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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Comparison of different fertilisation media for an in vitro maturation–fertilisation–culture system using flow-cytometrically sorted X chromosome-bearing spermatozoa for bovine embryo production

Luis B. Ferré A F , Yanina Bogliotti B , James L. Chitwood B , Cristóbal Fresno C , Hugo H. Ortega D , Michael E. Kjelland E and Pablo J. Ross B
+ Author Affiliations
- Author Affiliations

A Instituto Nacional de Tecnología Agropecuaria, Ruta Nacional 34, Km 227, Rafaela (2300), Santa Fe, Argentina.

B Department of Animal Science, One Shields Avenue, University of California, Davis, CA 95616, USA.

C Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Facultad de Ingeniería, Universidad Católica de Córdoba, Av. Armada Argentina 3555, X5016DHK, Córdoba, Argentina.

D Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral/CONICET, R.P. Kreder 2805 (S3080HOF), Esperanza, Santa Fe, Argentina.

E Conservation, Genetics and Biotech, LLC, Vicksburg, MS 39182, USA.

F Corresponding author. Email: ferre.luis@inta.gob.ar

Reproduction, Fertility and Development 28(11) 1695-1703 https://doi.org/10.1071/RD15019
Submitted: 19 September 2014  Accepted: 29 March 2015   Published: 13 May 2015

Abstract

High demand exists among commercial cattle producers for in vitro-derived bovine embryos fertilised with female sex-sorted spermatozoa from high-value breeding stock. The aim of this study was to evaluate three fertilisation media, namely M199, synthetic oviductal fluid (SOF) and Tyrode’s albumin–lactate–pyruvate (TALP), on IVF performance using female sex-sorted spermatozoa. In all, 1143, 1220 and 1041 cumulus–oocyte complexes were fertilised in M199, SOF and TALP, respectively. There were significant differences among fertilisation media (P < 0.05) in cleavage rate (M199 = 57%, SOF = 71% and TALP = 72%), blastocyst formation (M199 = 9%, SOF = 20% and TALP = 19%), proportion of Grade 1 blastocysts (M199 = 15%, SOF = 52% and TALP = 51%), proportion of Grade 3 blastocysts (M199 = 58%, SOF = 21% and TALP = 20%) and hatching rates (M199 = 29%, SOF = 60% and TALP = 65%). The inner cell mass (ICM) and trophectoderm (TE) cells of Day 7 blastocysts were also affected by the fertilisation medium. Embryos derived from SOF and TALP fertilisation media had higher numbers of ICM, TE and total cells than those fertilised in M199. In conclusion, fertilisation media affected cleavage rate, as well as subsequent embryo development, quality and hatching ability. SOF and TALP fertilisation media produced significantly more embryos of higher quality than M199.

Additional keywords: in vitro produced, zona pellucida.


References

Agarwal, A., Said, T. M., Bedaiwy, M. A., Banerjee, J., and Alvarez, J. G. (2006). Oxidative stress in an assisted reproductive techniques setting. Fertil. Steril. 86, 503–512.
Oxidative stress in an assisted reproductive techniques setting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCqs7bJ&md5=5bafbb29bda869e24316f7d96ecffc58CAS | 16860798PubMed |

Aitken, R. J., and Henkel, R. R. (2011). Sperm cell biology: current perspectives and future prospects. Asian J. Androl. 13, 3–5.
Sperm cell biology: current perspectives and future prospects.Crossref | GoogleScholarGoogle Scholar | 21102477PubMed |

Aitken, R. J., Jones, K. T., and Robertson, S. A. (2012). Reactive oxygen species and sperm function: in sickness and in health. J. Androl. 33, 1096–1106.
Reactive oxygen species and sperm function: in sickness and in health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvFaqsQ%3D%3D&md5=010ceeceed5ece4735d0c1e3f6b01b33CAS | 22879525PubMed |

Al-Katanani, Y. M., Drost, M., Monson, R. L., Rutledge, J. J., Krininger, C. E., Block, J., Thatcher, W. W., and Hanse, P. J. (2002). Pregnancy rates following timed embryo transfer with fresh or vitrified in vitro produced embryos in lactating dairy cows under heat stress conditions. Theriogenology 58, 171–182.
Pregnancy rates following timed embryo transfer with fresh or vitrified in vitro produced embryos in lactating dairy cows under heat stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38visF2nsA%3D%3D&md5=e577cbc96b64d92624c6d9b68fe87382CAS | 12182360PubMed |

Alomar, M., Mahieu, J., Verhaeghe, B., Defoin, L., and Donnay, I. (2006). Assessment of sperm quality parameters of six bulls showing different abilities to promote embryo development in vitro. Reprod. Fertil. Dev. 18, 395–402.
Assessment of sperm quality parameters of six bulls showing different abilities to promote embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287nt1aksA%3D%3D&md5=1cd5ee1d10f858db3d50bb2ee8190192CAS | 16554015PubMed |

Ambrose, J. D., Drost, M., Monson, R. L., Rutledge, J. J., Leibfried-Rutledge, M. L., Thatcher, M. J., Kassa, T., Binelli, M., Hansen, P. J., Chenoweth, P. J., and Thatcher, W. W. (1999). Efficacy of timed embryo transfer with fresh and frozen in vitro produced embryos to increase pregnancy rates in heat-stressed dairy cattle. J. Dairy Sci. 82, 2369–2376.
Efficacy of timed embryo transfer with fresh and frozen in vitro produced embryos to increase pregnancy rates in heat-stressed dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVGnur8%3D&md5=a5791243c626952b66e61601ece53177CAS | 10575603PubMed |

Arav, A., Aroyo, A., Yavin, S., and Roth, Z. (2008). Prediction of embryonic developmental competence by time-lapse observation and ‘shortest-half’ analysis. Reprod. Biomed. Online 17, 669–675.
Prediction of embryonic developmental competence by time-lapse observation and ‘shortest-half’ analysis.Crossref | GoogleScholarGoogle Scholar | 18983751PubMed |

Bansal, A. K., and Bilaspuri, G. S. (2010). Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 2010, 686137.
Impacts of oxidative stress and antioxidants on semen functions.Crossref | GoogleScholarGoogle Scholar | 20871827PubMed |

Barceló-Fimbres, M., Campos-Chillón, L. F., and Seidel, G. E. (2011). In vitro fertilization using non-sexed and sexed bovine sperm: sperm concentration, sorter pressure, and bull effects. Reprod. Domest. Anim. 46, 495–502.
In vitro fertilization using non-sexed and sexed bovine sperm: sperm concentration, sorter pressure, and bull effects.Crossref | GoogleScholarGoogle Scholar | 20946538PubMed |

Biggers, J. D., McGinnis, L. K., and Raffin, M. (2000). Amino acids and preimplantation development of the mouse in protein-free potassium simplex optimized medium. Biol. Reprod. 63, 281–293.
Amino acids and preimplantation development of the mouse in protein-free potassium simplex optimized medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2rsbw%3D&md5=cef8f9b558d8697631b0d0aa275879caCAS | 10859270PubMed |

Blondin, P., Beaulieu, M., Fournier, V., Morin, N., Crawford, L., Madan, P., and King, W. A. (2009). Analysis of bovine sexed sperm for IVF from sorting to the embryo. Theriogenology 71, 30–38.
Analysis of bovine sexed sperm for IVF from sorting to the embryo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1Gmuw%3D%3D&md5=60af48a4fb3b912f7fa476c394728a53CAS | 19004490PubMed |

Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xnt1WltQ%3D%3D&md5=13ba9e96972395a57c009a79e1b8e288CAS | 1122333PubMed |

Chatterjee, S., and Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Mol. Reprod. Dev. 59, 451–458.
Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVWmsb4%3D&md5=b23035aa48f27e41b1e95d518ba87dfeCAS | 11468782PubMed |

Chaubal, S. A., Ferre, L. B., Molina, J. A., Faber, D. C., Bols, P. E. J., Rezamand, P., Tian, X., and Yang, X. (2007). Hormonal treatments for increasing the oocyte and embryo production in an OPU–IVP system. Theriogenology 67, 719–728.
Hormonal treatments for increasing the oocyte and embryo production in an OPU–IVP system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCksLs%3D&md5=452a68254de9d5e1b611c99edec0b908CAS | 17140652PubMed |

Choi, Y. H., Fukui, Y., and Ono, H. (1991). Effects of media and the presence of bovine oviduct epithelial cells during in vitro fertilization on fertilizability and developmental capacity of bovine oocytes. Theriogenology 36, 863–873.
Effects of media and the presence of bovine oviduct epithelial cells during in vitro fertilization on fertilizability and developmental capacity of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFyiug%3D%3D&md5=60ad73512be0007322e40a8fd41460c8CAS | 16727055PubMed |

Crichton, E. H. S., McSweeney, K., and Schenk, J. (2006). Artificial insemination of lactating Holstein cows with sexed sperm. Reprod. Fertil. Dev. 18, 281.
Artificial insemination of lactating Holstein cows with sexed sperm.Crossref | GoogleScholarGoogle Scholar |

DeJarnette, J. M., Nebel, R. L., Marshall, C. E., Moreno, J. F., McCleary, C. R., and Lenz, R. W. (2008). Effect of sex-sorted sperm dosage on conception rates in Holstein heifers and lactating cows. J. Dairy Sci. 91, 1778–1785.
Effect of sex-sorted sperm dosage on conception rates in Holstein heifers and lactating cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlWmtL8%3D&md5=b163777f9826f6278ebe429fa306469bCAS | 18420608PubMed |

DeJarnette, J. M., Nebel, R. L., and Marshall, C. E. (2009). Evaluating the success of sex-sorted semen in US dairy herds from on farm records. Theriogenology 71, 49–58.
Evaluating the success of sex-sorted semen in US dairy herds from on farm records.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1CrtQ%3D%3D&md5=11102e040d05b6df161f7b4e27da5ed0CAS | 18996579PubMed |

DeJarnette, J. M., McCleary, C. R., Leach, M. A., Moreno, J. F., Nebel, R. L., and Marshall, C. E. (2010). Effects of 2.1 and 3.5x10(6) sex-sorted sperm dosages on conception rates of Holstein cows and heifers. J. Dairy Sci. 93, 4079–4085.
Effects of 2.1 and 3.5x10(6) sex-sorted sperm dosages on conception rates of Holstein cows and heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCqtrjF&md5=de3a58e6afdfcb44d098163ec4c9fb48CAS | 20723682PubMed |

DeJarnette, J. M., Leach, M. A., Nebel, R. L., Marshall, C. E., McCleary, C. R., and Moreno, J. F. (2011). Effects of sex-sorting and sperm dosage on conception rates of Holstein heifers: is comparable fertility of sex-sorted and conventional semen plausible? J. Dairy Sci. 94, 3477–3483.
Effects of sex-sorting and sperm dosage on conception rates of Holstein heifers: is comparable fertility of sex-sorted and conventional semen plausible?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFahs7c%3D&md5=3383026ba0121dfa4b0fea9d9a9f2ce1CAS | 21700034PubMed |

Development-Core-Team (2005). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.)

Di Rienzo, J., Casanoves, F., Balzarini, M., Gonzalez, L., Tablada, M., and Robledo, C. (2011). ‘InfoStat v2011.’ (InfoStat Group, College of Agricultural Sciences, National University of Córdoba: Argentina.)

Dinnyés, A., Lonergan, P., Fair, T., Boland, M. P., and Yang, X. (1999). Timing of the first cleavage post-insemination affects cryosurvival of in vitro-produced bovine blastocysts. Mol. Reprod. Dev. 53, 318–324.
Timing of the first cleavage post-insemination affects cryosurvival of in vitro-produced bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 10369392PubMed |

Dochi, O., Takahashi, K., Hirai, T., Hayakawa, H., Tanisawa, M., Yamamoto, Y., and Koyama, H. (2008). The use of embryo transfer to produce pregnancies in repeat-breeding dairy cattle. Theriogenology 69, 124–128.
The use of embryo transfer to produce pregnancies in repeat-breeding dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2sjhvVCmtg%3D%3D&md5=6946d941f4203056defe6f461ab7a30aCAS | 17942148PubMed |

Donnay, I., Verhaeghe, B., and Neirinckx, G. (2004). Enriching a defined maturation medium improves subsequent embryonic development of bovine oocytes cultured in small and large groups. Reprod. Fertil. Dev. 16, 274.
Enriching a defined maturation medium improves subsequent embryonic development of bovine oocytes cultured in small and large groups.Crossref | GoogleScholarGoogle Scholar |

Galantino-Homer, H. L., Florman, H. M., Storey, B. T., Dobrinski, I., and Kopf, G. S. (2004). Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Mol. Reprod. Dev. 67, 487–500.
Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWnurk%3D&md5=578d1b3f82a297c34a1b072699a400cdCAS | 14991741PubMed |

Galli, C., Crotti, G., Notari, C., Turini, P., Duchi, R., and Lazzari, G. (2001). Embryo production by ovum pick up from live donors. Theriogenology 55, 1341–1357.
Embryo production by ovum pick up from live donors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzotlWjtg%3D%3D&md5=c260a13eb07555cfb642c56e61669e10CAS | 11327688PubMed |

Gandhi, A. P., Lane, M., Gardner, D. K., and Krisher, R. L. (2000). A single medium supports development of bovine embryos throughout maturation, fertilization and culture. Hum. Reprod. 15, 395–401.
A single medium supports development of bovine embryos throughout maturation, fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1eruw%3D%3D&md5=138c58f4bfd5a813baad22084f8ed0beCAS | 10655312PubMed |

Garner, D. L. (2006). Flow cytometric sexing of mammalian sperm. Theriogenology 65, 943–957.
Flow cytometric sexing of mammalian sperm.Crossref | GoogleScholarGoogle Scholar | 16242764PubMed |

Garner, D. L., and Seidel, G. E. (2008). History of commercializing sexed semen for cattle. Theriogenology 69, 886–895.
History of commercializing sexed semen for cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3hsFertw%3D%3D&md5=6f117d6777f769701422268845145c42CAS | 18343491PubMed |

Garner, D. L., Evans, K. M., and Seidel, G. E. (2013). Sex-sorting sperm using flow cytometry/cell sorting. Methods Mol. Biol. 927, 279–295.
Sex-sorting sperm using flow cytometry/cell sorting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1SmsrY%3D&md5=42e907a80274dbf8a731d96e1aaa32a7CAS | 22992923PubMed |

Goissis, M. D., and Cibelli, J. B. (2014). Functional characterization of SOX2 in bovine preimplantation embryos. Biol. Reprod. 90, 30.
Functional characterization of SOX2 in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 24389873PubMed |

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL0%3D&md5=ae43df3fd3d386c7af3d91773ce3c33aCAS | 16452720PubMed |

Gosálvez, J., Ramirez, M. A., López-Fernández, C., Crespo, F., Evans, K. M., Kjelland, M. E., and Moreno, J. F. (2011). Sex-sorted bovine spermatozoa and DNA damage: II. Dynamic features. Theriogenology 75, 206–211.
Sex-sorted bovine spermatozoa and DNA damage: II. Dynamic features.Crossref | GoogleScholarGoogle Scholar | 21040960PubMed |

Hegde, A., and Behr, B. (2012). Media composition: growth factors. Methods Mol. Biol. 912, 177–198.
| 1:CAS:528:DC%2BC3sXmslWrtg%3D%3D&md5=b0905ce603288138dbb44c041aea1d1fCAS | 22829375PubMed |

Holm, P., Shukri, N. N., Vajta, G., Booth, P., Bendixen, C., and Callesen, H. (1998). Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology 50, 1285–1299.
Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVKitQ%3D%3D&md5=360cd03bd7e262027a98a755d167385bCAS | 10734442PubMed |

Johnson, L. A., Flook, J. P., and Hawk, H. W. (1989). Sex preselection in rabbits: live births from X and Y sperm separated by DNA and cell sorting. Biol. Reprod. 41, 199–203.
Sex preselection in rabbits: live births from X and Y sperm separated by DNA and cell sorting.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGisA%3D%3D&md5=fd6d26defc4abdc32e6d8c86583932c4CAS | 2804212PubMed |

Johnson, L. A., Welch, G. R., and Rens, W. (1999). The Beltsville sperm sexing technology: high-speed sperm sorting gives improved sperm output for in vitro fertilization and AI. J. Anim. Sci. 77, 213–220.
| 1:CAS:528:DyaK1MXlvFWgsro%3D&md5=69cdbb4fb15ef6dc82b3c52fa99341faCAS | 15526798PubMed |

Kirkegaard, K., Agerholm, I. E., and Ingerslev, H. J. (2012). Time-lapse monitoring as a tool for clinical embryo assessment. Hum. Reprod. 27, 1277–1285.
Time-lapse monitoring as a tool for clinical embryo assessment.Crossref | GoogleScholarGoogle Scholar | 22419744PubMed |

Koyama, K., Kang, S. S., Huang, W., Yanagawa, Y., Takahashi, Y., and Nagano, M. (2014). Aging-related changes in in vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation. J. Reprod. Dev. 60, 136–142.
Aging-related changes in in vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpslWmsLw%3D&md5=dc662de87c5a141f744c7e395aacb193CAS | 24492658PubMed |

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

Lane, M., and Gardner, D. (1997a). Nonessential amino acids and glutamine decrease the time of the first three cleavage divisions and increase compaction of mouse zygotes in vitro. J. Assist. Reprod. Genet. 14, 398–403.
Nonessential amino acids and glutamine decrease the time of the first three cleavage divisions and increase compaction of mouse zygotes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svjtFagsA%3D%3D&md5=4b23bcbd75b4efa055ac32c765e55d7cCAS | 9285325PubMed |

Lane, M., and Gardner, D. K. (1997b). Differential regulation of mouse embryo development and viability by amino acids. J. Reprod. Fertil. 109, 153–164.
Differential regulation of mouse embryo development and viability by amino acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gls78%3D&md5=713b097cab2f61406a4b92590ddf66d7CAS | 9068427PubMed |

Lechniak, D., Pers-Kamczyc, E., and Pawlak, P. (2008). Timing of the first zygotic cleavage as a marker of developmental potential of mammalian embryos. Reprod. Biol. 8, 23–42.
Timing of the first zygotic cleavage as a marker of developmental potential of mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 18432305PubMed |

Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P., and Boland, M. P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J. Reprod. Fertil. 117, 159–167.
Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlaltLo%3D&md5=e2d335849ccff9709d0bac8120a40199CAS | 10645257PubMed |

Lu, K. H., and Seidel, G. E. (2004). Effects of heparin and sperm concentration on cleavage and blastocyst development rates of bovine oocytes inseminated with flow cytometrically-sorted sperm. Theriogenology 62, 819–830.
Effects of heparin and sperm concentration on cleavage and blastocyst development rates of bovine oocytes inseminated with flow cytometrically-sorted sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1aisbo%3D&md5=9bfb76f544470be59bb18fc63e56fed1CAS | 15251233PubMed |

Lu, K. H., Cran, D. G., and Seidel, G. E. (1999). In vitro fertilization with flow-cytometrically-sorted bovine sperm. Theriogenology 52, 1393–1405.
In vitro fertilization with flow-cytometrically-sorted bovine sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFamuw%3D%3D&md5=8dc901bd042896fad305e3991145984aCAS | 10735084PubMed |

Miao, Y. L., Kikuchi, K., Sun, Q. Y., and Schatten, H. (2009). Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum. Reprod. Update 15, 573–585.
Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility.Crossref | GoogleScholarGoogle Scholar | 19429634PubMed |

Morgan, J. F., Morton, H. J., and Parker, R. C. (1950). Nutrition of animal cells in tissue culture; initial studies on a synthetic medium. Proc. Soc. Exp. Biol. Med. 73, 1–8.
Nutrition of animal cells in tissue culture; initial studies on a synthetic medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3cXit1ynsw%3D%3D&md5=e865a1738365819ace10e2224cd92983CAS | 15402504PubMed |

Nakao, H., and Nakatsuji, N. (1990). Effects of co-culture, medium components and gas phase on in vitro culture of in vitro matured and in vitro fertilized bovine embryos. Theriogenology 33, 591–600.
Effects of co-culture, medium components and gas phase on in vitro culture of in vitro matured and in vitro fertilized bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFGiug%3D%3D&md5=60fdfe081238a7b402285dc940760656CAS | 16726755PubMed |

Nedambale, T. L., Du, F., Xu, J., Chaubal, S. A., Dinnyes, A., Groen, W., Faber, D., Dobrinsky, J. R., Yang, X., and Tian, X. C. (2006). Prolonging bovine sperm–oocyte incubation in modified medium 199 improves embryo development rate and the viability of vitrified blastocysts. Theriogenology 66, 1951–1960.
Prolonging bovine sperm–oocyte incubation in modified medium 199 improves embryo development rate and the viability of vitrified blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28nlsF2isA%3D%3D&md5=67f5a81eb0b308807065273e67c30b11CAS | 16787658PubMed |

Norman, H. D., Hutchison, J. L., and Miller, R. H. (2010). Use of sexed semen and its effect on conception rate, calf sex, dystocia, and stillbirth of Holsteins in the United States. J. Dairy Sci. 93, 3880–3890.
Use of sexed semen and its effect on conception rate, calf sex, dystocia, and stillbirth of Holsteins in the United States.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1GgurzN&md5=b2030616d7a741bea4dbbfa9d770e149CAS | 20655457PubMed |

Ottolenghi, C., Uda, M., Hamatani, T., Crisponi, L., Garcia, J.-E., Ko, M., Pilia, G., Sforza, C., Schlessinger, D., and Forabosco, A. (2004). Aging of oocyte, ovary, and human reproduction. Ann. N. Y. Acad. Sci. 1034, 117–131.
Aging of oocyte, ovary, and human reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFKksrs%3D&md5=4cd7c72f0ebaac34ff068d8611f8f790CAS | 15731305PubMed |

Paria, B. C., and Dey, S. K. (1990). Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc. Natl Acad. Sci. USA 87, 4756–4760.
Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslWrsbw%3D&md5=34b281b8963de479a484d7f417215f2eCAS | 2352946PubMed |

Parinaud, J., Mieusset, R., Vieitez, G., Labal, B., and Richoilley, G. (1993). Influence of sperm parameters on embryo quality. Fertil. Steril. 60, 888–892.
| 1:STN:280:DyaK2c%2FjvFylug%3D%3D&md5=70a78e02eafb608f3ea40700d0031176CAS | 8224276PubMed |

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 | GoogleScholarGoogle Scholar | 24274411PubMed |

Parrish, J. J., Susko-Parrish, J. L., Leibfried-Rutledge, M. 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=3d8b66736c1341a2c3c3af334575f8c6CAS | 16726150PubMed |

Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=ce314afbc3c46d43a8a2669561972956CAS | 3408784PubMed |

Parrish, J. J., Susko-Parrish, J. L., and First, N. L. (1989). Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol. Reprod. 41, 683–699.
Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmvFOmsQ%3D%3D&md5=0dbe7a4b3b6d708b6a03a8e62c939554CAS | 2620077PubMed |

Parrish, J. J., Susko-Parrish, J. L., Uguz, C., and First, N. L. (1994). Differences in the role of cyclic adenosine 3′,5′-monophosphate during capacitation of bovine sperm by heparin or oviduct fluid. Biol. Reprod. 51, 1099–1108.
Differences in the role of cyclic adenosine 3′,5′-monophosphate during capacitation of bovine sperm by heparin or oviduct fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFOqt7g%3D&md5=d55d158312caf63c00fb3c4cbcd382e3CAS | 7888489PubMed |

Partridge, R. J., and Leese, H. J. (1996). Consumption of amino acids by bovine preimplantation embryos. Reprod. Fertil. Dev. 8, 945–950.
Consumption of amino acids by bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlGgtL4%3D&md5=58ba98ea20f761cc72d2409e2cc44c13CAS | 8896028PubMed |

Pieterse, M. C., Vos, P. L. A. M., Kruip, T. A. M., Wurth, Y. A., van Beneden, T. H., Willemse, A. H., and Taverne, M. A. M. (1991). Transvaginal ultrasound guided follicular aspiration of bovine oocytes. Theriogenology 35, 857–862.
Transvaginal ultrasound guided follicular aspiration of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFOitQ%3D%3D&md5=af99e5f6e1976f11286f6fa968c70e84CAS | 16726954PubMed |

Pinyopummintr, T., and Bavister, B. D. (1996a). Effects of amino acids on development in vitro of cleavage-stage bovine embryos into blastocysts. Reprod. Fertil. Dev. 8, 835–841.
Effects of amino acids on development in vitro of cleavage-stage bovine embryos into blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVKluro%3D&md5=6126c66bb49833a141ff4653e233bcccCAS | 8876042PubMed |

Pinyopummintr, T., and Bavister, B. D. (1996b). Energy substrate requirements for in vitro development of early cleavage-stage bovine embryos. Mol. Reprod. Dev. 44, 193–199.
Energy substrate requirements for in vitro development of early cleavage-stage bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsVCqtL8%3D&md5=3d9520da33a9b30eb7d673d81f01c936CAS | 9115717PubMed |

Pribenszky, C., Losonczi, E., Molnar, M., Lang, Z., Matyas, S., Rajczy, K., Molnar, K., Kovacs, P., Nagy, P., Conceicao, J., and Vajta, G. (2010). Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reprod. Biomed. Online 20, 371–379.
Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment.Crossref | GoogleScholarGoogle Scholar | 20089456PubMed |

Rasmussen, S., Block, J., Seidel, G. E., Brink, Z., McSweeney, K., Farin, P. W., Bonilla, L., and Hansen, P. J. (2013). Pregnancy rates of lactating cows after transfer of in vitro produced embryos using X-sorted sperm. Theriogenology 79, 453–461.
Pregnancy rates of lactating cows after transfer of in vitro produced embryos using X-sorted sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s7msVekug%3D%3D&md5=9503e61d49fd7e260772261066aa3373CAS | 23182749PubMed |

Rath, D., and Johnson, L. A. (2008). Application and commercialization of flow cytometrically sex-sorted semen. Reprod. Domest. Anim. 43, 338–346.
Application and commercialization of flow cytometrically sex-sorted semen.Crossref | GoogleScholarGoogle Scholar | 18638144PubMed |

Rath, D., Moench-Tegeder, G., Taylor, U., and Johnson, L. A. (2009). Improved quality of sex-sorted sperm: a prerequisite for wider commercial application. Theriogenology 71, 22–29.
Improved quality of sex-sorted sperm: a prerequisite for wider commercial application.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1CksQ%3D%3D&md5=2c016e98a97efa738012f87fec3689d7CAS | 18995893PubMed |

Rath, D., Barcikowski, S., de Graaf, S., Garrels, W., Grossfeld, R., Klein, S., Knabe, W., Knorr, C., Kues, W., Meyer, H., Michl, J., Moench-Tegeder, G., Rehbock, C., Taylor, U., and Washausen, S. (2013). Sex selection of sperm in farm animals: status report and developmental prospects. Reproduction 145, R15–R30.
Sex selection of sperm in farm animals: status report and developmental prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGisLk%3D&md5=d8d7429bf174c0d409100205ae0fcbe7CAS | 23148085PubMed |

Richter, K. S. (2008). The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr. Opin. Obstet. Gynecol. 20, 292–304.
The importance of growth factors for preimplantation embryo development and in-vitro culture.Crossref | GoogleScholarGoogle Scholar | 18460945PubMed |

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=00324f56c44b413ab24b73818dece8b1CAS | 11803560PubMed |

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.
| 1:CAS:528:DyaK2cXisVeitr4%3D&md5=b0e55cb738250c801a14b3c7c4088c2eCAS | 8157527PubMed |

Rutledge, J. J. (2001). Use of embryo transfer and IVF to bypass effects of heat stress. Theriogenology 55, 105–111.
Use of embryo transfer and IVF to bypass effects of heat stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7nslarsg%3D%3D&md5=c2787f6f84db68b0a7499081d1bc52e8CAS | 11198076PubMed |

Sartori, R., Souza, A. H., Guenther, J. N., Caraviello, D. Z., Geiger, L. N., Schenk, J. L., and Wiltbank, M. C. (2004). Fertilization rate and embryo quality in superovulated Holstein heifers artificially inseminated with X-sorted or unsorted sperm. Anim. Reprod. 1, 86–90.

Schenk, J. L., and Seidel, G. E. (2007). Pregnancy rates in cattle with cryopreserved sexed spermatozoa: effects of laser intensity, staining conditions and catalase. Soc. Reprod. Fertil. Suppl. 64, 165–177.
| 1:STN:280:DC%2BD2s3otlKjuw%3D%3D&md5=1bfaaedd4105a7e8646385a8d637e346CAS | 17491146PubMed |

Schenk, J. L., Suh, T. K., Cran, D. G., and Seidel, G. E. (1999). Cryopreservation of flow-sorted bovine spermatozoa. Theriogenology 52, 1375–1391.
Cryopreservation of flow-sorted bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFamug%3D%3D&md5=4482df9ee6aa399fe558c6271a35f94eCAS | 10735083PubMed |

Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
| 1:CAS:528:DC%2BC38XhtVKntb7P&md5=b185f20c8797a84cfbb62751d93dfd7cCAS | 22930834PubMed |

Seidel, G. E., and Garner, D. L. (2002). Current status of sexing mammalian spermatozoa. Reproduction 124, 733–743.
Current status of sexing mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVWitg%3D%3D&md5=cb17347ef0c0480682e93d08a1dbc850CAS | 12537000PubMed |

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFCqtr4%3D&md5=fd27b1a63fae5078c50b2b09d4ceb664CAS | 10456851PubMed |

Stewart, B. M., Block, J., Morelli, P., Navarette, A. E., Amstalden, M., Bonilla, L., Hansen, P. J., and Bilby, T. R. (2011). Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen. J. Dairy Sci. 94, 3437–3445.
Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFahs7o%3D&md5=b07855bc90c65e27c5b03b63fc48dc6eCAS | 21700029PubMed |

Stringfellow, D. A., Givens, M. D., and Society, I. E. T. (2010). ‘Manual of the International Embryo Transfer Society: A Procedural Guide and General Information for the Use of Embryo Transfer Technology Emphasizing Sanitary Procedures.’ (International Embryo Transfer Society: Savory, IL.)

Suh, T. K., Schenk, J. L., and Seidel, G. E. (2005). High pressure flow cytometric sorting damages sperm. Theriogenology 64, 1035–1048.
High pressure flow cytometric sorting damages sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvlvF2mtA%3D%3D&md5=7eb9ab560a81cf0a03e787921c155ff3CAS | 16125550PubMed |

Tervit, H. R., Whittingham, D. G., and Rowson, L. E. (1972). Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil. 30, 493–497.
Successful culture in vitro of sheep and cattle ova.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3s%2FgvFamug%3D%3D&md5=e4afd0254b5264c8e991d8413a92f57aCAS | 4672493PubMed |

Thompson, J. G., Simpson, A. C., Pugh, P. A., Donnelly, P. E., and Tervit, H. R. (1990). Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J. Reprod. Fertil. 89, 573–578.
Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlsV2nsLk%3D&md5=7a6bea1a0dee3d9d8015fe84c2714078CAS | 2401984PubMed |

Tsunoda, S., Kimura, N., and Fujii, J. (2013). Oxidative stress and redox regulation of gametogenesis, fertilization, and embryonic development. Reprod. Med. Biol. 13, 71–79.
Oxidative stress and redox regulation of gametogenesis, fertilization, and embryonic development.Crossref | GoogleScholarGoogle Scholar |

van Soom, A., Ysebaert, M. T., and de Kruif, A. (1997). Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol. Reprod. Dev. 47, 47–56.
Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislGnurw%3D&md5=ceb888510fbdbc72c69ba2db0d6b26fcCAS | 9110314PubMed |

Van Winkle, L. J. (2001). Amino acid transport regulation and early embryo development. Biol. Reprod. 64, 1–12.
Amino acid transport regulation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCntw%3D%3D&md5=6e1e60cefe3aaba9ef7c362b782241d0CAS | 11133652PubMed |

Visconti, P. E., Galantino-Homer, H., Moore, G. D., Bailey, J. L., Ning, X., Fornes, M., and Kopf, G. S. (1998). The molecular basis of sperm capacitation. J. Androl. 19, 242–248.
| 1:STN:280:DyaK1c3jtVKktQ%3D%3D&md5=6e871b99d9dceeed057f82c6e75323acCAS | 9570749PubMed |

Voelkel, S. A., and Hu, Y. X. (1992). Effect of gas atmosphere on the development of one-cell bovine embryos in two culture systems. Theriogenology 37, 1117–1131.
Effect of gas atmosphere on the development of one-cell bovine embryos in two culture systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xks1Gqtrg%3D&md5=3c6722b51e82d0d29886486c4cd67eebCAS | 16727109PubMed |

Vredenburgh-Wilberg, W. L., and Parrish, J. J. (1995). Intracellular pH of bovine sperm increases during capacitation. Mol. Reprod. Dev. 40, 490–502.
Intracellular pH of bovine sperm increases during capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvV2gsbc%3D&md5=f954b41fe6a200b6fdea5004554a2e44CAS | 7598914PubMed |

Wang, Q., and Sun, Q. Y. (2007). Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod. Fertil. Dev. 19, 1–12.
Evaluation of oocyte quality: morphological, cellular and molecular predictors.Crossref | GoogleScholarGoogle Scholar | 17389130PubMed |

Ward, F., Rizos, D., Corridan, D., Quinn, K., Boland, M., and Lonergan, P. (2001). Paternal influence on the time of first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo. Mol. Reprod. Dev. 60, 47–55.
Paternal influence on the time of first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFWisrY%3D&md5=61db522105037ce4f0ad5aea52c7e963CAS | 11550267PubMed |

Wheeler, M. B., Rutledge, J. J., Fischer-Brown, A., VanEtten, T., Malusky, S., and Beebe, D. J. (2006). Application of sexed semen technology to in vitro embryo production in cattle. Theriogenology 65, 219–227.
Application of sexed semen technology to in vitro embryo production in cattle.Crossref | GoogleScholarGoogle Scholar | 16263159PubMed |

Wilson, R. D., Weigel, K. A., Fricke, P. M., Rutledge, J. J., Leibfried-Rutledge, M. L., Matthews, D. L., and Schutzkus, V. R. (2005). In vitro production of holstein embryos using sex-sorted sperm and oocytes from selected cull cows. J. Dairy Sci. 88, 776–782.
In vitro production of holstein embryos using sex-sorted sperm and oocytes from selected cull cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFKrsw%3D%3D&md5=4102384ccebab412b5cf550069a47267CAS | 15653544PubMed |

Wilson, R. D., Fricke, P. M., Leibfried-Rutiedge, M. L., Rutledge, J. J., Penfield, C. M. S., and Weigel, K. A. (2006). In vitro production of bovine embryos using sex-sorted sperm. Theriogenology 65, 1007–1015.
In vitro production of bovine embryos using sex-sorted sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287jtFWiuw%3D%3D&md5=de201476f3c196007a1af7b171aa99ffCAS | 16122781PubMed |

Xu, J., Chaubal, S. A., and Du, F. (2009). Optimizing IVF with sexed sperm in cattle. Theriogenology 71, 39–47.
Optimizing IVF with sexed sperm in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1SmtA%3D%3D&md5=5c053e36580a62293d471682d7f36d71CAS | 18947864PubMed |

Yanagimachi, R. (2011). Mammalian sperm acrosome reaction: where does it begin before fertilization? Biol. Reprod. 85, 4–5.
Mammalian sperm acrosome reaction: where does it begin before fertilization?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOlsrw%3D&md5=f8e2917cf0823edffe4c4cb93c0addeaCAS | 21490244PubMed |

Zhang, M., Lu, K. H., and Seidel, G. E. (2003). Development of bovine embryos after in vitro fertilization of oocytes with flow cytometrically sorted, stained and unsorted sperm from different bulls. Theriogenology 60, 1657–1663.
Development of bovine embryos after in vitro fertilization of oocytes with flow cytometrically sorted, stained and unsorted sperm from different bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot12jsL8%3D&md5=2550ae9b3af44f30bde8378517740aafCAS | 14580648PubMed |