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

Secretome derived from different cell lines in bovine embryo production in vitro

C. Perrini A B , P. Esposti A , F. Cremonesi A B and A. Lange Consiglio B C
+ Author Affiliations
- Author Affiliations

A Department of Veterinary Medicine, Università degli Studi di Milano, Via Celoria 10, 20133 Milano, Italy.

B Reproduction Unit, Centro Clinico-Veterinario e Zootecnico Sperimentale di Ateneo, Università degli Studi di Milano, Via dell’Università 6, 26900 Lodi, Italy.

C Corresponding author. Email: anna.langeconsiglio@unimi.it

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17356
Submitted: 5 April 2017  Accepted: 12 September 2017   Published online: 6 October 2017

Abstract

The present study investigated the effects of conditioned medium (CM), composed of microvesicles (MVs) and soluble factors present in the supernatant (SN), of bovine endometrial and amniotic cells on embryo quality and rate of blastocyst production. Presumptive zygotes were randomly assigned on Days 1, 3 and 5 after fertilisation to synthetic oviducal fluid with amino acids (SOFaa; control) or to SOFaa supplemented with either 20% endometrial or amniotic CM, 20% SN or 100 × 106 MVs mL−1. Embryos were evaluated on Day 7. For groups supplemented with MVs derived from either endometrial or amniotic cells on Day 1 of culture, blastocysts had developed, but at a lower rate than in the control group. Blastocysts had developed in all groups in which endometrial or amniotic cell-derived CM or MVs were added on Day 3 of culture, but the rate of blastocyst development was significantly lower in both CM groups than in the MVs groups. The addition of all secretome fractions (CM, MVs and SN) derived from either bovine endometrial or amniotic cells on Day 5 of culture resulted in blastocyst production, but only amniotic MVs resulted in a blastocyst production rate comparable to that in the control group. Supplementation of SOFaa on Day 5 resulted in a qualitatively higher number of inner cell mass cells compared with the control group only for the amniotic CM and MVs groups. At day 7, these data were confirmed by RT-qPCR evaluation of genes (Bcl-2-associated X protein (BAX) and glutathione peroxidase 1 (GPX1) involved in apoptosis and protection against reactive oxygen species. In conclusion, of the different secretome fractions tested, only amniotic MVs added to SOFaa resulted in better outcomes than in the control group.

Additional keywords: amniotic cells, conditioned medium, embryo quality, endometrial cells, microvesicles.


References

Bakri, N. M., Ibrahim, S. F., Osman, N. A., Hasan, N., Jaffar, F. H. F., Rahman, Z. A., and Osman, K. (2016). Embryo apoptosis identification: oocyte grade or cleavage stage? Saudi J. Biol. Sci. 23, S50–S55.
Embryo apoptosis identification: oocyte grade or cleavage stage?CrossRef |

Barañao, R. I., Piazza, A., Rumi, L. S., and Polak de Fried, E. (1997). Determination of IL-1 and IL-6 levels in human embryo culture-conditioned media. Am. J. Reprod. Immunol. 37, 191–194.
Determination of IL-1 and IL-6 levels in human embryo culture-conditioned media.CrossRef |

Berg, D. K., van Leeuwen, J., Beaumont, S., Berg, M., and Pfeffer, P. L. (2010). Embryo loss in cattle between Days 7 and 16 of pregnancy. Theriogenology 73, 250–260.
Embryo loss in cattle between Days 7 and 16 of pregnancy.CrossRef | 1:STN:280:DC%2BD1MfhvVWguw%3D%3D&md5=cce5e75b0f97b6b244e505af4f1156daCAS |

Booth, P. J., Holm, P., and Callesen, H. (2005). The effect of oxygen tension on porcine embryonic development is dependent on embryo type. Theriogenology 63, 2040–2052.
The effect of oxygen tension on porcine embryonic development is dependent on embryo type.CrossRef |

Bruno, S., Grange, C., Deregibus, M. C., Calogero, R. A., Saviozzi, S., Collino, F., Morando, L., Busca, A., Falda, M., Bussolati, B., Tetta, C., and Camussi, G. (2009). Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J. Am. Soc. Nephrol. 20, 1053–1067.
Mesenchymal stem cell-derived microvesicles protect against acute tubular injury.CrossRef | 1:CAS:528:DC%2BD1MXlvFKqtrY%3D&md5=1791bb5a4126ee52d8fc1d3e6ab1d76aCAS |

Bruno, S., Grange, C., Collino, F., Deregibus, M. C., Cantaluppi, V., Biancone, L., Tetta, C., and Camussi, G. (2012). Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 7, e33115.
Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury.CrossRef | 1:CAS:528:DC%2BC38Xks1KitLs%3D&md5=d7cf427fbdf8a1575927a9920adc12faCAS |

Burns, G., Brooks, K., Wildung, M., Navakanitworakul, R., Christenson, L. K., and Spencer, T. E. (2014). Extracellular vesicles in luminal fluid of the ovine uterus. PLoS One 9, e90913.
Extracellular vesicles in luminal fluid of the ovine uterus.CrossRef |

Camussi, G., Deregibus, M. C., Bruno, S., Cantaluppi, V., and Biancone, L. (2010). Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 78, 838–848.
Exosomes/microvesicles as a mechanism of cell-to-cell communication.CrossRef | 1:CAS:528:DC%2BC3cXht1yrsrrP&md5=7bfdadab339147eeba1e5ea85ced845aCAS |

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 |

Corradetti, B., Meucci, A., Bizzaro, D., Cremonesi, F., and Lange Consiglio, A. (2013). Mesenchymal stem cells from amnion and amniotic fluid in bovine. Reproduction 145, 391–400.
Mesenchymal stem cells from amnion and amniotic fluid in bovine.CrossRef | 1:CAS:528:DC%2BC3sXotFaitLo%3D&md5=b95afab38077836e501ae4ce2cf00e1fCAS |

Donofrio, G., Franceschi, V., Capocefalo, A., Cavirani, S., and Sheldon, I. M. (2008). Bovine endometrial stromal cells display osteogenic properties. Reprod. Biol. Endocrinol. 6, 65–73.
Bovine endometrial stromal cells display osteogenic properties.CrossRef |

Gjørret, J. O., Wengle, J., Maddox-Hyttel, P., and King, W. A. (2005). Chronological appearance of apoptosis in bovine embryos reconstructed by somatic cell nuclear transfer from quiescent granulosa cells. Reprod. Domest. Anim. 40, 210–216.
Chronological appearance of apoptosis in bovine embryos reconstructed by somatic cell nuclear transfer from quiescent granulosa cells.CrossRef |

Gualtieri, R., Mollo, V., Braun, S., Barbato, V., Fiorentino, I., and Talevi, R. (2012). Long-term viability and differentiation of bovine oviductal monolayers: bidimensional versus three-dimensional culture. Theriogenology 78, 1456–1464.
Long-term viability and differentiation of bovine oviductal monolayers: bidimensional versus three-dimensional culture.CrossRef | 1:CAS:528:DC%2BC38Xht1Kjur7P&md5=cf8d4dcead70d48a323122578cc7ea1bCAS |

Gutiérrez-Adán, A., Granados, J., Pintado, B., and de la Fuente, J. (2001). Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod. Fertil. Dev. 13, 361–365.
Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro.CrossRef |

Harvey, M. B., Arcellana-Panlilio, M. Y., Zhang, X., Schultz, G. A., and Watson, A. J. (1995). Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol. Reprod. 53, 532–540.
Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture.CrossRef | 1:CAS:528:DyaK2MXns1yls7o%3D&md5=f3f9f67533a48735e63ea15c7d205dcbCAS |

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 |

Ijaz, A., Lambert, R. D., and Sirard, M. A. (1994). In vitro cultured bovine granulosa and oviductal cells secrete sperm motility maintaining factor(s). Mol. Reprod. Dev. 37, 54–60.
In vitro cultured bovine granulosa and oviductal cells secrete sperm motility maintaining factor(s).CrossRef | 1:STN:280:DyaK2c7ns1WltA%3D%3D&md5=c2d60a9f1219d495a4017be80a12563cCAS |

Ishiwata, I., Tokieda, Y., Kiguchi, K., Sato, K., and Ishikawa, H. (2000). Effects of embryotrophic factors on the embryogenesis and organogenesis of mouse embryos in vitro. Hum. Cell 13, 185–195.
| 1:STN:280:DC%2BD3MzpsFKjug%3D%3D&md5=a2ea2e4ec7f8156304291050f7611252CAS |

Izquierdo, D., Villamediana, P., and Paramio, M. T. (1999). Effect of culture media on embryo development from prepubertal goat IVM-IVF oocytes. Theriogenology 52, 847–861.
Effect of culture media on embryo development from prepubertal goat IVM-IVF oocytes.CrossRef | 1:STN:280:DC%2BD3c7pvFejsg%3D%3D&md5=b01a42c2a05d26eaccdf36b8d5dc9674CAS |

Kikuchi, K., Onishi, A., Kashiwazaki, N., Iwamoto, M., Noguchi, J., Kaneko, H., Akita, T., and Nagai, T. (2002). Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol. Reprod. 66, 1033–1041.
Successful piglet production after transfer of blastocysts produced by a modified in vitro system.CrossRef | 1:CAS:528:DC%2BD38XitlClur8%3D&md5=dcc08d1b959b6c754a17420baa44b209CAS |

Kim, J. H., Niwa, K., Lim, J. M., and Okuda, K. (1993). Effects of phosphate, energy substrates, and amino acids on development of in vitro-matured, in vitro-fertilized bovine oocytes in a chemically defined, protein-free culture medium. Biol. Reprod. 48, 1320–1325.
Effects of phosphate, energy substrates, and amino acids on development of in vitro-matured, in vitro-fertilized bovine oocytes in a chemically defined, protein-free culture medium.CrossRef | 1:CAS:528:DyaK3sXks1yrtrs%3D&md5=fba00c7fbe3b4f453d88aec0a202f5a9CAS |

Kobayashi, K., Takagi, Y., Satoh, T., Hoshi, H., and Oikawa, T. (1992). Development of early bovine embryos to the blastocyst stage in serum-free conditioned medium from bovine granulosa cells. In Vitro Cell. Dev. Biol. 28A, 255–259.
Development of early bovine embryos to the blastocyst stage in serum-free conditioned medium from bovine granulosa cells.CrossRef | 1:STN:280:DyaK383lvFCnsQ%3D%3D&md5=d0723f94a3da9b4212fb247c3945b860CAS |

Lange-Consiglio, A., Maggio, V., Pellegrino, L., and Cremonesi, F. (2012). Equine bone marrow mesenchymal or amniotic epithelial stem cells as feeder in a model for the in vitro culture of bovine embryos. Zygote 20, 45–51.
Equine bone marrow mesenchymal or amniotic epithelial stem cells as feeder in a model for the in vitro culture of bovine embryos.CrossRef | 1:CAS:528:DC%2BC38Xjs1aktw%3D%3D&md5=fec57477379af1c5a5f3c089454d564dCAS |

Lange-Consiglio, A., Accogli, G., Cremonesi, F., and Desantis, S. (2014). Cell surface glycan changes in the spontaneous epithelial–mesenchymal transition of equine amniotic multipotent progenitor cells. Cells Tissues Organs 200, 212–226.
Cell surface glycan changes in the spontaneous epithelial–mesenchymal transition of equine amniotic multipotent progenitor cells.CrossRef | 1:CAS:528:DC%2BC2MXhsF2rtLvK&md5=ba3f025d05a6f3ec26449bad496ab144CAS |

Lange-Consiglio, A., Perrini, C., Tasquier, R., Deregibus, M. C., Camussi, G., Pascucci, L., Marini, M. G., Corradetti, B., Bizzaro, D., De Vita, B., Romele, P., Parolini, O., and Cremonesi, F. (2016). Microvesicles secreted from equine amniotic-derived cells and their potential role in reducing inflammation in a tendon in vitro model. Stem Cells Dev. 25, 610–621.
Microvesicles secreted from equine amniotic-derived cells and their potential role in reducing inflammation in a tendon in vitro model.CrossRef | 1:CAS:528:DC%2BC28Xlsl2jtLY%3D&md5=111c8b53783e4134ff90f669f56281fbCAS |

Lee, Y. L., Lee, K. F., Xu, J. S., Kwok, K. L., Luk, J. M., Lee, W. M., and Yeung, W. S. (2003). Embryotrophic factor-3 from human oviductal cells affects the messenger RNA expression of mouse blastocyst. Biol. Reprod. 68, 375–382.
Embryotrophic factor-3 from human oviductal cells affects the messenger RNA expression of mouse blastocyst.CrossRef | 1:CAS:528:DC%2BD3sXntVequw%3D%3D&md5=7903d1050d2be6c5bfa61812cc5b3045CAS |

Li, X., Morris, L. H. A., and Allen, W. R. (2001). Influence of coculture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI). Reproduction 121, 925–932.
Influence of coculture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI).CrossRef | 1:CAS:528:DC%2BD3MXkslWntrk%3D&md5=03f0a726ce0ec53490e9e8d16b952c15CAS |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCT method.CrossRef | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=27001fc4d390214adec9d2e6245c9fd6CAS |

Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H., and Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol. Reprod. 54, 1420–1429.
Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro.CrossRef | 1:CAS:528:DyaK28XjtV2nsLo%3D&md5=ec83ca6e229ad8bbd13e65761ffaf007CAS |

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 |

Machtinger, R., Laurent, L. C., and Baccarelli, A. A. (2016). Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum. Reprod. Update 22, 182–193.

Marini, M. G., Perrini, C., Esposti, P., Corradetti, B., Bizzaro, D., Riccaboni, P., Fantinato, E., Urbani, G., Gelati, G., Cremonesi, F., and Lange-Consiglio, A. (2016). Effects of platelet-rich plasma in a model of bovine endometrial inflammation in vitro. Reprod. Biol. Endocrinol. 14, 58.
Effects of platelet-rich plasma in a model of bovine endometrial inflammation in vitro.CrossRef |

McCallie, B., Schoolcraft, W., and Katz-Jaffe, M. G. (2010). Aberration of blastocyst microRNA expression is associated with human infertility. Fertil. Steril. 93, 2374–2382.
Aberration of blastocyst microRNA expression is associated with human infertility.CrossRef | 1:CAS:528:DC%2BC3cXms1ylsbk%3D&md5=477b3fd0c88bf1e3a36ecd1d4cef3356CAS |

Melka, M. G., Rings, F., Holker, M., Tholen, E., Havlicek, V., Besenfelder, U., Schellander, K., and Tesfaye, D. (2010). Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos. Reprod. Domest. Anim. 45, 915–921.
| 1:CAS:528:DC%2BC3cXhtlSgtLbL&md5=08a72cb01b2e31ecc086e4e311a12708CAS |

Mermillod, P., Vansteenbrugge, A., Wils, C., Mourmeaux, J. L., Massip, A., and Dessy, F. (1993). Characterization of the embryotrophic activity of exogenous protein-free oviduct-conditioned medium used in culture of cattle embryos. Biol. Reprod. 49, 582–587.
Characterization of the embryotrophic activity of exogenous protein-free oviduct-conditioned medium used in culture of cattle embryos.CrossRef | 1:STN:280:DyaK2c%2Fgt1Omuw%3D%3D&md5=58fa67e405516fbbb2dc2316531378b8CAS |

Park, J. S., Han, Y. M., Lee, C. S., Kim, S. J., Kim, Y. H., Lee, K. J., Lee, K. S., and Lee, K. K. (2000). Improved development of DNA-injected bovine embryos co-cultured with mouse embryonic fibroblast cells. Anim. Reprod. Sci. 59, 13–22.
Improved development of DNA-injected bovine embryos co-cultured with mouse embryonic fibroblast cells.CrossRef | 1:CAS:528:DC%2BD3cXjtVeqtr0%3D&md5=65668f43407a8f0474d6b4913fa9f6a8CAS |

Pereira, T., Ivanova, G., Caseiro, A. R., Barbosa, P., Bàrtolo, P. J., Santos, J. D., Luìs, A. L., and Maurıcio, A. C. (2014). MSCs conditioned media and umbilical cord blood plasma metabolomics and composition. PLoS One 9, e113769.
MSCs conditioned media and umbilical cord blood plasma metabolomics and composition.CrossRef |

Pohland, R., and Tiemann, U. (1994). Immunohistochemical localization of the epidermal growth factor and its binding sites in the bovine female reproductive tract. J. Reprod. Fertil. Abstr. Ser. 14, Abstract 56.

Pomar, F. J., Teerds, K. J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguilar, B., and Roelen, B. A. (2005). Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–2268.
Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study.CrossRef | 1:CAS:528:DC%2BD2MXjtFyrtbg%3D&md5=1bc4bb8367e6553fe7b7f46704d2a225CAS |

Raposo, G., and Stoorvogel, W. (2013). Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373–383.
Extracellular vesicles: exosomes, microvesicles, and friends.CrossRef | 1:CAS:528:DC%2BC3sXjtFCnsbk%3D&md5=73224e7b99e8c01f220c50fbe60cb4c3CAS |

Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2006). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495.
Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication.CrossRef | 1:CAS:528:DC%2BD28XosVSjsrk%3D&md5=b0ada5a144cda19cffd70d7638d57fdfCAS |

Rexroad, C. E., and Powell, A. M. (1993). Development of ovine embryos co-cultured on oviductal cells, embryonic fibroblasts, or STO cell monolayers. Biol. Reprod. 49, 789–793.
Development of ovine embryos co-cultured on oviductal cells, embryonic fibroblasts, or STO cell monolayers.CrossRef |

Rieger, D., Grisart, B., Semple, E., Van Langendonckt, A., Betteridge, K., and Dessy, F. (1995). Comparison of the effects of oviductal cell co-culture and oviductal cell-conditioned medium on the development and metabolic activity of cattle embryos. J. Reprod. Fertil. 105, 91–98.
Comparison of the effects of oviductal cell co-culture and oviductal cell-conditioned medium on the development and metabolic activity of cattle embryos.CrossRef | 1:CAS:528:DyaK2MXptVKmt7k%3D&md5=5d4281c9f8d07e58402892c41c569d7cCAS |

Rosenbluth, E. M., Shelton, D. N., Wells, L. M., Sparks, A. E. T., and Van Voorhis, B. J. (2014). Human embryos secrete microRNAs into culture media – a potential biomarker for implantation. Fertil. Steril. 101, 1493–1500.
Human embryos secrete microRNAs into culture media – a potential biomarker for implantation.CrossRef | 1:CAS:528:DC%2BC2cXksFWgurs%3D&md5=b1397588b43ee3fa6f156f74529822d4CAS |

Rottmayer, R., Ulbrich, S., Kölle, S., Prelle, K., Neumüller, C., Sinowatz, F., Meyer, H., Wolf, E., and Hiendleder, S. (2006). A bovine oviduct epithelial cell suspension culture system suitable for studying embryo–maternal interactions: morphological and functional characterization. Reproduction 132, 637–648.
A bovine oviduct epithelial cell suspension culture system suitable for studying embryo–maternal interactions: morphological and functional characterization.CrossRef | 1:CAS:528:DC%2BD28Xht1ahs7rJ&md5=ffc360fd04c692dfe8fadd2bcd27510eCAS |

Schmaltz-Panneau, B., Locatelli, Y., Uzbekova, S., Perreau, C., and Mermillod, P. (2015). Bovine oviduct epithelial cells dedifferentiate partly in culture, while maintaining their ability to improve early embryo development rate and quality. Reprod. Domest. Anim. 50, 719–729.
Bovine oviduct epithelial cells dedifferentiate partly in culture, while maintaining their ability to improve early embryo development rate and quality.CrossRef | 1:CAS:528:DC%2BC2MXhsFGitbnK&md5=175d0f5d29053cf373b14a0ad7107290CAS |

Sostaric, E., Dieleman, S. J., van de Lest, C. H., Colenbrander, B., Vos, P. L., Garcia-Gil, N., and Gadella, B. M. (2008). Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation. Mol. Reprod. Dev. 75, 60–74.
Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation.CrossRef |

Thatcher, W. W., Guzeloglu, A., Mattos, R., Binelli, M., Hansen, T. R., and Pru, J. K. (2001). Uterine–conceptus interactions and reproductive failure in cattle. Theriogenology 56, 1435–1450.
Uterine–conceptus interactions and reproductive failure in cattle.CrossRef | 1:CAS:528:DC%2BD38XjslyqsQ%3D%3D&md5=a2cbb22dacc3425fce14964ea1052cc2CAS |

Théry, C., Ostrowski, M., and Segura, E. (2009). Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581–593.
Membrane vesicles as conveyors of immune responses.CrossRef |

Thouas, G. A., Korfiatis, N. A., French, A. J., Jones, G. M., and Trounson, A. O. (2001). A simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3, 25–29.
A simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts.CrossRef |

Ulbrich, S. E., Zitta, K., Hiendleder, S., and Wolf, E. (2010). In vitro systems for intercepting early embryo–maternal cross-talk in the bovine oviduct. Theriogenology 73, 802–816.
In vitro systems for intercepting early embryo–maternal cross-talk in the bovine oviduct.CrossRef | 1:CAS:528:DC%2BC3cXivFGltr0%3D&md5=352c3e30cbdfb15531b9cb53784d2238CAS |

Van Langendonckt, A., Vansteenbrugge, A., Donnay, I., Van Soom, A., Berg, U., Semple, E., Grisart, B., Mermillod, P., Brem, G., Massip, A., and Dessy, F. (1996). Three-year results of in vitro production of bovine embryos in serum-poor bovine oviduct conditioned medium. An overview. Reprod. Nutr. Dev. 36, 493–502.
Three-year results of in vitro production of bovine embryos in serum-poor bovine oviduct conditioned medium. An overview.CrossRef | 1:STN:280:DyaK2s7ktVKgsg%3D%3D&md5=b249f5cccc27948bdcdb67e5cf738882CAS |

Ventura-Juncá, P., Irarrázaval, I., Rolle, A. J., Gutiérrez, J. I., Moreno, R. D., and Santos, M. J. (2015). In vitro fertilization (IVF) in mammals: epigenetic and developmental alterations. Scientific and bioethical implications for IVF in humans. Biol. Res. 48, 68.
In vitro fertilization (IVF) in mammals: epigenetic and developmental alterations. Scientific and bioethical implications for IVF in humans.CrossRef |

White, K. L., Hehnke, K., Rickords, L. F., Southern, L. L., Thompson, D. L., and Wood, T. C. (1989). Early embryonic development in vitro by co-culture with oviductal epithelial cells in pigs. Biol. Reprod. 41, 425–430.
Early embryonic development in vitro by co-culture with oviductal epithelial cells in pigs.CrossRef | 1:STN:280:DyaK3c%2FnsVKktw%3D%3D&md5=38974482112b32f500eda8d55477cbb7CAS |

Wrenzycki, C., and Stinshoff, H. (2013). Maturation environment and impact on subsequent developmental competence of bovine oocytes. Reprod. Domest. Anim. 48, 38–43.
Maturation environment and impact on subsequent developmental competence of bovine oocytes.CrossRef |

Xu, J. S., Cheung, T. M., Chan, S. T. H., Ho, P. C., and Yeung, W. S. B. (2001). Temporal effect of human oviductal cell and its derived embryotrophic factors on mouse embryo development. Biol. Reprod. 65, 1481–1488.
Temporal effect of human oviductal cell and its derived embryotrophic factors on mouse embryo development.CrossRef | 1:CAS:528:DC%2BD3MXnvVers7g%3D&md5=bcbc1ce8c78a0cf387732d8c7de1fa50CAS |

Zhang, M., Ouyang, H., and Xia, G. (2009). The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol. Hum. Reprod. 15, 399–409.
The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption.CrossRef |

Zhu, J., Barrat, C. L., Lippes, J., Pacey, A. A., and Cooke, I. D. (1994). The sequential effects of human cervical mucus, oviductal fluid, and follicular fluid on sperm function. Fertil. Steril. 61, 1129–1135.
The sequential effects of human cervical mucus, oviductal fluid, and follicular fluid on sperm function.CrossRef | 1:STN:280:DyaK2c3lt1Cgtg%3D%3D&md5=fee2a3a50a62a5c2f2818310a5b0abffCAS |



Export Citation