In vivo-derived horse blastocysts show transcriptional upregulation of developmentally important genes compared with in vitro-produced horse blastocysts
Katrien Smits A C , Karen Goossens B , Ann Van Soom A , Jan Govaere A , Maarten Hoogewijs A and Luc J. Peelman B
+ Author Affiliations
- Author Affiliations
A Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium.
B Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium.
C Corresponding author. Email: katrien.smits@ugent.be
Reproduction, Fertility and Development 23(2) 364-375 https://doi.org/10.1071/RD10124
Submitted: 2 June 2010 Accepted: 17 August 2010 Published: 4 January 2011
Abstract
In vitro-produced (IVP) equine blastocysts can give rise to successful pregnancies, but their morphology and developmental rate differ from those of in vivo-derived equine blastocysts. The aim of the present study was to evaluate this difference at the genetic level. Suppression subtractive hybridisation (SSH) was used to construct a cDNA library enriched for transcripts preferentially expressed in in vivo-derived equine blastocysts compared with IVP blastocysts. Of the 62 different genes identified in this way, six genes involved in embryonic development (BEX2, FABP3, HSP90AA1, MOBKL3, MCM7 and ODC) were selected to confirm this differential expression by reverse transcription–quantitative real-time polymerase chain reaction (RT-qPCR). Using RT-qPCR, five genes were confirmed to be significantly upregulated in in vivo-derived blastocysts (i.e. FABP3, HSP90AA1 (both P < 0.05), ODC, MOBKL3 and BEX2 (P < 0.005 for all three)), confirming the results of the SSH. There was no significant difference in MCM7 expression between IVP and in vivo-derived blastocysts. In conclusion, five genes that are transcriptionally upregulated in in vivo-derived equine blastocysts compared with IVP blastocysts have been identified. Because of their possible importance in embryonic development, the expression of these genes can be used as a marker to evaluate in vitro embryo production systems in the horse.
Additional keyword: gene expression.
References
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410.| Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVGmsA%3D%3D&md5=bcf83eb446ceb389aa2a0dcd3d07b71fCAS | 2231712PubMed |
Arai, Y., Funatsu, N., Numayama-Tsuruta, K., Nomura, T., Nakamura, S., and Osumi, N. (2005). Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J. Neurosci. 25, 9752–9761.
| Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1WqsrbI&md5=d01e4da8603d4bb0d55915b5adfc1a20CAS | 16237179PubMed |
Bensaude, O., Babinet, C., Morange, M., and Jacob, F. (1983). Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature 305, 331–333.
| Heat shock proteins, first major products of zygotic gene activity in mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsFGqtb0%3D&md5=1080657e0992103f3bbbb98fc8f819ceCAS | 6684733PubMed |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gurierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
| Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFymtbo%3D&md5=19b22bbb2f205001e61f233e89a23df2CAS |
Betteridge, K. J. (2007). Equine embryology: an inventory of unanswered questions. Theriogenology 68, S9–S21.
| Equine embryology: an inventory of unanswered questions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaiurc%3D&md5=411969f9da90e6428321b7d63509e11dCAS | 17532037PubMed |
Blanco, I. D. P., Devito, L. G., Ferreira, H. N., Araujo, G. H. M., Fernandes, C. B., Alvarenga, M. A., and Landim-Alvarenga, F. C. (2009). Aspiration of equine oocytes from immature follicles after treatment with equine pituitary extract (EPE) alone or in combination with hCG. Anim. Reprod. Sci. 114, 203–209.
| Aspiration of equine oocytes from immature follicles after treatment with equine pituitary extract (EPE) alone or in combination with hCG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12jsro%3D&md5=5478a95a9750f258ee5ae4cacf3671b1CAS | 18930362PubMed |
Blow, J. J., and Laskey, R. A. (1988). A role for the nuclear envelope in controlling DNA replication winthin the cell cycle. Nature 332, 546–548.
| A role for the nuclear envelope in controlling DNA replication winthin the cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitVSgsbw%3D&md5=98a5988d7825507de34a801ba450b2deCAS | 3357511PubMed |
Brown, A. L., and Kay, G. F. (1999). Bex1, a gene with increased expression in parthenogenetic embryos, is a member of a novel gene family on the mouse X chromosome. Hum. Mol. Genet. 8, 611–619.
| Bex1, a gene with increased expression in parthenogenetic embryos, is a member of a novel gene family on the mouse X chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlGnsro%3D&md5=3358e6d27dd2358e93ad5d84c4f1c7f9CAS | 10072429PubMed |
Chakraborty, A., Uechi, T., Higa, S., Torihara, H., and Kenmochi, N. (2009). Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response. PLoS ONE 4, e4152.
| Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response.Crossref | GoogleScholarGoogle Scholar | 19129914PubMed |
Chin, P. Y., Macpherson, A. M., Thompson, J. G., Lane, M., and Robertson, S. A. (2009). Stress response genes are suppressed in mouse preimplantation embryos by granulocyte–macrophage colony-stimulating factor (GM-CSF). Hum. Reprod. 24, 2997–3009.
| Stress response genes are suppressed in mouse preimplantation embryos by granulocyte–macrophage colony-stimulating factor (GM-CSF).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVKls7rJ&md5=0d765ad45cb6bf5984d1351fa55bfcb7CAS | 19737804PubMed |
Choi, Y. H., Harding, H. D., Hartman, D. L., Obermiller, A. D., Kurosaka, S., McLaughlin, K. J., and Hinrichs, K. (2009). The uterine environment modulates trophectodermal POU5F1 levels in equine blastocysts. Reproduction 138, 589–599.
| The uterine environment modulates trophectodermal POU5F1 levels in equine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrjK&md5=ab323fa2642f971d46b24ad6c5a30a36CAS | 19525365PubMed |
Christians, E., Campion, E., Thompson, E. M., and Renard, J. (1995). Expression of the HSP 70.1 gene, a landmark of early zygotic activity in the mouse embryo, is restricted to the first burst of transcription. Development 121, 113–122..
| 1:CAS:528:DyaK2MXjtlentLc%3D&md5=859f754c53ceecc9d273648ba1dfbcf2CAS | 7867493PubMed |
Colleoni, S., Barbacini, S., Necchi, D., Duchi, R., Lazzari, G., and Galli, C. (2007). Application of ovum pick-up, intracytoplasmic sperm injection and embryo culture in equine practice. In ‘Proceedings of the 53rd Annual Convention of the American Association of Equine Practitioners, Orlando, Florida’. (Eds American Association of Equine Practitioners.) pp. 554–559. (American Association of Equine Practitioners: Orlando, FL.)
Corcoran, D., Fair, T., Park, S., Rizos, D., Patel, O. V., Smith, G. W., Coussens, P. M., Ireland, J. J., Boland, M. P., Evans, A. C., and Lonergan, P. (2006). Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Reproduction 131, 651–660.
| Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtr8%3D&md5=12547053da663fc3011fff6759af19abCAS | 16595716PubMed |
Cui, X. S., and Kim, N. H. (2005). Polyamines inhibit apoptosis in porcine parthenotes developing in vitro. Mol. Reprod. Dev. 70, 471–477.
| Polyamines inhibit apoptosis in porcine parthenotes developing in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1Sls7s%3D&md5=fa636136b9dbf04822f137795daf9113CAS | 15685629PubMed |
Dell’Aquila, M. E., Caillaud, M., Maritato, F., Martoriati, A., Gérard, N., Aiudi, G., Minoia, P., and Goudet, G. (2004). Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus–oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis. Reprod. Biol. Endocrinol. 2, 44.
| Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus–oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis.Crossref | GoogleScholarGoogle Scholar | 15212696PubMed |
Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D., and Siebert, P. D. (1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl Acad. Sci. USA 93, 6025–6030.
| Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjs1Ojsbk%3D&md5=b19c537011e476599d757cd270dbfa7fCAS |
Donaldson, A. D., and Blow, J. J. (1999). The regulation of replication origin activation. Curr. Opin. Genet. Dev. 9, 62–68.
| The regulation of replication origin activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFSntLo%3D&md5=14bf46be8f58a1a03a14e52c14db7672CAS | 10072361PubMed |
Esfandiari, N., Falcone, T., Goldberg, J. M., Agarwal, A., and Sharma, K. R. (2007). Heat-shock proteins modulate the incidence of apoptosis and oxidative stress in preimplantation mouse embryos. Fertil. Steril. 87, 1214–1217.
| Heat-shock proteins modulate the incidence of apoptosis and oxidative stress in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslKgtbg%3D&md5=aac31af1056b7cbdde9b7c0d778e2fc3CAS | 17239868PubMed |
Fernández-Gonzalez, R., Moreira, P. N., Pérez-Crespo, M., Sánchez-Martín, M., Ramirez, M. A., Pericuesta, E., Bilbao, A., Bermejo-Alvarez, P., de Dios Hourcade, J., de Fonseca, F. R., and Gutiérrez-Adán, A. (2008). Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol. Reprod. 78, 761–772.
| Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring.Crossref | GoogleScholarGoogle Scholar | 18199884PubMed |
Fernández-González, R., de Dios Hourcade, J., López-Vidriero, I., Benguría, A., De Fonseca, F. R., and Gutiérrez-Adán, A. (2009). Analysis of gene transcription alterations at the blastocyst stage related to the long-term consequences of in vitro culture in mice. Reproduction 137, 271–283.
| Analysis of gene transcription alterations at the blastocyst stage related to the long-term consequences of in vitro culture in mice.Crossref | GoogleScholarGoogle Scholar | 19017722PubMed |
Galli, C., Colleoni, S., Duchi, R., Lagutina, I., and Lazzari, G. (2007). Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer. Anim. Reprod. Sci. 98, 39–55.
| Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Sksr4%3D&md5=e50c1ce5ff679d2385d18cbeb0aa5fa1CAS | 17101246PubMed |
Gao, H., Wu, G., Spencer, T. E., Johnson, G. A., and Bazer, F. W. (2009). Select nutrients in the ovine uterine lumen. V. Nitric oxide synthase, GTP cyclohydrolase, and ornithine decarboxylase in ovine uteri and peri-implantation conceptuses. Biol. Reprod. 81, 67–76.
| Select nutrients in the ovine uterine lumen. V. Nitric oxide synthase, GTP cyclohydrolase, and ornithine decarboxylase in ovine uteri and peri-implantation conceptuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslaru7Y%3D&md5=bdafece7f348e1a7c6972a8396306326CAS | 19246319PubMed |
Gentili, C., Tutolo, G., Zerega, B., Di Marco, E., Cancedda, R., and Cancedda, F. D. (2005). Acute phase lipocalin Ex-FABP is involved in heart development and cell survival. J. Cell. Physiol. 202, 683–689.
| Acute phase lipocalin Ex-FABP is involved in heart development and cell survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOntbo%3D&md5=4070c9982c838ea63777224e93625622CAS | 15455366PubMed |
Giritharan, G., Talbi, S., Donjacour, A., Di Sebastiano, F., Dobson, A. T., and Finaudo, P. F. (2007). Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction 134, 63–72.
| Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFGis74%3D&md5=72ec33f4af82b09fb1cd35ce0f402b50CAS | 17641089PubMed |
Goossens, K., Van Soom, A., Van Poucke, M., Vandaele, L., Vandesompele, J., Van Zeveren, A., and Peelman, L. (2007). Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Dev. Biol. 7, 64.
| Identification and expression analysis of genes associated with bovine blastocyst formation.Crossref | GoogleScholarGoogle Scholar | 17559642PubMed |
Hergovich, A., Cornils, H., and Hemmings, B. A. (2008). Mammalian NDR Protein kinases: from regulation to a role in centrosome duplication. Biochim. Biophys. Acta 1784, 3–15..
| 1:CAS:528:DC%2BD1cXptlequw%3D%3D&md5=0deebed0a22ff574f81203877dbc2961CAS | 17881309PubMed |
Hinrichs, K., Choi, Y. H., Walckenaer, B. E., Varner, D. D., and Hartman, D. L. (2007). In vitro-produced equine embryos: production of foals after transfer, assessement by differential staining and effect of medium calcium concentrations during culture. Theriogenology 68, 521–529.
| In vitro-produced equine embryos: production of foals after transfer, assessement by differential staining and effect of medium calcium concentrations during culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlWqurc%3D&md5=67874db96d4e7319de56470ae58a9e1aCAS | 17586036PubMed |
Kobayashi, S., Fujihara, Y., Mise, N., Kaseda, K., Abe, K., Ishino, F., and Okabe, M. (2010). The X-linked imprinted gene family FTH17 shows predominantly female expression following the two-cell stage in mouse embryos. Nucleic Acids Res. 38, 3672–3681.
| The X-linked imprinted gene family FTH17 shows predominantly female expression following the two-cell stage in mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVOit78%3D&md5=e1acfb48f4d1b374fe1d6e437deca62fCAS | 20185572PubMed |
Labib, K., Tercero, J. A., and Diffley, J. F. (2000). Uninterrupted MCM2–7 function required for DNA replication fork progression. Science 288, 1643–1647..
| 1:CAS:528:DC%2BD3cXjvVGru7k%3D&md5=3b89ba5d0bd0114b484ec046d1c9ada9CAS | 10834843PubMed |
Lazzari, G., Colleoni, S., Lagutina, I., Crotti, G., Turini, P., Tessaro, I., Brunetti, D., Duchi, R., and Galli, C. (2010). Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology 73, 748–757.
| Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7ot1aksw%3D%3D&md5=b67a0e02c2461c0449120311ea17647aCAS | 19726075PubMed |
Leroy, J. L. M. R., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–778.
| The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFeitr8%3D&md5=b0f7e6536db7b75d0e41d7a38ffd1f76CAS | 20007613PubMed |
Lopez-Garcia, C., Lopez-Contreras, A. J., Cremades, A., Castells, M. T., and Peñafiel, R. (2009). Transcriptomic analysis of polyamine-related genes and polyamine levels in placenta, yolk sac and fetus during the second half of mouse pregnancy. Placenta 30, 241–249.
| Transcriptomic analysis of polyamine-related genes and polyamine levels in placenta, yolk sac and fetus during the second half of mouse pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2kurk%3D&md5=0077d11d7947c63e87070faa39d39395CAS | 19131104PubMed |
McElroy, S. L., Kim, J. H., Kim, S., Jeong, Y. W., Lee, E. G., Park, S. M., Hossein, M. S., Koo, O. J., Abul Hashem, M. D., Jang, G., Kang, S. K., Lee, B. C., and Hwang, W. S. (2008). Effects of culture conditions and nuclear transfer protocols on blastocyst formation and mRNA expression in pre-implantation porcine embryos. Theriogenology 69, 416–425.
| Effects of culture conditions and nuclear transfer protocols on blastocyst formation and mRNA expression in pre-implantation porcine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVSmsro%3D&md5=17550751818303d33496cd83439cbde5CAS | 18055008PubMed |
Mohan, M., Hurst, A. G., and Malayer, J. R. (2004). Global gene expression analysis comparing bovine blastocysts flushed on Day 7 or produced in vitro. Mol. Reprod. Dev. 68, 288–298.
| Global gene expression analysis comparing bovine blastocysts flushed on Day 7 or produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1eqsLk%3D&md5=577171214e4744f7edd4d80f8409c37dCAS | 15112321PubMed |
Neuer, A., Mele, C., Liu, H. C., Rosenwaks, Z., and Witkin, S. S. (1998). Monoclonal antibodies to mammalian heat shock proteins impair mouse embryo development in vitro. Hum. Reprod. 13, 987–990.
| Monoclonal antibodies to mammalian heat shock proteins impair mouse embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3otVymug%3D%3D&md5=456c1c77ef83d8e4e3975d26cb0b108bCAS | 9619559PubMed |
Niemann, H., and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.
| Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvVyqug%3D%3D&md5=2b3884316b6428a88c212fb17b141839CAS | 10735059PubMed |
Niu, B. Y., Xiong, Y. Z., Li, F. E., Deng, C. Y., Jiang, C. W., Ye, L. Z., Wang, J., Ding, S. H., and Guo, W. H. (2006). Polymorphism of the pig pre-implantation protein 3 (prei3) gene and its association with litter size traits. S. Afr. J. Anim. Sci. 36, 209–214..
| 1:CAS:528:DC%2BD2sXmtlyqsg%3D%3D&md5=af1175c4076259e576e1ec659b745dbeCAS |
Panić, L., Tamarut, S., Sticker-Jantscheff, M., Barkić, M., Solter, D., Uzelac, M., Grabušić, K., and Volarević, S. (2006). Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol. Cell. Biol. 26, 8880–8891.
| Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation.Crossref | GoogleScholarGoogle Scholar | 17000767PubMed |
Pendeville, H., Carpino, N., Marine, J. C., Takahashi, Y., Muller, M., Martial, J. A., and Cleveland, J. L. (2001). The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol. Cell. Biol. 21, 6549–6558.
| The ornithine decarboxylase gene is essential for cell survival during early murine development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFGhsbw%3D&md5=723460eb2997b51a4528904d4801665cCAS | 11533243PubMed |
Pomar, F. J., Teerds, K. J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguilar, B., and Roelen, B. A. (2005). Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–2268.
| Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyrtbg%3D&md5=094730150a1dbf3ac7905dd14f5d3ec8CAS | 15826688PubMed |
Pretheeban, T., Gordon, M., Singh, R., Perera, R., and Rajamhendran, R. (2009). Differential mRNA expression in in vivo produced pre-implantation embryos of dairy heifers and mature cows. Mol. Reprod. Dev. 76, 1165–1172.
| Differential mRNA expression in in vivo produced pre-implantation embryos of dairy heifers and mature cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12msbvJ&md5=dfffd789153ec368c7b2fcd7c750deb5CAS | 19650113PubMed |
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=4610f8da484f53da6d62aa93b31345a6CAS | 19288542PubMed |
Rambags, B. P., Krijtenburg, P. J., Drie, H. F., Lazzari, G., Galli, C., Pearson, P. L., Colenbrander, B., and Stout, T. A. (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=7e40fc76ff7476771c529eb6d270f03eCAS | 15948165PubMed |
Rambags, B. P., van Tol, H. T., Van den Eng, M. M., Colenbrander, B., and Stout, T. A. (2008). Expression of progesterone and oestrogen receptors by early intrauterine equine conceptuses. Theriogenology 69, 366–375.
| Expression of progesterone and oestrogen receptors by early intrauterine equine conceptuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvV2hsA%3D%3D&md5=ea2b9c139eacac2acbcf61fe7f28a545CAS | 18037481PubMed |
Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., de la Fuente, J., and Gutiérrez-Adàn, A. (2002). Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol. Reprod. 66, 589–595.
| Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVeitLo%3D&md5=f4b57f6e819b94cb2e9eaeecdd8d0628CAS | 11870062PubMed |
Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386..
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=5890392ec27be7d27225017ba8e7a16bCAS | 10547847PubMed |
Ryu, S., and Driever, W. (2006). Minichromosome maintenance proteins as markers for proliferation zones during embryogenesis. Cell Cycle 5, 1140–1142..
| 1:CAS:528:DC%2BD28XnvFWqt7k%3D&md5=b7eadd03cf48f8ab1cfc82643d2c9280CAS | 16721065PubMed |
Scherzer, J., Fayrer-Hosken, R. A., Ray, L., Hurley, D. J., and Heusner, G. L. (2008). Advancements in large animal embryo transfer and related biotechnologies. Reprod. Domest. Anim. 43, 371–376.
| Advancements in large animal embryo transfer and related biotechnologies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1czgtFOhsQ%3D%3D&md5=1ccf42c70d4785bd11f01a567d3b3450CAS | 18226021PubMed |
Smits, K., Goossens, K., Van Soom, A., Govaere, J., Hoogewijs, M., Vanhaesebrouck, E., Galli, C., Colleoni, S., Vandesompele, J., and Peelman, L. (2009). Selection of reference genes for quantitative real-time PCR in equine in vivo and fresh and frozen–thawed in vitro blastocysts. BMC Res. Notes 2, 246.
| Selection of reference genes for quantitative real-time PCR in equine in vivo and fresh and frozen–thawed in vitro blastocysts.Crossref | GoogleScholarGoogle Scholar | 20003356PubMed |
Smits, K., Govaere, J., Hoogewijs, M., De Schauwer, C., Vanhaesebrouck, E., Van Poucke, M., Peelman, L. J., Van den Berg, M., Vullers, T., and Van Soom, A. (2010). Birth of the first ICSI foal in the Benelux. Vlaams Diergeneeskund. Tijds. 79, 134–138..
Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–58.
| Role of fatty acids in energy provision during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 19660080PubMed |
Swiech, L., Kisiel, K., Czolowska, R., Zientarski, M., and Borsuk, E. (2007). Accumulation and dynamics of proteins of the MCM family during mouse oogenesis and the first embryonic cell cycle. Int. J. Dev. Biol. 51, 283–295.
| Accumulation and dynamics of proteins of the MCM family during mouse oogenesis and the first embryonic cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1Crur0%3D&md5=1aedd4fe4a7364d9f6c0d04f5d7de013CAS | 17554680PubMed |
Temeles, G. L., Ram, P. T., Rothstein, J. L., and Schultz, R. M. (1994). Expression patterns of novel genes during mouse preimplantation embryogenesis. Mol. Reprod. Dev. 37, 121–129.
| Expression patterns of novel genes during mouse preimplantation embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt1Kgtbc%3D&md5=212415dd359ed00b71bd1fb07af02379CAS | 7545925PubMed |
Tremoleda, J. L., Stout, T. A., Lagutina, I., Lazzari, G., Bevers, M. M., Colenbrander, B., and Galli, C. (2003). Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biol. Reprod. 69, 1895–1906.
| Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCns7k%3D&md5=099ca974c068499e2c1fea9ae9104963CAS | 12904313PubMed |
Williams, J. W., Hawes, S. M., Patel, B., and Latham, K. E. (2002). Trophectoderm-specific expression of the X-linked Bex1/Rex3 gene in preimplantation stage mouse embryos. Mol. Reprod. Dev. 61, 281–287.
| Trophectoderm-specific expression of the X-linked Bex1/Rex3 gene in preimplantation stage mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFCgtL0%3D&md5=cf9d778862442b83f6b2ef9ff9852a2bCAS | 11835573PubMed |
Wilmeth, L. J., Shrestha, S., Montaño, G., Rashe, J., and Bradley, C. S. (2010). Mutual dependence of mob1 and the chromosomal passenger complex for localization during mitosis. Mol. Biol. Cell 21, 380–392.
| Mutual dependence of mob1 and the chromosomal passenger complex for localization during mitosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlCis7k%3D&md5=67e0e751002a751c50eb0c2663e4af62CAS | 19955215PubMed |
Wu, G., Bazer, F. W., Datta, S., Johnson, G. A., Li, P., Satterfield, M. C., and Spencer, T. E. (2008). Proline metabolism in the conceptus: implications for fetal growth and development. Amino Acids 35, 691–702.
| Proline metabolism in the conceptus: implications for fetal growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ais77O&md5=fbbe5f821e61de59d4ae5b1b87a0ff73CAS | 18330497PubMed |
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=2077e1e455edac4e7e3dc16f0fc255adCAS | 11175780PubMed |
Zhang, L. (2008). Adaptive evolution and frequent gene conversion in the brain expressed X-linked gene family in mammals. Biochem. Genet. 46, 293–311.
| Adaptive evolution and frequent gene conversion in the brain expressed X-linked gene family in mammals.Crossref | GoogleScholarGoogle Scholar | 18236150PubMed |
Zhou, Y., Ma, C., Karmouch, J., Katbi, H. A., and Liu, X. J. (2009). Antiapoptotic role for ornithine decarboxylase during oocyte maturation. Mol. Cell. Biol. 29, 1786–1795.
| Antiapoptotic role for ornithine decarboxylase during oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1Wqtrk%3D&md5=19a3a01d476044cd9d84194844d10a3eCAS | 19158268PubMed |
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406–3415.
| Mfold web server for nucleic acid folding and hybridization prediction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVWisr8%3D&md5=8efceaa1773d2c5d6dd9ab87df6ae435CAS | 12824337PubMed |
