Short- and long-term outcomes of the absence of protein during bovine blastocyst formation in vitro
A. Murillo-Ríos A , V. Maillo B , M. Muñoz A , A. Gutiérrez-Adán B , S. Carrocera A , D. Martín-González A , A. Fernandez-Buznego A and E. Gómez A C
+ Author Affiliations
- Author Affiliations
A Genética y Reproducción Animal, Centro de Biotecnología Animal, SERIDA, Camino de Rioseco 1225, 33394 Gijón, Spain.
B Departamento de Reproducción Animal, INIA, Ctra de la Coruña, km 5.9, 2804 Madrid, Spain.
C Corresponding author. Email: egomez@serida.org
Reproduction, Fertility and Development 29(6) 1064-1073 https://doi.org/10.1071/RD15485
Submitted: 22 November 2015 Accepted: 16 February 2016 Published: 6 April 2016
Abstract
In cattle, individual in vitro embryo culture after Day 6 benefits development, allowing non-invasive analysis of culture medium. However, undefined supplements in culture reduce analytical reliability. In this study we assayed the short- and long-term performance of embryos after bovine serum albumin removal over a 24-h period in individual culture. The absence of protein decreased embryo development and cell counts in the inner cell mass without affecting blastocyst sex ratio. However, the absence of protein produced embryos with an improved tendency to survive vitrification after 24 h in culture (P = 0.07). After transfer to recipients, birth rates of embryos that had been cultured with protein tended to decrease (P < 0.06) mostly as a result of a higher number of miscarriages (P < 0.013), reflecting lower viability. Birthweight, gestation length, height and thorax circumference did not differ between embryos cultured with or without protein. In fresh blastocysts cultured without protein, gene expression analysis showed higher abundance (P < 0.05) of insulin-like growth factor 2 receptor (IGF2R; imprinting) and activating transcription factor 4 (ATF4) and DNA-damage-inducible transcript 3 (DDIT3; endoplasmic reticulum stress) transcripts, with DNA methyltransferase 3A (DNMT3A; imprinting) tending to increase (P = 0.062). However, in hatched blastocysts that survived cryopreservation, glucose-6-phosphate dehydrogenase (G6PD) was overexpressed in embryos cultured without protein (P < 0.01). The absence of protein results in fewer blastocysts but improved long-term viability after cryopreservation.
Additional keywords: embryo, gene expression, pregnancy.
References
Bebbere, D., Bauersachs, S., Fürst, R. W., Reichenbach, H. D., Reichenbach, M., Medugorac, I., Ulbrich, S. E., Wolf, E., Ledda, S., and Hiendleder, S. (2013). Tissue-specific and minor inter-individual variation in imprinting of IGF2R is a common feature of Bos taurus concepti and not correlated with fetal weight. PLoS One 8, e59564.| Tissue-specific and minor inter-individual variation in imprinting of IGF2R is a common feature of Bos taurus concepti and not correlated with fetal weight.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlSnu7w%3D&md5=7948fa7feee03b721d16f312662ae891CAS | 23593146PubMed |
Bermejo-Álvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
| Epigenetic differences between male and female bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 17986520PubMed |
Caamaño, J. N., Gómez, E., Trigal, B., Muñoz, M., Carrocera, S., Martín, D., and Díez, C. (2015). Survival of vitrified in vitro-produced bovine embryos after a one-step warming in-straw cryoprotectant dilution procedure. Theriogenology 83, 881–890.
| Survival of vitrified in vitro-produced bovine embryos after a one-step warming in-straw cryoprotectant dilution procedure.Crossref | GoogleScholarGoogle Scholar | 25542458PubMed |
Castaneda, C. A., Kaye, P., Pantaleon, M., Phillips, N., Norman, S., Fry, R., and D’Occhio, M. J. (2013). Lipid content, active mitochondria and brilliant cresyl blue staining in bovine oocytes. Theriogenology 79, 417–422.
| Lipid content, active mitochondria and brilliant cresyl blue staining in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslGjsb3K&md5=78d716f586c92916ff409e66115e4bcaCAS | 23199746PubMed |
Constant, F., Guillomot, M., Heyman, Y., Vignon, X., Laigre, P., Servely, J. L., Renard, J. P., and Chavatte-Palmer, P. (2006). Large offspring or large placenta syndrome? Morphometric analysis of late gestation bovine placentomes from somatic nuclear transfer pregnancies complicated by hydrallantois. Biol. Reprod. 75, 122–130.
| Large offspring or large placenta syndrome? Morphometric analysis of late gestation bovine placentomes from somatic nuclear transfer pregnancies complicated by hydrallantois.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmtlyisbs%3D&md5=021b25e0c2999d94d9d08ad9246c2f9eCAS | 16571872PubMed |
Duque, P., Hidalgo, C. O., Gómez, E., Pintado, B., Facal, N., and Díez, C. (2003). Macromolecular source as dependent on osmotic pressure and water source: effects on bovine in vitro embryo development and quality. Reprod. Nutr. Dev. 43, 487–496.
| Macromolecular source as dependent on osmotic pressure and water source: effects on bovine in vitro embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 15141434PubMed |
Francis, G. L. (2010). Albumin and mammalian cell culture: implications for biotechnology applications. Cytotechnology 62, 1–16.
| Albumin and mammalian cell culture: implications for biotechnology applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltlyrtbY%3D&md5=238b4245296b0b377a17679edf56cc55CAS | 20373019PubMed |
Gómez, E., Royo, L. J., Duque, P., Carneiro, G., Hidalgo, C., Goyache, F., Lorenzo, P. L., Alvarez, I., Facal, N., and Díez, C. (2003). 9-cis-retinoic acid during in vitro maturation improves development of the bovine oocyte and increases midkine but not IGF-I expression in cumulus–granulosa cells. Mol. Reprod. Dev. 66, 247–255.
| 9-cis-retinoic acid during in vitro maturation improves development of the bovine oocyte and increases midkine but not IGF-I expression in cumulus–granulosa cells.Crossref | GoogleScholarGoogle Scholar | 14502603PubMed |
Gómez, E., Rodríguez, A., Goyache, F., Díez, C., Royo, J. L., Moreira, P. N., Caamaño, J. N., Morán, E., and Gutiérrez-Adán, A. (2004). Retinoid-dependent mRNA expression and poly-(A) contents in bovine oocytes meiotically arrested and/or matured in vitro. Mol. Reprod. Dev. 69, 101–108.
| Retinoid-dependent mRNA expression and poly-(A) contents in bovine oocytes meiotically arrested and/or matured in vitro.Crossref | GoogleScholarGoogle Scholar | 15278910PubMed |
Gómez, E., Rodríguez, A., Muñoz, M., Caamaño, J. N., Hidalgo, C. O., Morán, E., Facal, N., and Díez, C. (2008a). Serum-free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification. Theriogenology 69, 1013–1021.
| Serum-free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification.Crossref | GoogleScholarGoogle Scholar | 18358521PubMed |
Gómez, E., Rodríguez, A., Muñoz, M., Caamaño, J. N., Carrocera, S., Martín, D., Facal, N., and Díez, C. (2008b). Development and quality of bovine morulae cultured in serum-free medium with specific retinoid receptor agonists. Reprod. Fertil. Dev. 20, 884–891.
| Development and quality of bovine morulae cultured in serum-free medium with specific retinoid receptor agonists.Crossref | GoogleScholarGoogle Scholar | 19007552PubMed |
Gómez, E., Correia-Álvarez, E., Caamaño, J. N., Díez, C., Carrocera, S., Peynot, N., Martín, D., Giraud-Delville, C., Duranthon, V., Sandra, O., and Muñoz, M. (2014). Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture. Reproduction 148, 353–365.
| Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture.Crossref | GoogleScholarGoogle Scholar | 25009202PubMed |
Goovaerts, I. G., Leroy, J. L., Jorssen, E. P., and Bols, P. E. (2010). Non-invasive bovine oocyte quality assessment: possibilities of a single oocyte culture. Theriogenology 74, 1509–1520.
| Non-invasive bovine oocyte quality assessment: possibilities of a single oocyte culture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbjtFSntA%3D%3D&md5=5c1f011a82835bf1f608349ecaf89b87CAS | 20708251PubMed |
Gutiérrez, J. P., Goyache, F., Fernández, I., Álvarez, I., and Royo, L. J. (2007). Genetic relationships among calving ease, calving interval, birth weight and weaning weight in the Asturiana de los Valles beef cattle breed. J. Anim. Sci. 85, 69–75.
| Genetic relationships among calving ease, calving interval, birth weight and weaning weight in the Asturiana de los Valles beef cattle breed.Crossref | GoogleScholarGoogle Scholar | 17179541PubMed |
Gutiérrez-Adán, A., Oter, M., Martínez-Madrid, B., Pintado, B., and De La Fuente, J. (2000). Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage. Mol. Reprod. Dev. 55, 146–151.
| Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 10618653PubMed |
Gutiérrez-Adán, A., Rizos, D., Fair, T., Moreira, P. N., Pintado, B., de la Fuente, J., Boland, M. P., and Lonergan, P. (2004). Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol. Reprod. Dev. 68, 441–448.
| Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 15236328PubMed |
Hasler, J. F. (2000). In vitro production of cattle embryos: problems with pregnancies and parturition. Hum. Reprod. 15, 47–58.
| In vitro production of cattle embryos: problems with pregnancies and parturition.Crossref | GoogleScholarGoogle Scholar | 11263537PubMed |
Havlicek, V., Kuzmany, A., Cseh, S., Brem, G., and Besenfelder, U. (2010). The effect of long-term in vivo culture in bovine oviduct and uterus on the development and cryo-tolerance of in vitro-produced bovine embryos. Reprod. Domest. Anim. 45, 832–837.
| 1:STN:280:DC%2BC3MzosFeqtA%3D%3D&md5=777a304e662ef250fd620ecfc5c883bbCAS | 19416481PubMed |
Heyman, Y., Chavatte-Palmer, P., LeBourhis, D., Camous, S., Vignon, X., and Renard, J. P. (2002). Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol. Reprod. 66, 6–13.
| Frequency and occurrence of late-gestation losses from cattle cloned embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1ymug%3D%3D&md5=6aedfbb55409aceba11927f9299dea10CAS | 11751257PubMed |
Hidalgo, C. O., Díez, C., Duque, P., Facal, N., and Gómez, E. (2003). Pregnancies and improved early embryonic development with bovine oocytes matured in vitro with 9-cis-retinoic acid. Reproduction 125, 409–416.
| Pregnancies and improved early embryonic development with bovine oocytes matured in vitro with 9-cis-retinoic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVWqtb8%3D&md5=2b0022b13ad3b272873fb7e6558624f7CAS | 12611604PubMed |
Hidalgo, C. O., Gómez, E., Prieto, L., Duque, P., Goyache, F., Fernández, L., Fernández, I., Facal, N., and Díez, C. (2004). Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer. Theriogenology 62, 664–676.
| Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltF2rsrc%3D&md5=f799bf74cb7a2a0ec85356252f7d9526CAS | 15226021PubMed |
Hidalgo, C., Díez, C., Duque, P., Prendes, J. M., Rodríguez, A., Goyache, F., Fernández, I., Facal, N., Ikeda, S., Alonso-Montes, C., and Gómez, E. (2005). Oocytes recovered from cows treated with retinol become unviable as blastocysts produced in vitro. Reproduction 129, 411–421.
| Oocytes recovered from cows treated with retinol become unviable as blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1ertLg%3D&md5=95c4a5e5cdc1d5f45f7948af6be1c5bcCAS | 15798016PubMed |
Hughes, J., Kwong, W. Y., Li, D., Salter, A. M., Lea, R. G., and Sinclair, K. D. (2011). Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty-acid metabolism. Reproduction 141, 105–118.
| Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty-acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7k%3D&md5=9d6a93b5a4108a6d6cdcc36bee8d0c91CAS | 21045166PubMed |
Iwasaki, S., Yoshiba, N., Ushijima, H., Watanabe, S., and Nakahara, T. (1990). Morphology and proportion of inner cell mass of bovine blastocysts fertilised in vitro and in vivo. J. Reprod. Fertil. 90, 279–284.
| Morphology and proportion of inner cell mass of bovine blastocysts fertilised in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M%2FjvFSlsw%3D%3D&md5=03a1e2d3ccac6a42161d0261867118c4CAS | 2231548PubMed |
Kimura, K., Spate, L. D., Green, M. P., and Roberts, R. M. (2004). Effects of oxidative stress and inhibitors of the pentose phosphate pathway on sexually dimorphic production of IFN-tau by bovine blastocysts. Mol. Reprod. Dev. 68, 88–95.
| Effects of oxidative stress and inhibitors of the pentose phosphate pathway on sexually dimorphic production of IFN-tau by bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFyrsr0%3D&md5=5d24deebf2b21541f434e4438a47d925CAS | 15039952PubMed |
Kimura, K., Spate, L. D., Green, M. P., and Roberts, R. M. (2005). Effects of D-glucose concentration, D-fructose and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol. Reprod. Dev. 72, 201–207.
| Effects of D-glucose concentration, D-fructose and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1ygu7c%3D&md5=2add478cdef37a7dfed9f2cc4ce74f5fCAS | 15968626PubMed |
Krisher, R. L., Lane, M., and Bavister, B. D. (1999). Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media. Biol. Reprod. 60, 1345–1352.
| Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVejtr4%3D&md5=c814756d4d347911a9a4f567c23653a2CAS | 10330091PubMed |
Krisher, R. L., Schoolcraft, W. B., and Katz-Jaffe, M. G. (2015). Omics as a window to view embryo viability. Fertil. Steril. 103, 333–341.
| Omics as a window to view embryo viability.Crossref | GoogleScholarGoogle Scholar | 25639968PubMed |
Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
| Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsV2js7Y%3D&md5=c3dca518184dc25602aaf4edcee2ee75CAS | 12193383PubMed |
Leese, H. J. (2002). Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. BioEssays 24, 845–849.
| Quiet please, do not disturb: a hypothesis of embryo metabolism and viability.Crossref | GoogleScholarGoogle Scholar | 12210521PubMed |
Leese, H. J., Baumann, C. G., Brison, D. R., McEvoy, T. G., and Sturmey, R. G. (2008). Metabolism of the viable mammalian embryo: quietness revisited. Mol. Hum. Reprod. 14, 667–672.
| Metabolism of the viable mammalian embryo: quietness revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gsA%3D%3D&md5=80f6db2afafa8040cce9666a18fba40cCAS | 19019836PubMed |
Leroy, J. L., Valckx, S. D., Jordaens, L., De Bie, J., Desmet, K. L., Van Hoeck, V., Britt, J. H., Marei, W. F., and Bols, P. E. (2015). Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod. Fertil. Dev , .
| Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model.Crossref | GoogleScholarGoogle Scholar | 25690396PubMed |
Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q., and Hansen, P. J. (2009). Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
| Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCht7bF&md5=b305084c703fa07cf75a98da47489422CAS | 19797121PubMed |
Lim, K. T., Jang, G., Ko, K. H., Lee, W. W., Park, H. J., Kim, J. J., Lee, S. H., Hwang, W. S., Lee, B. C., and Kang, S. K. (2007). Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media. Theriogenology 67, 293–302.
| Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media.Crossref | GoogleScholarGoogle Scholar | 16979228PubMed |
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-fertilisation culture environment on the incidence of chromosome aberrations in bovine blastocysts. Biol. Reprod. 71, 1096–1100.
| Effect of the post-fertilisation culture environment on the incidence of chromosome aberrations in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7w%3D&md5=0aa28b8c9fb8716bf3c8d1a21f8269b6CAS | 15189826PubMed |
Mohammadi-Sangcheshmeh, A., Veshkini, A., Hajarizadeh, A., Jamshidi-Adegani, F., Zhandi, M., Abazari-Kia, A. H., Cinar, M. U., Soleimani, M., and Gastal, E. L. (2014). Association of glucose-6-phosphate dehydrogenase activity with oocyte cytoplasmic lipid content, developmental competence and expression of candidate genes in a sheep model. J. Assist. Reprod. Genet. 31, 1089–1098.
| Association of glucose-6-phosphate dehydrogenase activity with oocyte cytoplasmic lipid content, developmental competence and expression of candidate genes in a sheep model.Crossref | GoogleScholarGoogle Scholar | 24913026PubMed |
Muñoz, M., Corrales, F. J., Caamaño, J. N., Díez, C., Trigal, B., Mora, M. I., Martín, D., Carrocera, S., and Gómez, E. (2012). Proteome of the early embryo–maternal dialogue in the cattle uterus. J. Proteome Res. 11, 751–766.
| Proteome of the early embryo–maternal dialogue in the cattle uterus.Crossref | GoogleScholarGoogle Scholar | 22148898PubMed |
Muñoz, M., Uyar, A., Correia, E., Díez, C., Fernandez-Gonzalez, A., Caamaño, J. N., Martínez-Bello, D., Trigal, B., Humblot, P., Ponsart, C., Guyader-Joly, C., Carrocera, S., Martin, D., Marquant Le Guienne, B., Seli, E., and Gomez, E. (2014a). Prediction of pregnancy viability in bovine in vitro-produced embryos and recipient plasma with Fourier transform infrared spectroscopy. J. Dairy Sci. 97, 5497–5507.
| Prediction of pregnancy viability in bovine in vitro-produced embryos and recipient plasma with Fourier transform infrared spectroscopy.Crossref | GoogleScholarGoogle Scholar | 24997663PubMed |
Muñoz, M., Uyar, A., Correia, E., Ponsart, C., Guyader-Joly, C., Martínez-Bello, D., Marquant-Le Guienne, B., Fernandez-Gonzalez, A., Díez, C., Caamaño, J. N., Trigal, B., Humblot, P., Carrocera, S., Martin, D., Seli, E., and Gomez, E. (2014b). Metabolomic prediction of pregnancy viability in superovulated cattle embryos and recipients with Fourier transform infrared spectroscopy. BioMed Res. Int. 2014, 608579.
| Metabolomic prediction of pregnancy viability in superovulated cattle embryos and recipients with Fourier transform infrared spectroscopy.Crossref | GoogleScholarGoogle Scholar | 24834432PubMed |
Muñoz, M., Uyar, A., Correia, E., Díez, C., Fernandez-Gonzalez, A., Caamaño, J. N., Trigal, B., Carrocera, S., Seli, E., and Gómez, E. (2014c). Non-invasive assessment of embryonic sex in cattle by metabolic fingerprinting of in vitro culture medium. Metabolomics 10, 443–451.
| Non-invasive assessment of embryonic sex in cattle by metabolic fingerprinting of in vitro culture medium.Crossref | GoogleScholarGoogle Scholar |
Orsi, N. M., and Leese, H. J. (2004). Amino-acid metabolism of preimplantation bovine embryos cultured with bovine serum albumin or polyvinyl alcohol. Theriogenology 61, 561–572.
| Amino-acid metabolism of preimplantation bovine embryos cultured with bovine serum albumin or polyvinyl alcohol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1OksLc%3D&md5=55c37aea8b250e565dfbf720cdea2247CAS | 14662152PubMed |
Pérez-Crespo, M., Ramírez, M. A., Fernández-González, R., Rizos, D., Lonergan, P., Pintado, B., and Gutiérrez-Adán, A. (2005). Differential sensitivity of male and female mouse embryos to oxidative induced heat stress is mediated by glucose-6-phosphate dehydrogenase gene expression. Mol. Reprod. Dev. 72, 502–510.
| Differential sensitivity of male and female mouse embryos to oxidative induced heat stress is mediated by glucose-6-phosphate dehydrogenase gene expression.Crossref | GoogleScholarGoogle Scholar | 16149081PubMed |
Puscheck, E. E., Awonuga, A. O., Yang, Y., Jiang, Z., and Rappolee, D. A. (2015). Molecular biology of the stress response in the early embryo and its stem cells. Adv. Exp. Med. Biol. 843, 77–128.
| Molecular biology of the stress response in the early embryo and its stem cells.Crossref | GoogleScholarGoogle Scholar | 25956296PubMed |
Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilisation 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, fertilisation 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=fd530554a4e416cc604ed66ebc4922a4CAS | 11803560PubMed |
Rodríguez, A., De Frutos, C., Díez, C., Caamaño, J. N., Facal, N., Duque, P., García-Ochoa, C., and Gómez, E. (2007). Effects of human versus mouse leukaemia inhibitory factor on the in vitro development of bovine embryos. Theriogenology 67, 1092–1095.
| Effects of human versus mouse leukaemia inhibitory factor on the in vitro development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 17210172PubMed |
Romek, M., Gajda, B., Krzysztofowicz, E., Kepczyński, M., and Smorag, Z. (2011). Lipid content in pig blastocysts cultured in the presence or absence of protein and vitamin E or phenazine ethosulfate. Folia Biol. (Krakow) 59, 45–52.
| Lipid content in pig blastocysts cultured in the presence or absence of protein and vitamin E or phenazine ethosulfate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVChu7o%3D&md5=2c8ef669a2c3ecdd32a47316e832ad1aCAS | 21614967PubMed |
Schmittgen, T. D., and Livak, K. J. (2008). Analysing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
| Analysing real-time PCR data by the comparative C(T) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=c9af4cd1fb90fdc7f3a7e145ccaafe84CAS | 18546601PubMed |
Smith, L. C., Therrien, J., Filion, F., Bressan, F., and Meirelles, F. V. (2015). Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R. Front. Genet. 6, 58.
| Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R.Crossref | GoogleScholarGoogle Scholar | 25763013PubMed |
Song, B. S., Kim, J. S., Yoon, S. B., Lee, K. S., Koo, D. B., Lee, D. S., Choo, Y. K., Huh, J. W., Lee, S. R., Kim, S. U., Kim, S. H., Kim, H. M., and Chang, K. T. (2011). Inactivated Sendai virus-mediated fusion improves early development of cloned bovine embryos by avoiding endoplasmic reticulum-stress-associated apoptosis. Reprod. Fertil. Dev. 23, 826–836.
| Inactivated Sendai virus-mediated fusion improves early development of cloned bovine embryos by avoiding endoplasmic reticulum-stress-associated apoptosis.Crossref | GoogleScholarGoogle Scholar | 21791184PubMed |
Song, B. S., Yoon, S. B., Kim, J. S., Sim, B. W., Kim, Y. H., Cha, J. J., Choi, S. A., Min, H. K., Lee, Y., Huh, J. W., Lee, S. R., Kim, S. H., Koo, D. B., Choo, Y. K., Kim, H. M., Kim, S. U., and Chang, K. T. (2012). Induction of autophagy promotes preattachment development of bovine embryos by reducing endoplasmic reticulum stress. Biol. Reprod. 87, 8.
| Induction of autophagy promotes preattachment development of bovine embryos by reducing endoplasmic reticulum stress.Crossref | GoogleScholarGoogle Scholar | 22539678PubMed |
Stringfellow, D. A. (2010) Recommendations for the sanitary handling of in vivo-derived embryos. In ‘Manual of the International Embryo Transfer Society’. 4th edn. (Eds D. A. Stringfellow and M. D. Givens.) pp. 65–68. (International Embryo Transfer Society: Savoy, IL, USA.)
Sturmey, R. G., Bermejo-Alvarez, P., Gutierrez-Adan, A., Rizos, D., Leese, H. J., and Lonergan, P. (2010). Amino-acid metabolism of bovine blastocysts: a biomarker of sex and viability. Mol. Reprod. Dev. 77, 285–296.
| Amino-acid metabolism of bovine blastocysts: a biomarker of sex and viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotFSmuw%3D%3D&md5=d96365d54029f627f491dfde70198c8cCAS | 20058302PubMed |
Thompson, J. G., Sherman, A. N., Allen, N. W., McGowan, L. T., and Tervit, H. R. (1998). Total protein content and protein synthesis within pre-elongation stage bovine embryos. Mol. Reprod. Dev. 50, 139–145.
| Total protein content and protein synthesis within pre-elongation stage bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislWks7k%3D&md5=18b73b4168929b0628c0f54179f5f988CAS | 9590529PubMed |
Trigal, B., Gómez, E., Caamaño, J. N., Muñoz, M., Moreno, J., Carrocera, S., Martín, D., and Diez, C. (2012a). In vitro and in vivo quality of bovine embryos in vitro produced with sex-sorted spermatozoa. Theriogenology 78, 1465–1475.
| In vitro and in vivo quality of bovine embryos in vitro produced with sex-sorted spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bhs1enuw%3D%3D&md5=30df66fce7ec97d991a75daebb66b75aCAS | 22925642PubMed |
Trigal, B., Gómez, E., Díez, C., Caamaño, J. N., Muñoz, M., Moreno, J. F., Carrocera, S., Martín, D., Goyache, F., and Álvarez, I. (2012b). Comparative study of PCR-sexing procedures using bovine embryos fertilised with sex-sorted spermatozoa. Span. J. Agric. Res. 10, 353–359.
| Comparative study of PCR-sexing procedures using bovine embryos fertilised with sex-sorted spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Vajta, G., Holm, P., Kuwayama, M., Booth, P. J., Jacobsen, H., Greve, T., and Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–58.
| Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVGrs7g%3D&md5=e2e80288377ae9cc2b9febc9b6fec070CAS | 9712317PubMed |
van Wagtendonk-de Leeuw, A. M., Mullaart, E., de Roos, A. P., Merton, J. S., den Daas, J. H., Kemp, B., and de Ruigh, L. (2000). Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575–597.
| Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFahtA%3D%3D&md5=f6a087098732d6e3a5b6aae8cb499b79CAS | 10735051PubMed |
Watkins, A. J., Ursell, E., Panton, R., Papenbrock, T., Hollis, L., Cunningham, C., Wilkins, A., Perry, V. H., Sheth, B., Kwong, W. Y., Eckert, J. J., Wild, A. E., Hanson, M. A., Osmond, C., and Fleming, T. P. (2008). Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult-onset disease. Biol. Reprod. 78, 299–306.
| Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult-onset disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Kru7c%3D&md5=b825de8dd6802e8c48ab819ae98b21dfCAS | 17989357PubMed |
Yang, L., Yu, W., Yan, W. L., and Peng, G. (2013). Expression of insulin-like growth factor 2 receptor (IGF2R), leptin receptor (LEPR) and serum- and glucocorticoid-regulated kinase 1 (SGK1) mRNA in human and bovine pregnancies. Reprod. Fertil. Dev. 25, 205.
| Expression of insulin-like growth factor 2 receptor (IGF2R), leptin receptor (LEPR) and serum- and glucocorticoid-regulated kinase 1 (SGK1) mRNA in human and bovine pregnancies.Crossref | GoogleScholarGoogle Scholar |
Yoon, S. B., Choi, S. A., Sim, B. W., Kim, J. S., Mun, S. E., Jeong, P. S., Yang, H. J., Lee, Y., Park, Y. H., Song, B. S., Kim, Y. H., Jeong, K. J., Huh, J. W., Lee, S. R., Kim, S. U., and Chang, K. T. (2014). Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress. Biol. Reprod. 90, 104.
| Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress.Crossref | GoogleScholarGoogle Scholar | 24695629PubMed |
Yotsushima, K., Sakaguchi, M., Shimizu, M., Okimura, T., and Izaike, Y. (2004). Effects of fatty acid-free bovine serum albumin and fetal calf serum supplementing repair cultures on pre- and post-warm viability of biopsied bovine embryos produced in vitro. J. Reprod. Dev. 50, 471–476.
| Effects of fatty acid-free bovine serum albumin and fetal calf serum supplementing repair cultures on pre- and post-warm viability of biopsied bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvFant7g%3D&md5=ada46a674ab488116050e309ddcb793aCAS | 15329479PubMed |
Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
| Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFGktL8%3D&md5=eb2f860a259dfd94c8b31fde3d21914aCAS | 11175780PubMed |
