Gene expression analysis of bovine blastocysts produced by parthenogenic activation or fertilisation
Rémi Labrecque A and Marc-André Sirard A B
+ Author Affiliations
- Author Affiliations
A Centre de Recherche en Biologie de la Reproduction, Université Laval, Québec, QC, Canada.
B Corresponding author. Email: marc-andre.sirard@fsaa.ulaval.ca
Reproduction, Fertility and Development 23(4) 591-602 https://doi.org/10.1071/RD10243
Submitted: 26 September 2010 Accepted: 17 December 2010 Published: 3 May 2011
Abstract
The processes underlying the very first moments of embryonic development are still not well characterised in mammals. To better define the kinetics of events taking place following fertilisation, it would be best to have perfect synchronisation of sperm entry. With fertilisation occurring during a time interval of 6 to 12 h in the same group of fertilised oocytes, this causes a major variation in the time of activation of embryonic development. Bovine parthenogenesis could potentially result in better synchronisation and, if so, would offer a better model for studying developmental competence. In the present study, bovine oocytes were either parthenogenetically activated or fertilised and cultured in vitro for 7 days. Gene expression analysis for those two groups of embryos at early and expanded stages was performed with BlueChip, a customised 2000-cDNA array developed in our laboratory and enriched in clones from various stages of bovine embryo development. The microarray data analysis revealed that only a few genes were differentially expressed, showing the relative similarity between those two kinds of embryos. Nevertheless, the fact that we obtained a similar diversity of developmental stages with parthenotes suggests that synchronisation is more oocyte-specific than sperm entry-time related. We then analysed our data with Ingenuity pathway analysis. Networks of genes involved in blastocyst implantation but also previous stages of embryo development, like maternal-to-embryonic transition, were identified. This new information allows us to better understand the regulatory mechanisms of embryonic development associated with embryo status.
Additional keywords: embryo, microarray, parthenote.
References
Aflalo, E., Sod-Moriah, U., Potashnik, G., and Har-Vardi, I. (2005). Expression of plasminogen activators in preimplantation rat embryos developed in vivo and in vitro. Reprod. Biol. Endocrinol. 3, 7.| Expression of plasminogen activators in preimplantation rat embryos developed in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 15703084PubMed |
Blasi, F., Vassalli, J. D., and Dano, K. (1987). Urokinase-type plasminogen activator: proenzyme, receptor and inhibitors. J. Cell Biol. 104, 801–804.
| Urokinase-type plasminogen activator: proenzyme, receptor and inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhvFWmtLk%3D&md5=c3d6f6fa0caae340045a32429c769a7eCAS | 3031083PubMed |
Charpigny, G., Reinaud, P., Tamby, J. P., Créminon, C., and Guillomot, M. (1997). Cyclooxygenase-2, unlike cyclooxygenase-1, is highly expressed in ovine embryos during the implantation period. Biol. Reprod. 57, 1032–1040.
| Cyclooxygenase-2, unlike cyclooxygenase-1, is highly expressed in ovine embryos during the implantation period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvFSgu7g%3D&md5=fad01caa38e1511f1c7cec76f9077d3bCAS | 9369167PubMed |
Chian, R., and Sirard, M.-A. (1996). Protein synthesis is not required for male pronuclear formation in bovine zygotes. Zygote 4, 41–48.
| Protein synthesis is not required for male pronuclear formation in bovine zygotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xkt1Sktrg%3D&md5=cfadc8b664e1e4703363911cf360f29eCAS | 8735369PubMed |
Cui, X.-S., Li, X.-Y., and Kim, N.-H. (2007). Global gene transcription patterns in in vitro-cultured fertilized embryos and diploid and haploid murine parthenotes. Biochem. Biophys. Res. Commun. 352, 709–715.
| Global gene transcription patterns in in vitro-cultured fertilized embryos and diploid and haploid murine parthenotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtleis73P&md5=29dd4404b2c4ffb443708119b324380bCAS | 17141201PubMed |
Davis, W.,, De Sousa, P. A., and Schultz, R. M. (1996). Transient expression of translation initiation factor eIF-4C during the 2-cell stage of the preimplantation mouse embryo: identification by mRNA differential display and the role of DNA replication in zygotic gene activation. Dev. Biol. 174, 190–201.
| Transient expression of translation initiation factor eIF-4C during the 2-cell stage of the preimplantation mouse embryo: identification by mRNA differential display and the role of DNA replication in zygotic gene activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvVSgsLs%3D&md5=6dd9a9a94aba3e7f4d098a4d6d5fa7eeCAS | 8631492PubMed |
Dealy, M., Nguyen, K., Lo, J., Gstaiger, M., Krek, W., Elson, D., Arbeit, J., Kipreos, E., and Johnson, R. (1999). Loss of Cul1 results in early embryonic lethality and dysregulation of cyclin E. Nat. Genet. 23, 245–248.
| Loss of Cul1 results in early embryonic lethality and dysregulation of cyclin E.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlOhurk%3D&md5=d3275549884cabb30445f96dbcea5905CAS | 10508527PubMed |
De Sousa, P. A., Watson, A. J., and Schultz, R. M. (1998). Transient expression of a translation initiation factor is conservatively associated with embryonic gene activation in murine and bovine embryos. Biol. Reprod. 59, 969–977.
| Transient expression of a translation initiation factor is conservatively associated with embryonic gene activation in murine and bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVGrtrc%3D&md5=83c6aedeaf979799d2ae496a0b22cde4CAS | 9746750PubMed |
El-Sayed, A., Hoelker, M., Rings, F., Salilew, D., Jennen, D., Tholen, E., Sirard, M.-A., Schellander, K., and Tesfaye, D. (2006). Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol. Genomics 28, 84–96.
| Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCmtrzK&md5=3df176bd43bc3e4a707e7018766317b6CAS | 17018689PubMed |
Fukui, Y., Sawai, K., Furudate, M., Sato, N., Iwazumi, Y., and Ohsaki, K. (1992). Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin b after in vitro maturation. Mol. Reprod. Dev. 33, 357–362.
| Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin b after in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsVSqug%3D%3D&md5=d97fc200a7eeb27598c3f27f75cb5957CAS | 1449802PubMed |
Geng, Y., Yu, Q., Sicinska, E., Das, M., Schneider, J. E., Bhattacharya, S., Rideout Iii, W. M., Bronson, R. T., Gardner, H., and Sicinski, P. (2003). Cyclin E ablation in the mouse. Cell 114, 431–443.
| Cyclin E ablation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFahtbo%3D&md5=4bcd6ef1b6a49766c2da18a674d3b32cCAS | 12941272PubMed |
Gilbert, I., Scantland, S., Dufort, I., Gordynska, O., Labbe, A., Sirard, M.-A., and Robert, C. (2009). Real-time monitoring of aRNA production during T7 amplification to prevent the loss of sample representation during microarray hybridization sample preparation. Nucleic Acids Res. 37, e65.
| Real-time monitoring of aRNA production during T7 amplification to prevent the loss of sample representation during microarray hybridization sample preparation.Crossref | GoogleScholarGoogle Scholar | 19336411PubMed |
Gomez, E., Caamaño, J., Bermejo-Alvarez, P., Díez, C., Muñoz, M., Martín, D., Carrocera, S., and Gutiérrez-Adán, A. (2009a). Gene expression in early expanded parthenogenetic and in vitro-fertilized bovine blastocysts. J. Reprod. Dev. 55, 607–614.
| Gene expression in early expanded parthenogenetic and in vitro-fertilized bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVyqtL4%3D&md5=b3e3688ed3596c510b4e4485d1d72f0eCAS | 19700929PubMed |
Gomez, E., Gutierrez-Adan, A., Diez, C., Bermejo-Alvarez, P., Munoz, M., Rodriguez, A., Otero, J., Alvarez-Viejo, M., Martin, D., Carrocera, S., and Caamano, J. N. (2009b). Biological differences between in vitro-produced bovine embryos and parthenotes. Reproduction 137, 285–295.
| Biological differences between in vitro-produced bovine embryos and parthenotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ksLo%3D&md5=b2cf845697bac75eedab7cf39f22441aCAS | 19036952PubMed |
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 |
Gutierrez-Adan, A., Behboodi, E., Andersen, G. B., Medrano, J. F., and Murray, J. D. (1996). Relationship between stage of development and sex of bovine IVM–IVF embryos cultured in vitro versus in the sheep oviduct. Theriogenology 46, 515–525.
| Relationship between stage of development and sex of bovine IVM–IVF embryos cultured in vitro versus in the sheep oviduct.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVKktw%3D%3D&md5=5c5499825ab4b863c1eac51940fd9868CAS | 16727919PubMed |
Hammadeh, M. E., Fischer-Hammadeh, C., Georg, T., Rosenbaum, P., and Schmidt, W. (2003). Comparison between cytokine concentration in follicular fluid of poor- and high-responder patients and their influence of ICSI outcome. Am. J. Reprod. Immunol. 50, 131–136.
| Comparison between cytokine concentration in follicular fluid of poor- and high-responder patients and their influence of ICSI outcome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szhslalug%3D%3D&md5=3e9213feed3701f3c590529ca10adabdCAS | 12846676PubMed |
Harada, K., and Buss, E. (1981). Cytogenetic studies of embryos developing parthenogenetically in turkeys. Poult. Sci. 60, 1362..
| 7322963PubMed |
Harper, K. M., and Brackett, B. G. (1993). Bovine blastocyst development after follicle-stimulating hormone and platelet-derived growth factor treatment for oocyte maturation in vitro. Zygote 1, 27–34.
| Bovine blastocyst development after follicle-stimulating hormone and platelet-derived growth factor treatment for oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFaktrs%3D&md5=b17740863789fc12c6b74e286490457cCAS | 8081799PubMed |
Holm, P., Booth, P. J., and Callesen, H. (2003). Developmental kinetics of bovine nuclear transfer and parthenogenetic embryos. Cloning Stem Cells 5, 133–142.
| Developmental kinetics of bovine nuclear transfer and parthenogenetic embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtlOqsbY%3D&md5=241ea069b9550acfdb0157196de11d35CAS | 12930625PubMed |
Kobayashi, S., Isotani, A., Mise, N., Yamamoto, M., Fujihara, Y., Kaseda, K., Nakanishi, T., Ikawa, M., Hamada, H., Abe, K., and Okabe, M. (2006). Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages. Curr. Biol. 16, 166–172.
| Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xosl2mtw%3D%3D&md5=4a416aa040e8b27cf2184d5a408813faCAS | 16431368PubMed |
Kono, T., Obata, Y., Wu, Q., Niwa, K., Ono, Y., Yamamoto, Y., Park, E. S., Seo, J.-S., and Ogawa, H. (2004). Birth of parthenogenetic mice that can develop to adulthood. Nature 428, 860–864.
| Birth of parthenogenetic mice that can develop to adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crtrc%3D&md5=544d7fb21746be2d1e515c15526a166bCAS | 15103378PubMed |
Kubisch, H. M., Rasmussen, T. A., and Johnson, K. M. (2003). Interferon-tau in bovine blastocysts following parthenogenetic activation of oocytes: pattern of secretion and polymorphism in expressed mRNA sequences. Mol. Reprod. Dev. 64, 79–85.
| Interferon-tau in bovine blastocysts following parthenogenetic activation of oocytes: pattern of secretion and polymorphism in expressed mRNA sequences.Crossref | GoogleScholarGoogle Scholar | 12420302PubMed |
Kure-bayashi, S., Miyake, M., Okada, K., and Kato, S. (2000). Successful implantation of in vitro-matured, electro-activated oocytes in the pig. Theriogenology 53, 1105–1119.
| Successful implantation of in vitro-matured, electro-activated oocytes in the pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3ls1entA%3D%3D&md5=cd52ea12faf77bd3eb98b45e845384d3CAS | 10798488PubMed |
Larson, R. C., Ignotz, G. G., and Currie, W. B. (1992). Platelet-derived growth factor (PDGF) stimulates development of bovine embryos during the fourth cell cycle. Development 115, 821–826.
| 1:CAS:528:DyaK38XlvVGmsLs%3D&md5=290bd5c45ca53422dc28ca79526bb952CAS | 1425356PubMed |
Lawrence, Y., Whitaker, M., and Swann, K. (1997). Sperm–egg fusion is the prelude to the initial Ca2+ increase at fertilization in the mouse. Development 124, 233–241.
| 1:CAS:528:DyaK2sXnsFCmsg%3D%3D&md5=b25d771f6c46d9d7176ad4394fc0b24aCAS | 9006083PubMed |
Lim, J., and Hansel, W. (1996). Roles of growth factors in the development of bovine embryos fertilized in vitro and cultured singly in a defined medium. Reprod. Fertil. Dev. 8, 1199–1206.
| Roles of growth factors in the development of bovine embryos fertilized in vitro and cultured singly in a defined medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslSntw%3D%3D&md5=31b720f1d06edea331f3ecf8fe393d51CAS | 8981645PubMed |
Loeb, J. (1899). On the nature of the process of fertilization and the artificial production of normal larvae (plutei) from the unfertilized eggs of the sea urchin. Am. J. Physiol. 3, 135..
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. Reproduction 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=84e0d36c534120be1be92a6dd8f977c1CAS |
Lopata, A., and Oliva, K. (1993). Chorionic gonadotrophin secretion by human blastocysts. Hum. Reprod. 8, 932–938.
| 1:STN:280:DyaK3szks1Kisg%3D%3D&md5=8bdcce0371c7f1fbb1226e701d44e86bCAS | 8393891PubMed |
Magnani, L., Johnson, C. M., and Cabot, R. A. (2008). Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential. Reprod. Fertil. Dev. 20, 818–825.
| Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWmsb7N&md5=2405b763ed0e72c380ab51d21d234904CAS | 18842184PubMed |
Marshall, V. S., Wilton, L. J., and Moore, H. D. (1998). Parthenogenetic activation of marmoset (Callithrix jacchus) oocytes and the development of marmoset parthenogenones in vitro and in vivo. Biol. Reprod. 59, 1491–1497.
| Parthenogenetic activation of marmoset (Callithrix jacchus) oocytes and the development of marmoset parthenogenones in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVOhsLk%3D&md5=23c1d85cfc18a81e2878f1d468492964CAS | 9828197PubMed |
McElroy, S. L., Byrne, J. A., Chavez, S. L., Behr, B., Hsueh, A. J., Westphal, L. M., and Pera, R. A. (2010). Parthenogenic blastocysts derived from cumulus-free in vitro-matured human oocytes. PLoS ONE 5, e10979.
| Parthenogenic blastocysts derived from cumulus-free in vitro-matured human oocytes.Crossref | GoogleScholarGoogle Scholar | 20539753PubMed |
Osterlund, C., Wramsby, H., and Pousette, A. (1996). Temporal expression of platelet-derived growth factor (PDGF)-A and its receptor in human preimplantation embryos. Mol. Hum. Reprod. 2, 507–512.
| 1:STN:280:DyaK2szotlKkuw%3D%3D&md5=e8c77520e90de6f868d2ab0e0d9a8e4bCAS | 9239660PubMed |
Papanikolaou, T., Amiridis, G. S., Dimitriadis, I., Vainas, E., and Rekkas, C. A. (2008). Effect of plasmin, plasminogen activators and a plasmin inhibitor on bovine in vitro embryo production. Reprod. Fertil. Dev. 20, 320–327.
| Effect of plasmin, plasminogen activators and a plasmin inhibitor on bovine in vitro embryo production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXislyqur4%3D&md5=541ccbf01558081f9e387897cab1b26cCAS | 18255022PubMed |
Pincus, G., and Shapiro, H. (1940). The comparative behaviour of mammalian eggs in vivo and in vitro. VII. Further studies on the activation of rabbit eggs. Proc. Am. Philos. Soc. 83, 631–647.
Ramos, S. B. V., Stumpo, D. J., Kennington, E. A., Phillips, R. S., Bock, C. B., Ribeiro-Neto, F., and Blackshear, P. J. (2004). The CCCH tandem zinc-finger protein Zfp36l2 is crucial for female fertility and early embryonic development. Development 131, 4883–4893.
| The CCCH tandem zinc-finger protein Zfp36l2 is crucial for female fertility and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVOksrs%3D&md5=c1ca3a52276a9493c04a19a48e8df7cdCAS | 15342461PubMed |
Roberts, R., Leaman, D., and Cross, J. (1992). Role of interferons in maternal recognition of pregnancy in ruminants. Proc. Soc. Exp. Biol. Med. 200, 7–18.
| 1:CAS:528:DyaK38Xitlegtro%3D&md5=23f7f2612e294cc1d858f167a4f2999dCAS | 1373898PubMed |
Sharov, A. A., Dudekula, D. B., and Ko, M. S. H. (2005). A web-based tool for principal component and significance analysis of microarray data. Bioinformatics 21, 2548–2549.
| A web-based tool for principal component and significance analysis of microarray data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktl2qs7k%3D&md5=e88d197efb5b88d5e2169e1b71c52c89CAS | 15734774PubMed |
Sirard, M. A., Dufort, I., Vallee, M., Massicotte, L., Gravel, C., Reghenas, H., Watson, A. J., King, W. A., and Robert, C. (2005). Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development: preliminary analysis using a bovine embryonic array. Reprod. Fertil. Dev. 17, 47–57.
| Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development: preliminary analysis using a bovine embryonic array.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKrurbJ&md5=dd4f930a6f5f4def3124a4639ce1f7b2CAS | 15745631PubMed |
Smith, S., Francis, R., Guilbert, L., and Baker, P. N. (2002). Growth factor rescue of cytokine-mediated trophoblast apoptosis. Placenta 23, 322–330.
| Growth factor rescue of cytokine-mediated trophoblast apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlyrsL8%3D&md5=cc5b9e318182143c37a9000602cd6290CAS | 11969343PubMed |
Snabes, M. C., and Harper, M. J. K. (1984). Site of action of indomethacin on implantation in the rabbit. J. Reprod. Fertil. 71, 559–565.
| Site of action of indomethacin on implantation in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1ers7Y%3D&md5=765efda09d296fbdceeb7be4c3fd12b7CAS | 6747963PubMed |
Somfai, T., Inaba, Y., Aikawa, Y., Ohtake, M., Kobayashi, S., Konishi, K., and Imai, K. (2010). Relationship between the length of cell cycles, cleavage pattern and developmental competence in bovine embryos generated by in vitro fertilization or parthenogenesis. J. Reprod. Dev. 56, 200–207.
| Relationship between the length of cell cycles, cleavage pattern and developmental competence in bovine embryos generated by in vitro fertilization or parthenogenesis.Crossref | GoogleScholarGoogle Scholar | 20035110PubMed |
Stumpo, D. J., Byrd, N. A., Phillips, R. S., Ghosh, S., Maronpot, R. R., Castranio, T., Meyers, E. N., Mishina, Y., and Blackshear, P. J. (2004). Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc-finger protein of the tristetraprolin family. Mol. Cell. Biol. 24, 6445–6455.
| Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc-finger protein of the tristetraprolin family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlslentro%3D&md5=f4563c594d54aaaa809fc9bf7692177bCAS | 15226444PubMed |
Surani, M. A., Barton, S. C., and Norris, M. L. (1987). Experimental reconstruction of mouse eggs and embryos: an analysis of mammalian development. Biol. Reprod. 36, 1–16.
| Experimental reconstruction of mouse eggs and embryos: an analysis of mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7osFKltw%3D%3D&md5=275fc72fab2b495b0ddd3e913c128254CAS | 3552065PubMed |
Tateishi, K., Omata, M., Tanaka, K., and Chiba, T. (2001). The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice. J. Cell Biol. 155, 571–580.
| The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVKitbc%3D&md5=5ccffb70b924e75f29c77e1307347b3cCAS | 11696557PubMed |
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |
Vigneault, C., McGraw, S., Massicotte, L., and Sirard, M.-A. (2004). Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal–zygotic transition. Biol. Reprod. 70, 1701–1709.
| Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal–zygotic transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmt74%3D&md5=4999d12e6e05818593d436d493afc780CAS | 14960490PubMed |
Vigneault, C., Gravel, C., Vallee, M., McGraw, S., and Sirard, M.-A. (2009). Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition. Reproduction 137, 245–257.
| Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ksL8%3D&md5=773e81c6930f4430a3fa4014e9b73223CAS | 18987256PubMed |
Wang, Y., Penfold, S., Tang, X., Hattori, N., Riley, P., Harper, J. W., Cross, J. C., and Tyers, M. (1999). Deletion of the Cul1 gene in mice causes arrest in early embryogenesis and accumulation of cyclin E. Curr. Biol. 9, 1191–1194.
| Deletion of the Cul1 gene in mice causes arrest in early embryogenesis and accumulation of cyclin E.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVSlt7Y%3D&md5=922dd79e8579caa67c09af3c9e4cd89dCAS | 10531039PubMed |
Xia, X.-Q., McClelland, M., Porwollik, S., Song, W., Cong, X., and Wang, Y. (2009). WebArrayDB: cross-platform microarray data analysis and public data repository. Bioinformatics 25, 2425–2429.
| WebArrayDB: cross-platform microarray data analysis and public data repository.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFSnsrnI&md5=6444c72b68394fb128241feec89d6aa3CAS | 19602526PubMed |
Yao, N., Wan, P. C., Hao, Z. D., Gao, F. F., Yang, L., Cui, M. S., Wu, Y., Liu, J. H., Liu, S., Chen, H., and Zeng, S. M. (2009). Expression of interferon-tau mRNA in bovine embryos derived from different procedures. Reprod. Domest. Anim. 44, 132–139.
| Expression of interferon-tau mRNA in bovine embryos derived from different procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislKitrY%3D&md5=b6477a6f72c54b9bae48fb01a2810f27CAS | 19019066PubMed |
Yoshida, Y., Miyamura, M., Hamano, S., and Yoshida, M. (1998). Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro. J. Vet. Med. Sci. 60, 549–554.
| Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVCmu74%3D&md5=1b2646d74c254c0cd8977a913bbfb19bCAS | 9637286PubMed |
