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

Effects of oocyte quality, incubation time and maturation environment on the number of chromosomal abnormalities in IVF-derived early bovine embryos

Sebastian Demyda-Peyrás A D , Jesus Dorado B , Manuel Hidalgo B , Jaouad Anter A , Leonardo De Luca C , Enrique Genero C and Miguel Moreno-Millán A
+ Author Affiliations
- Author Affiliations

A Department of Genetics, University of Cordoba, CN IV KM 396, Campus Rabanales CP 14071, Gregor Mendel Building, Cordoba, Spain.

B Animal Reproduction Group, Department of Medicine and Animal Surgery, Faculty of Veterinary Medicine, University of Cordoba, CN IV KM 396, Campus Rabanales CP 14071, Spain.

C Animal Production Department, Lomas de Zamora University, Ruta 4 Km 2 CP 1834, Llavallol, Bs As, Argentina.

D Corresponding author. Email: ge2depes@uco.es

Reproduction, Fertility and Development 25(7) 1077-1084 https://doi.org/10.1071/RD12140
Submitted: 1 May 2012  Accepted: 27 September 2012   Published: 27 November 2012

Abstract

Chromosomal aberrations are one of the major causes of embryo developmental failures in mammals. The occurrence of these types of abnormalities is higher in in vitro-produced (IVP) embryos. The aim of the present study was to investigate the effect of oocyte morphology and maturation conditions on the rate of chromosomal abnormalities in bovine preimplantational embryos. To this end, 790 early cattle embryos derived from oocytes with different morphologies and matured under different conditions, including maturation period (24 v. 36 h) and maturation media (five different serum supplements in TCM-199), were evaluated cytogenetically in three sequential experiments. The rates of normal diploidy and abnormal haploidy, polyploidy and aneuploidy were determined in each embryo. Throughout all the experiments, the rate of chromosomal abnormalities was significantly (P < 0.05) affected by oocyte morphology and maturation conditions (maturation time and culture medium). Lower morphological quality was associated with a high rate of chromosome abnormalities (P < 0.05). Moreover, polyploidy was associated with increased maturation time (P < 0.01), whereas the maturation medium significantly (P < 0.05) affected the rates of haploidy and polyploidy. In general, supplementing the maturation medium with oestrous cow serum or fetal calf serum resulted in higher rates of chromosomal aberrations (P < 0.05) compared with the other serum supplements tested (bovine steer serum, anoestroues cow serum, bovine amniotic fluid and bovine serum albumin). On the basis of the results of the present study, we conclude that the morphological quality of oocytes and the maturation conditions affect the rate of chromosomal abnormalities in IVP bovine embryos.

Additional keywords: aneuploidy, cattle, chromosome analysis, developmental failures, in vitro produced (IVP) embryos, maturation time, polyploidy, serum supplementation.


References

A’arabi, S. Y., Roussel, J. D., and Chandler, J. E. (1997). Chromosomal analysis of mammalian oocytes matured in vitro with various culture systems. Theriogenology 48, 1173–1183.
Chromosomal analysis of mammalian oocytes matured in vitro with various culture systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtV2mtQ%3D%3D&md5=219370bebef6f80e38e1cd252690d935CAS | 16728206PubMed |

Alexander, B., Coppola, G., Berardina, D., Rho, G.J., St John, E., Bett, D. H., and King, W. A. (2006). The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos. Mol. Reprod. Dev. 73, 20–30.
The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht12ntb%2FF&md5=cdbee20e45c0ca001b65c1a02e6acb57CAS | 16211597PubMed |

Barrett, S. L., and Albertini, D. F. (2010). Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J. Assist. Reprod. Genet. 27, 29–39.
Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence.Crossref | GoogleScholarGoogle Scholar | 20039198PubMed |

Bilodeau-Goeseels, S. (2006). Effects of culture media and energy sources on the inhibition of nuclear maturation in bovine oocytes. Theriogenology 66, 297–306.
Effects of culture media and energy sources on the inhibition of nuclear maturation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 16384597PubMed |

Blondin, P., and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsVagsrs%3D&md5=cba71ae9155a69088ccc1199253de068CAS | 7619506PubMed |

Cetica, P. D., Dalvit, G. C., and Beconi, M. T. (1999). Study of evaluation criteria used for in vitro bovine oocyte selection and maturation. Biocell 23, 125–133.
| 1:STN:280:DC%2BD3czosVerug%3D%3D&md5=8a85ffe28735d371b2d27338323b5336CAS | 10904537PubMed |

Christopikou, D., Karamalegos, C., Doriza, S., Argyrou, M., Sisi, P., Davies, S., and Mastrominas, M. (2010). Spindle and chromosome configurations of human oocytes matured in vitro in two different culture media. Reprod. Biomed. Online 20, 639–648.
Spindle and chromosome configurations of human oocytes matured in vitro in two different culture media.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfgsVentA%3D%3D&md5=2747017548951aad011ff47f97098355CAS | 20347392PubMed |

Coticchio, G., Sereni, E., Serrao, L., Mazzone, S., Iadarola, I., and Borini, A. (2004). What criteria for the definition of oocyte quality? Ann. N. Y. Acad. Sci. 1034, 132–144.
What criteria for the definition of oocyte quality?Crossref | GoogleScholarGoogle Scholar | 15731306PubMed |

Dale, B., and Defelice, L. (2011). Polyspermy prevention: facts and artifacts? J. Assist. Reprod. Genet. 28, 199–207.
Polyspermy prevention: facts and artifacts?Crossref | GoogleScholarGoogle Scholar | 21104196PubMed |

Dieleman, S. J., Hendriksen, P. J. M., Viuff, D., Thomsen, P. D., Hyttel, P., Knijn, H. M., Wrenzycki, C., Kruip, T. A. M., Niemann, H., Gadella, B. M., Bevers, M. M., and Vos, P. L. A. M. (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 5–20.
Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fksl2luw%3D%3D&md5=5abda134b64670cbceef40c80ae19443CAS | 11775980PubMed |

Ebner, T., Moser, M., Sommergruber, M., and Tews, G. (2003). Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum. Reprod. Update 9, 251–262.
Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szivFWqsA%3D%3D&md5=93e243b4c9572f3bb8a7679e309b1533CAS | 12859046PubMed |

Eichenlaub-Ritter, U., Wieczorek, M., Lüke, S., and Seidel, T. (2011). Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion 11, 783–796.
Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsr%2FF&md5=2de61c6cb829347a917b849e1e32c28fCAS | 20817047PubMed |

Frumkin, T., Malcov, M., Yaron, Y., and Ben-Yosef, D. (2008). Elucidating the origin of chromosomal aberrations in IVF embryos by preimplantation genetic analysis. Mol. Cell. Endocrinol. 282, 112–119.
Elucidating the origin of chromosomal aberrations in IVF embryos by preimplantation genetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVegtrY%3D&md5=0853e221c3d175e5a1568164f6ed6d2cCAS | 18177997PubMed |

Fukui, Y., and Ono, H. (1989). Effects of sera, hormones and granulosa cells added to culture medium for in-vitro maturation, fertilization, cleavage and development of bovine oocytes. J. Reprod. Fertil. 86, 501–506.
Effects of sera, hormones and granulosa cells added to culture medium for in-vitro maturation, fertilization, cleavage and development of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkslWitr8%3D&md5=dfcb2225e9667e9b0f94c385e6d82ed0CAS | 2760879PubMed |

Funahashi, H. (2003). Polyspermic penetration in porcine IVM–IVF systems. Reprod. Fertil. Dev. 15, 167–177.
Polyspermic penetration in porcine IVM–IVF systems.Crossref | GoogleScholarGoogle Scholar | 12921703PubMed |

Garcia-Herreros, M., Carter, T. F., Villagmez, D. A. F., MacAulay, A. D., Rath, D., King, W. A., and Lonergan, P. (2010). Incidence of chromosomal abnormalities in bovine blastocysts derived from unsorted and sex-sorted spermatozoa. Reprod. Fertil. Dev. 22, 1272–1278.
Incidence of chromosomal abnormalities in bovine blastocysts derived from unsorted and sex-sorted spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfms12ltA%3D%3D&md5=31d80dd8c2b2edb7e3ade28c1799a2c9CAS | 20883653PubMed |

Gliedt, D. W., Rosenkrans, C. F., Rorie, R. W., and Rakes, J. M. (1996). Effects of oocyte maturation length, sperm capacitation time, and heparin on bovine embryo development. J. Dairy Sci. 79, 532–535.
Effects of oocyte maturation length, sperm capacitation time, and heparin on bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjt1Ogur0%3D&md5=c6220952485a31fa4477bab65a2181e4CAS | 8744216PubMed |

Hawk, H. W., and Wall, R. J. (1994). Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells. Theriogenology 41, 1585–1594.
Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells.Crossref | GoogleScholarGoogle Scholar |

Jakobsen, A. S., Thomsen, P. D., and Avery, B. (2006). Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro. Theriogenology 65, 870–881.
Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 16115669PubMed |

Kawarsky, S. J., Basrur, P. K., Stubbings, R. B., Hansen, P. J., and King, W. A. (1996). Chromosomal abnormalities in bovine embryos and their influence on development. Biol. Reprod. 54, 53–59.
Chromosomal abnormalities in bovine embryos and their influence on development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLrJ&md5=340385b4e12cef81f6cdffd92c827cdeCAS | 8838000PubMed |

King, W. A. (1990). Chromosome abnormalities and pregnancy failure in domestic animals. Adv. Vet. Sci. Comp. Med. 34, 229–250.

King, W. A., Coppola, G., Alexander, B., Mastromonaco, G., Perrault, S., Nino-Soto, M. I., Pinton, A., Joudrey, E. M., and Betts, D. H. (2006). The impact of chromosomal alteration on embryo development. Theriogenology 65, 166–177.
The impact of chromosomal alteration on embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GitrzE&md5=25e5b240aa6e8d04dba95992e9edcfa6CAS | 16280155PubMed |

Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.
| 15471793PubMed |

Lechniak, D., Świtoński, M., and Sosnowski, M. (1996). The incidence of bovine diploid oocytes matured in vitro. Theriogenology 46, 267–277.
The incidence of bovine diploid oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVKmsA%3D%3D&md5=537ac3bc6d4173f2bfdeccb6860e0f72CAS | 16727896PubMed |

Lechniak, D., Szczepankiewicz, D., Kauss, D., Szulc, J., and Szydłowski, M. (2005). IVM media, oocyte diameter and donor genotype at RYR1 locus in relation to the incidence of porcine diploid oocytes after maturation in vitro. Theriogenology 64, 202–212.
IVM media, oocyte diameter and donor genotype at RYR1 locus in relation to the incidence of porcine diploid oocytes after maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVGkt7k%3D&md5=d2d4b3095f8a9619c5414ae21dcea420CAS | 15935853PubMed |

Liu, L., and Keefe, D. L. (2002). Ageing-associated aberration in meiosis of occytes from senescence-accelerated mice. Hum. Reprod. 17, 2678–2685.
Ageing-associated aberration in meiosis of occytes from senescence-accelerated mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1GgtL0%3D&md5=dc5141276347faa152b2b14119f9ed66CAS | 12351548PubMed |

Liu, S., Feng, H. L., Marchesi, D., Chen, Z. J., and Hershlag, A. (2011). Dose-dependent effects of gonadotropin on oocyte developmental competence and apoptosis. Reprod. Fertil. Dev. 23, 990–996.
Dose-dependent effects of gonadotropin on oocyte developmental competence and apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlWjt7nK&md5=1ff8ca4aa6008e2e638e9c6d8cdb9234CAS | 22127004PubMed |

Lonergan, P. (2007). State-of-the-art embryo technologies in cattle. Soc. Reprod. Fertil. Suppl. 64, 315–325.
| 1:STN:280:DC%2BD2s3otlKiuw%3D%3D&md5=193f1b3c76e0203e51f428b665f761c6CAS | 17491156PubMed |

Lonergan, P., Pedersen, H. G., Rizos, D., Greve, T., Thomsen, P. D., Fair, T., Evans, A., and Boland, M. P. (2004). Effect of the post-fertilization culture environment on the incidence of chromosome aberrations in bovine blastocysts. Biol. Reprod. 71, 1096–1100.
Effect of the post-fertilization culture environment on the incidence of chromosome aberrations in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7w%3D&md5=1b6926607d4bc319182fb845ddbc42afCAS | 15189826PubMed |

Long, C. R., Damiani, P., Pinto-Correia, C., MacLean, R. A., Duby, R. T., and Robl, J. M. (1994). Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization. J. Reprod. Fertil. 102, 361–369.
Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtFyns7w%3D&md5=578f5171a57736a58e65aea275893c1eCAS | 7861389PubMed |

Máximo, D. M., Martins da Silva, I. G., Mondadori, R. G., Neves, J. P., and Lucci, C. M. (2012). Ultrastructural characteristics of sheep oocytes during in vitro maturation (IVM). Small Rumin. Res. 105, 210–215.
Ultrastructural characteristics of sheep oocytes during in vitro maturation (IVM).Crossref | GoogleScholarGoogle Scholar |

Mermillod, P., Schmaltz, B., Perreau, C., Tsikis, G., Martinot, E., Cordova, A., and Locatelli, Y. (2010). Early development of ruminant embryos, autonomous process or the result of a positive dialog with surrounding maternal tissues? Acta Sci. Vet. 38, S521–S533.

Nagano, M., Katagiri, S., and Takahashi, Y. (2006). Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.
Relationship between bovine oocyte morphology and in vitro developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVCgt7o%3D&md5=5fc184a32fd41baa88f0857712247a30CAS | 16700976PubMed |

Nicodemo, D., Pauciullo, A., Cosenza, G., Peretti, V., Perucatti, A., Di Meo, G. P., Ramunno, L., Iannuzzi, L., Rubes, J., and Di Berardino, D. (2010). Frequency of aneuploidy in in vitro-matured MII oocytes and corresponding first polar bodies in two dairy cattle (Bos taurus) breeds as determined by dual-color fluorescent in situ hybridization. Theriogenology 73, 523–529.
Frequency of aneuploidy in in vitro-matured MII oocytes and corresponding first polar bodies in two dairy cattle (Bos taurus) breeds as determined by dual-color fluorescent in situ hybridization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7hs1ykuw%3D%3D&md5=053e354bf0bfd6a1e502ccec55105441CAS | 20022097PubMed |

Niwa, K. (1993). Effectiveness of in vitro maturation and in vitro fertilization techniques in pigs. J. Reprod. Fertil. Suppl. 48, 49–59.
| 1:STN:280:DyaK2c7psVCktA%3D%3D&md5=4d6047fd021a8fe505771eca771efe60CAS | 8145214PubMed |

Ocaña-Quero, J. M., Pinedo-Merlin, M., and Moreno-Millan, M. (1999a). Cytogenetic study of in vitro-derived bovine embryos. Vet. J. 158, 228–233.
Cytogenetic study of in vitro-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 10558844PubMed |

Ocaña-Quero, J. M., Pinedo-Merlin, M., and Moreno-Millan, M. (1999b). Influence of follicle size, medium, temperature and time on the incidence of diploid bovine oocytes matured in vitro. Theriogenology 51, 667–672.
Influence of follicle size, medium, temperature and time on the incidence of diploid bovine oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 10729051PubMed |

Ott, M., Schernthaner, W., Sinowatz, F., and Wolf, E. (2002). Effects of bovine serum albumin and estrous cow serum on development and ultrastructure of in vitro-produced porcine embryos. Anat. Histol. Embryol. 31, 151–157.
Effects of bovine serum albumin and estrous cow serum on development and ultrastructure of in vitro-produced porcine embryos.Crossref | GoogleScholarGoogle Scholar | 12479358PubMed |

Pan, H., Ma, P., Zhu, W., and Schultz, R. M. (2008). Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 316, 397–407.
Age-associated increase in aneuploidy and changes in gene expression in mouse eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVKrtLw%3D&md5=dfba40d84f10b41ca4a6e83852485038CAS | 18342300PubMed |

Parrish, J. J., Susko-Parrish, J. L., Critser, E. S., Eyestone, W. H., and First, N. L. (1986). Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25, 591–600.
Bovine in vitro fertilization with frozen-thawed semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvV2itQ%3D%3D&md5=58442e0cbb471ce7354cab23738b634fCAS | 16726150PubMed |

Pereira, M. M., MacHado, M. A., Costa, F. Q., Serapiao, R. V., Viana, J. H. M., and Camargo, L. S. A. (2010). Effect of oxygen tension and serum during IVM on developmental competence of bovine oocytes. Reprod. Fertil. Dev. 22, 1074–1082.
Effect of oxygen tension and serum during IVM on developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 20797345PubMed |

Pontes, J. H. F., Nonato-Junior, I., Sanches, B. V., Ereno-Junior, J. C., Uvo, S., Barreiros, T. R. R., Oliveira, J. A., Hasler, J. F., and Seneda, M. M. (2009). Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology 71, 690–697.
Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2Fpt1yrsw%3D%3D&md5=4390f2499a6c0df55c1f334be3941bd9CAS |

Pontes, J. H. F., Silva, K. C. F., Basso, A. C., Rigo, A. G., Ferreira, C. R., Santos, G. M. G., Sanches, B. V., Porcionato, J. P. F., Vieira, P. H. S., Faifer, F. S., Sterza, F. A. M., Schenk, J. L., and Seneda, M. M. (2010). Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus–taurus dairy cows using sexed sperm. Theriogenology 74, 1349–1355.
Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus–taurus dairy cows using sexed sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfntlyqsA%3D%3D&md5=65603a0547e5478080d9df852fefa5e5CAS |

Purpera, M. N., Giraldo, A. M., Ballard, C. B., Hylan, D., Godke, R. A., and Bondioli, K. R. (2009). Effects of culture medium and protein supplementation on mRNA expression of in vitro produced bovine embryos. Mol. Reprod. Dev. 76, 783–793.
Effects of culture medium and protein supplementation on mRNA expression of in vitro produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKjs70%3D&md5=6ffb3da7173343fb7455a9ddc8f6c40bCAS | 19288542PubMed |

Rambags, B. P. B., Krijtenburg, P. J., Van Drie, H. F., Lazzari, G., Galli, C., Pearson, P. L., Colenbrander, B., and Stout, T. A. E. (2005). Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87.
Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsL4%3D&md5=b1fb2105350a44573e94d467be66281cCAS |

Räty, M., Ketoja, E., Pitkänen, T., Ahola, V., Kananen, K., and Peippo, J. (2011). In vitro maturation supplements affect developmental competence of bovine cumulus–oocyte complexes and embryo quality after vitrification. Cryobiology 63, 245–255.
In vitro maturation supplements affect developmental competence of bovine cumulus–oocyte complexes and embryo quality after vitrification.Crossref | GoogleScholarGoogle Scholar | 21985767PubMed |

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=7e1cd9cffb7fc878404e93f2e0a29d94CAS | 11803560PubMed |

Russell, D. F., Baqir, S., Bordignon, J., and Betts, D. H. (2006). The impact of oocyte maturation media on early bovine embryonic development. Mol. Reprod. Dev. 73, 1255–1270.
The impact of oocyte maturation media on early bovine embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptlSnu7w%3D&md5=5814b93751f81dba631acc1b6cbcec63CAS | 16865717PubMed |

Suzuki, H., Saito, Y., Kagawa, N., and Yang, X. (2003). In vitro fertilization and polyspermy in the pig: factors affecting fertilization rates and cytoskeletal reorganization of the oocyte. Microsc. Res. Tech. 61, 327–334.
In vitro fertilization and polyspermy in the pig: factors affecting fertilization rates and cytoskeletal reorganization of the oocyte.Crossref | GoogleScholarGoogle Scholar | 12811737PubMed |

Tajik, P., and Esfandabadi, N. S. (2003). In vitro maturation of caprine oocytes in different culture media. Small Rumin. Res. 47, 155–158.
In vitro maturation of caprine oocytes in different culture media.Crossref | GoogleScholarGoogle Scholar |

Tajik, P., Beheshti-Govij, R., Soleimani-Rad, J., Ghasemzadeh-Nava, H., and Mohamadi-Roshandeh, A. (2008). Effects of different concentrations of bovine follicular fluid and estrous cow serum on development of murine 2-cell embryos. Pak. J. Biol. Sci. 11, 628–632.
Effects of different concentrations of bovine follicular fluid and estrous cow serum on development of murine 2-cell embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnislGjuw%3D%3D&md5=90d2eac488ba2decb7ffe262f6ab7f5bCAS | 18817138PubMed |

Tarín, J. J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717–724.
Potential effects of age-associated oxidative stress on mammalian oocytes/embryos.Crossref | GoogleScholarGoogle Scholar | 9239688PubMed |

Tarín, J. J., Trounson, A. O., and Sathananthan, H. (1999). Origin and ploidy of multipronuclear zygotes. Reprod. Fertil. Dev. 11, 273–279.
Origin and ploidy of multipronuclear zygotes.Crossref | GoogleScholarGoogle Scholar | 10898292PubMed |

Ueno, S., Kurome, M., Ueda, H., Tomii, R., Hiruma, K., and Nagashima, H. (2005). Effects of maturation conditions on spindle morphology in porcine MII oocytes. J. Reprod. Dev. 51, 405–410.
Effects of maturation conditions on spindle morphology in porcine MII oocytes.Crossref | GoogleScholarGoogle Scholar | 15812143PubMed |

Ulloa Ulloa, C. M., Yoshizawa, M., Komoriya, E., Mitsui, A., Nagai, T., and Kikuchi, K. (2008a). The blastocyst production rate and incidence of chromosomal abnormalities by developmental stage in in vitro produced porcine embryos. J. Reprod. Dev. 54, 22–29.
The blastocyst production rate and incidence of chromosomal abnormalities by developmental stage in in vitro produced porcine embryos.Crossref | GoogleScholarGoogle Scholar |

Ulloa Ulloa, C. M., Yoshizawa, M., Yamashita, A., Hama, S., Mitsui, A., Hashi, C., Abe, H., Hoshi, H., Fukui, E., and Matsumoto, H. (2008b). Blastocyst production from in vitro-produced day-2 bovine embryos classified by cleavage stage, and cytogenetical evaluation of the resultant day-8 blastocysts. J. Reprod. Dev. 54, 465–472.
Blastocyst production from in vitro-produced day-2 bovine embryos classified by cleavage stage, and cytogenetical evaluation of the resultant day-8 blastocysts.Crossref | GoogleScholarGoogle Scholar | 18957827PubMed |

Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A., and Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68, S131–S137.
Gamete origin in relation to early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLk%3D&md5=49c77445178abdd5317c59684d4fae3bCAS | 17467789PubMed |

Vialard, F., Boitrelle, F., Molina-Gomes, D., and Selva, J. (2011). Predisposition to aneuploidy in the oocyte. Cytogenet. Genome Res. 133, 127–135.
Predisposition to aneuploidy in the oocyte.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MvivFCjtA%3D%3D&md5=a3a4e7423af42b57c26873ce6934e8f5CAS | 21335956PubMed |

Villamediana, P., Vidal, F., and Paramio, M. T. (2001). Cytogenetic analysis of caprine 2- to 4-cell embryos produced in vitro. Zygote 9, 193–199.
Cytogenetic analysis of caprine 2- to 4-cell embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsVOltbo%3D&md5=b015db5406d0792d6008602ae2b9f0bdCAS | 11508738PubMed |

Viuff, D., Rickords, L., Offenberg, H., Hyttel, P., Avery, B., Greve, T., Olsaker, I., Williams, J. L., Callesen, H., and Thomsen, P. D. (1999). A high proportion of bovine blastocysts produced in vitro are mixoploid. Biol. Reprod. 60, 1273–1278.
A high proportion of bovine blastocysts produced in vitro are mixoploid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVaqtbw%3D&md5=907e6e6432bab76a5f27b29d121f8e33CAS | 10330080PubMed |

Wang, W. H., Hosoe, M., and Shioya, Y. (1997). Induction of cortical granule exocytosis of pig oocytes by spermatozoa during meiotic maturation. J. Reprod. Fertil. 109, 247–255.
Induction of cortical granule exocytosis of pig oocytes by spermatozoa during meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivV2gtLc%3D&md5=a1413f66f1bc538f6664041fa83e0159CAS | 9155734PubMed |

Wortzman, G. B., and Evans, J. P. (2005). Membrane and cortical abnormalities in post-ovulatory aged eggs: analysis of fertilizability and establishment of the membrane block to polyspermy. Mol. Hum. Reprod. 11, 1–9.
Membrane and cortical abnormalities in post-ovulatory aged eggs: analysis of fertilizability and establishment of the membrane block to polyspermy.Crossref | GoogleScholarGoogle Scholar | 15516358PubMed |

Xu, L., Wang, Y., Zhou, P., Cao, Y. X., Huang, T. H., and Chian, R. C. (2008). Cytogenetic analysis of in vivo and in vitro matured oocytes derived from naturally cycling and stimulated mice. Syst. Biol. Reprod. Med. 54, 155–162.
Cytogenetic analysis of in vivo and in vitro matured oocytes derived from naturally cycling and stimulated mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFejs7s%3D&md5=8da0c049a139dd7acd5cbb84048875cbCAS | 18570051PubMed |

Yang, X., Jiang, S., and Foote, R. H. (1993). Bovine oocyte development following different oocyte maturation and sperm capacitation procedures. Mol. Reprod. Dev. 34, 94–100.
Bovine oocyte development following different oocyte maturation and sperm capacitation procedures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7hvFKksw%3D%3D&md5=d71dc6054149fce566c5d1dccd8db7d3CAS | 8418824PubMed |