fluid on development and quality of bovine embryos produced in vitro. Reprod. Fertil. Dev. 29, 621–629.
Effect of bovine oviductal fluid on development and quality of bovine embryos produced in vitro.CrossRef | 1:CAS:528:DC%2BC2sXivVOgs7o%3D&md5=caa1e68664e8dfea437af65f6d94681cCAS |

Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q. S., and Hansen, P. J. (2009). Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro.CrossRef | 1:CAS:528:DC%2BD1MXhsVCht7bF&md5=c662f1929cf665c12c19a680a7ceb919CAS |

McCauley, T. C., Buhi, W. C., Wu, G. M., Mao, J., Caamano, J. N., Didion, B. A., and Day, B. N. (2003). Oviduct-specific glycoprotein modulates sperm–zona binding and improves efficiency of porcine fertilization in vitro. Biol. Reprod. 69, 828–834.
Oviduct-specific glycoprotein modulates sperm–zona binding and improves efficiency of porcine fertilization in vitro.CrossRef | 1:CAS:528:DC%2BD3sXmvVeitL0%3D&md5=6a852950ecb6dcb326854b6162c35dd7CAS |

Mondéjar, I., Grullón, L. A., García-Vázquez, F. A., Romar, R., and Coy, P. (2012). Fertilization outcome could be regulated by binding of oviductal plasminogen to oocytes and by releasing of plasminogen activators during interplay between gametes. Fertil. Steril. 97, 453–461.e3.
Fertilization outcome could be regulated by binding of oviductal plasminogen to oocytes and by releasing of plasminogen activators during interplay between gametes.CrossRef |

Mondéjar, I., Martínez-Martínez, I., Avilés, M., and Coy, P. (2013). Identification of potential oviductal factors responsible for zona pellucida hardening and monospermy during fertilization in mammals. Biol. Reprod. 89, 67.
Identification of potential oviductal factors responsible for zona pellucida hardening and monospermy during fertilization in mammals.CrossRef |

Moore, K., Rodríguez-Sallaberry, C. J., Kramer, J. M., Johnson, S., Wroclawska, E., Goicoa, S., and Niasari-Naslaji, A. (2007). In vitro production of bovine embryos in medium supplemented with a serum replacer: effects on blastocyst development, cryotolerance and survival to term. Theriogenology 68, 1316–1325.
In vitro production of bovine embryos in medium supplemented with a serum replacer: effects on blastocyst development, cryotolerance and survival to term.CrossRef | 1:CAS:528:DC%2BD2sXht1Krs7jI&md5=53ebf3a4b9e842495a05a43139468a88CAS |

Nasr-Esfahani, M. H., Aitken, J. R., and Johnson, M. H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109, 501–507.
| 1:CAS:528:DyaK3cXlsV2nsbo%3D&md5=3e452df359ef8e45b6633262d3528f1eCAS |

Niemann, H., and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.
Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development.CrossRef | 1:CAS:528:DC%2BD3cXkvVyqug%3D%3D&md5=5874eb3ab0e04aa5887cfa57d61b63b4CAS |

O’Doherty, A. M., Magee, D. A., O’Shea, L. C., Forde, N., Beltman, M. E., Mamo, S., and Fair, T. (2015). DNA methylation dynamics at imprinted genes during bovine pre-implantation embryo development. BMC Dev. Biol. 15, 13.
DNA methylation dynamics at imprinted genes during bovine pre-implantation embryo development.CrossRef |

Parrish, J. J. (2014). Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin. Theriogenology 81, 67–73.
Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin.CrossRef |

Pradeep, M. A., Jagadeesh, J., De, A. K., Kaushik, J. K., Malakar, D., Kumar, S., Dang, A. K., Das, S. K., and Mohanty, A. K. (2011). Purification, sequence characterization and effect of goat oviduct-specific glycoprotein on in vitro embryo development. Theriogenology 75, 1005–1015.
Purification, sequence characterization and effect of goat oviduct-specific glycoprotein on in vitro embryo development.CrossRef | 1:CAS:528:DC%2BC3MXis1aru7k%3D&md5=abfc72f364126cb62908f7642f6aed33CAS |

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=b1311147b0c039d6783153079f8b6ad3CAS |

Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., De La Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–243.
Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression.CrossRef | 1:CAS:528:DC%2BD3sXjtFWj&md5=e26815a79f88578cc9a508423632b5e8CAS |

Rizos, D., Clemente, M., Bermejo-Alvarez, P., de La Fuente, J., Lonergan, P., and Gutiérrez-Adán, A. (2008). Consequences of in vitro culture conditions on embryo development and quality. Reprod. Domest. Anim. 43, 44–50.
Consequences of in vitro culture conditions on embryo development and quality.CrossRef |

Rizos, D., Ramirez, M. A., Pintado, B., Lonergan, P., and Gutierrez-Adan, A. (2010). Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct. Theriogenology 73, 777–785.
Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct.CrossRef | 1:STN:280:DC%2BC3c7ot1Gmug%3D%3D&md5=936bdd71120636b4e56bbca82f1ea1c6CAS |

Rosenkrans, C. F., and First, N. L. (1994). Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J. Anim. Sci. 72, 434–437.
Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro.CrossRef | 1:CAS:528:DyaK2cXisVeitr4%3D&md5=77de01c241bb519c62fd1eb869ae95e3CAS |

Saadeldin, I. M., Oh, H. J., and Lee, B. C. (2015). Embryonic–maternal cross-talk via exosomes: potential implications. Stem Cells Cloning 8, 103–107.

Santana, P. D. P. B., Silva, T. V. G., da Costa, N. N., da Silva, B. B., Carter, T. F., Cordeiro, M. S., da Silva, B. J. M., Santos, S. S. D., Herculano, A. M., Adona, P. R., Ohashi, O. M., and Miranda, M. S. (2014). Supplementation of bovine embryo culture medium with l-arginine improves embryo quality via nitric oxide production. Mol. Reprod. Dev. 81, 918–927.
Supplementation of bovine embryo culture medium with l-arginine improves embryo quality via nitric oxide production.CrossRef | 1:CAS:528:DC%2BC2cXhslelsrnM&md5=9f89f5d33cefc4a362dcea1a4e262371CAS |

Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
Analyzing real-time PCR data by the comparative C(T) method.CrossRef | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=c158bd79247a48891822495d3f4249a2CAS |

Soleilhavoup, C., Riou, C., Tsikis, G., Labas, V., Harichaux, G., Kohnke, P., Reynaud, K., de Graaf, S. P., Gerard, N., and Druart, X. (2016). Proteomes of the female genital tract during the oestrous cycle. Mol. Cell. Proteomics 15, 93–108.
Proteomes of the female genital tract during the oestrous cycle.CrossRef | 1:CAS:528:DC%2BC28XhvFOjug%3D%3D&md5=9ac9e14e10433f03f7b962a8d3b5b662CAS |

Steeves, T. E., and Gardner, D. K. (1999). Temporal and differential effects of amino acids on bovine embryo development in culture. Biol. Reprod. 61, 731–740.
Temporal and differential effects of amino acids on bovine embryo development in culture.CrossRef | 1:CAS:528:DyaK1MXlsFCqtr4%3D&md5=75816df871b5e74ef50da2960c179000CAS |

Sugino, N., Shimamura, K., Takiguchi, S., Tamura, H., Ono, M., Nakata, M., Nakamura, Y., Ogino, K., Uda, T., and Kato, H. (1996). Changes in activity of superoxide dismutase in the human endometrium throughout the menstrual cycle and in early pregnancy. Hum. Reprod. 11, 1073–1078.
Changes in activity of superoxide dismutase in the human endometrium throughout the menstrual cycle and in early pregnancy.CrossRef | 1:CAS:528:DyaK28XksVOksb4%3D&md5=76e5a7daae7e1209287d394f0149b3d3CAS |

Takahashi, Y., and First, N. L. (1992). In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963–978.
In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins.CrossRef | 1:CAS:528:DyaK3sXpvVOmtg%3D%3D&md5=7268bad7ee73f72bcb153740e03c2b87CAS |

Tesfaye, D., Lonergan, P., Hoelker, M., Rings, F., Nganvongpanit, K., Havlicek, V., Besenfelder, U., Jennen, D., Tholen, E., and Schellander, K. (2007). Suppression of connexin 43 and E-cadherin transcripts in in vitro derived bovine embryos following culture in vitro or in vivo in the homologous bovine oviduct. Mol. Reprod. Dev. 74, 978–988.
Suppression of connexin 43 and E-cadherin transcripts in in vitro derived bovine embryos following culture in vitro or in vivo in the homologous bovine oviduct.CrossRef | 1:CAS:528:DC%2BD2sXntVOhuro%3D&md5=63f8ec25cd04e546ede19825de99a5d7CAS |

Thompson, J. G., Partridge, R. J., Houghton, F. D., Cox, C. I., and Leese, H. J. (1996). Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J. Reprod. Fertil. 106, 299–306.
Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos.CrossRef | 1:CAS:528:DyaK28XitFKntrc%3D&md5=57cdad9e6db4a320de85344f646d7a31CAS |

Turan, N., Katari, S., Gerson, L. F., Chalian, R., Foster, M. W., Gaughan, J. P., Coutifaris, C., and Sapienza, C. (2010). Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet. 6, e1001033.
Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology.CrossRef |

Yong, P., Gu, Z., Luo, J. P., Wang, J. R., and Tso, J. K. (2002). Antibodies against the C-terminal peptide of rabbit oviductin inhibit mouse early embryo development to pass 2-cell stage. Cell Res. 12, 69–78.
Antibodies against the C-terminal peptide of rabbit oviductin inhibit mouse early embryo development to pass 2-cell stage.CrossRef |

Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.CrossRef | 1:CAS:528:DC%2BD3MXhtFGktL8%3D&md5=4b6c2abb2daa3f9e4b36bc4d8a131a97CAS |



Export Citation

View Altmetrics