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

De novo transcription of thyroid hormone receptors is essential for early bovine embryo development in vitro

N.-Y. Rho A , F. A. Ashkar A , T. Revay A , P. Madan A , G.-J. Rho B , W. A. King A and L. A. Favetta A C
+ Author Affiliations
- Author Affiliations

A Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

B Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Gyeongsang National University, Jinju 660-701, Republic of Korea.

C Corresponding author. Email: lfavetta@uoguelph.ca

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17165
Submitted: 29 April 2017  Accepted: 18 October 2017   Published online: 28 November 2017

Abstract

Thyroid hormone receptor (THR) α and THRβ mediate the genomic action of thyroid hormones (THs) that affect bovine embryo development. However, little is known about THRs in the preimplantation embryo. The aim of the present study was to investigate the importance of THRs in in vitro preimplantation bovine embryos. THR transcripts and protein levels were detected in developing preimplantation embryos up to the blastocyst stage. Embryonic transcription of THRs was inhibited by α-amanitin supplementation, and both maternal and embryonic transcription were knocked down by short interference (si) RNA microinjection. In the control group, mRNA and protein levels of THRs increased after fertilisation. In contrast, in both the transcription inhibition and knockdown groups there were significant (P < 0.05) decreases in mRNA expression of THRs from the 2-cell stage onwards. However, protein levels of THRs were not altered at 2-cell stage, although they did exhibit a significant (P < 0.05) decrease from the 4-cell stage. Moreover, inhibition of de novo transcripts of THRs using siRNA led to a significant (P < 0.01) decrease in the developmental rate and cell number, as well as inducing a change in embryo morphology. In conclusion, THRs are transcribed soon after fertilisation, before major activation of the embryonic genome, and they are essential for bovine embryo development in vitro.

Additional keywords: embryonic genome activation.


References

Ashkar, F. A. (2013). Developmental and genomic aspects of thyroid hormones during early embryo development in cattle. University of Guelph.

Ashkar, F. A., Semple, E., Schmidt, C. H., John, E. S., Bartlewski, P. M., and King, W. (2010). Thyroid hormone supplementation improves bovine embryo development in vitro. Hum. Reprod. 25, 334–344.
Thyroid hormone supplementation improves bovine embryo development in vitro.CrossRef | 1:CAS:528:DC%2BC3cXntlWhtQ%3D%3D&md5=12c61d132bc31d1424f3a3ebc2e8992dCAS |

Ashkar, F. A., Revay, T., Rho, N., Madan, P., Dufort, I., Robert, C., Favetta, L. A., Schmidt, C., and King, W. A. (2016). Thyroid hormones alter the transcriptome of in vitro-produced bovine blastocysts. Zygote 24, 266–276.
Thyroid hormones alter the transcriptome of in vitro-produced bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC28XltVKns7g%3D&md5=fbe19dbc214df866748ba791e8524738CAS |

Barnes, F., and Eyestone, W. (1990). Early cleavage and the maternal zygotic transition in bovine embryos. Theriogenology 33, 141–152.
Early cleavage and the maternal zygotic transition in bovine embryos.CrossRef |

Barnes, F. L., and First, N. L. (1991). Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev. 29, 117–123.
Embryonic transcription in in vitro cultured bovine embryos.CrossRef | 1:CAS:528:DyaK3MXltFWhurs%3D&md5=9eee7fbff0cf34346a17b7ab65a32120CAS |

Burgess, A., Vigneron, S., Brioudes, E., Labbe, J. C., Lorca, T., and Castro, A. (2010). Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc. Natl Acad. Sci. USA 107, 12564–12569.
Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance.CrossRef | 1:CAS:528:DC%2BC3cXpt1eiu7w%3D&md5=5c421fd4055d330c6f1078ab8cabc685CAS |

Choi, Y. H., Hartman, D. L., Fissore, R. A., Bedford-Guaus, S. J., and Hinrichs, K. (2009). Effect of sperm extract injection volume, injection of PLCzeta cRNA, and tissue cell line on efficiency of equine nuclear transfer. Cloning Stem Cells 11, 301–308.
Effect of sperm extract injection volume, injection of PLCzeta cRNA, and tissue cell line on efficiency of equine nuclear transfer.CrossRef | 1:CAS:528:DC%2BD1MXnt1Cis74%3D&md5=8ca917ed53d03c77f6ae62846fe3e8e6CAS |

Colazingari, S., Fiorenza, M. T., Carlomagno, G., Najjar, R., and Bevilacqua, A. (2014). Improvement of mouse embryo quality by myo-inositol supplementation of IVF media. J. Assist. Reprod. Genet. 31, 463–469.
Improvement of mouse embryo quality by myo-inositol supplementation of IVF media.CrossRef |

Costa, N. N., Cordeiro, M. S., Silva, T. V., Sastre, D., Santana, P. P., Sá, A. L., Sampaio, R. V., Santos, S. S., Adona, P. R., Miranda, M. S., and Ohashi, O. M. (2013). Effect of triiodothyronine on developmental competence of bovine oocytes. Theriogenology 80, 295–301.
Effect of triiodothyronine on developmental competence of bovine oocytes.CrossRef | 1:CAS:528:DC%2BC3sXnslChtLg%3D&md5=cbebe0a2ca6b88ae817c24444aa89972CAS |

Dittrich, R., Beckmann, M. W., Oppelt, P. G., Hoffmann, I., Lotz, L., Kuwert, T., and Mueller, A. (2011). Thyroid hormone receptors and reproduction. J. Reprod. Immunol. 90, 58–66.
Thyroid hormone receptors and reproduction.CrossRef | 1:CAS:528:DC%2BC3MXos1ygsbo%3D&md5=857afccef1c9c2dcd2deaa05ca1c8503CAS |

Favetta, L. A., Robert, C., St. John, E. J., Betts, D. H., and King, W. A. (2004). p66shc, but not p53, is involved in early arrest of in vitro‐produced bovine embryos. Mol. Hum. Reprod. 10, 383–392.
p66shc, but not p53, is involved in early arrest of in vitro‐produced bovine embryos.CrossRef | 1:CAS:528:DC%2BD2cXjvVSisr8%3D&md5=f27aba29373b488f37d559143387ab09CAS |

Favetta, L. A., Madan, P., Mastromonaco, G. F., St John, E. J., King, W. A., and Betts, D. H. (2007). The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro. BMC Dev. Biol. 7, 132.
The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro.CrossRef |

Ferris, J. (2015). Effects of oocyte bisphenol A exposure on aspects of oocyte maturation and early embryo development in Bos taurus. University of Guelph.

Ferris, J., Mahboubi, K., MacLusky, N., King, W. A., and Favetta, L. A. (2016). BPA exposure during in vitro oocyte maturation results in dose-dependent alterations to embryo development rates, apoptosis rate, sex ratio and gene expression. Reprod. Toxicol. 59, 128–138.
BPA exposure during in vitro oocyte maturation results in dose-dependent alterations to embryo development rates, apoptosis rate, sex ratio and gene expression.CrossRef | 1:CAS:528:DC%2BC28Xitl2ju70%3D&md5=a0c1edb5d20981aa5ce07708680153a7CAS |

Flach, G., Johnson, M., Braude, P., Taylor, R., and Bolton, V. (1982). The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1, 681.
| 1:CAS:528:DyaL38XltVOrsL0%3D&md5=ed64180008d0c8c1f0d6d063d250fdbcCAS |

Frei, R. E., Schultz, G. A., and Church, R. B. (1989). Qualitative and quantitative changes in protein synthesis occur at the 8–16-cell stage of embryogenesis in the cow. J. Reprod. Fertil. 86, 637–641.
Qualitative and quantitative changes in protein synthesis occur at the 8–16-cell stage of embryogenesis in the cow.CrossRef | 1:CAS:528:DyaL1MXkslGgtrk%3D&md5=85e97698d3725bb081cbf4071b562c36CAS |

Gilchrist, R. B., and Thompson, J. G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.
Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro.CrossRef |

Gilchrist, G. C., Kurjanowicz, P., Mereilles, F. V., King, W. A., and LaMarre, J. (2015). Telomere length and telomerase activity in bovine pre‐implantation embryos in vitro. Reprod. Domest. Anim. 50, 58–67.
Telomere length and telomerase activity in bovine pre‐implantation embryos in vitro.CrossRef | 1:CAS:528:DC%2BC2MXhsVWksbg%3D&md5=eb11560af15c0896cdc2ca237920ff9dCAS |

González-Grajales, L. A., Favetta, L. A., King, W. A., and Mastromonaco, G. F. (2016a). Developmental competence of 8–16-cell stage bison embryos produced by interspecies somatic cell nuclear transfer. Reprod. Fertil. Dev. 28, 1360–1368.
Developmental competence of 8–16-cell stage bison embryos produced by interspecies somatic cell nuclear transfer.CrossRef |

González-Grajales, L. A., Favetta, L. A., King, W. A., and Mastromonaco, G. F. (2016b). Lack of effects of ooplasm transfer on early development of interspecies somatic cell nuclear transfer bison embryos. BMC Dev. Biol. 16, 36.
Lack of effects of ooplasm transfer on early development of interspecies somatic cell nuclear transfer bison embryos.CrossRef |

Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A., and Peelman, L. J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.
Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos.CrossRef |

Graf, A., Krebs, S., Heininen-Brown, M., Zakhartchenko, V., Blum, H., and Wolf, E. (2014a). Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Anim. Reprod. Sci. 149, 46–58.
Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments.CrossRef | 1:CAS:528:DC%2BC2cXhtVymu7bF&md5=2197dea1d6d9bcc475c183b08870d022CAS |

Graf, A., Krebs, S., Zakhartchenko, V., Schwalb, B., Blum, H., and Wolf, E. (2014b). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc. Natl Acad. Sci. USA 111, 4139–4144.
Fine mapping of genome activation in bovine embryos by RNA sequencing.CrossRef | 1:CAS:528:DC%2BC2cXjtlyhsrs%3D&md5=ab118205af32ec7878414877b5951e62CAS |

Graupner, G., Zhang, X. K., Tzukerman, M., Wills, K., Hermann, T., and Pfahl, M. (1991). Thyroid hormone receptors repress estrogen receptor activation of a TRE. Mol. Endocrinol. 5, 365–372.
Thyroid hormone receptors repress estrogen receptor activation of a TRE.CrossRef | 1:CAS:528:DyaK3MXit1Wku7w%3D&md5=76cb2422bea9ff656340a97384fc9f64CAS |

Hamatani, T., Carter, M. G., Sharov, A. A., and Ko, M. S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–131.
Dynamics of global gene expression changes during mouse preimplantation development.CrossRef | 1:CAS:528:DC%2BD2cXntlaktA%3D%3D&md5=52ee43d3bab5d0a193b2a9035c3f5aafCAS |

Hamilton, C. K., Revay, T., Domander, R., Favetta, L. A., and King, W. A. (2011). A large expansion of the HSFY gene family in cattle shows dispersion across Yq and testis-specific expression. PLoS One 6, e17790.
A large expansion of the HSFY gene family in cattle shows dispersion across Yq and testis-specific expression.CrossRef | 1:CAS:528:DC%2BC3MXjsFShtr4%3D&md5=f9eccfc982acc64799dfea60cc845860CAS |

Hamilton, C. K., Combe, A., Caudle, J., Ashkar, F. A., Macaulay, A. D., Blondin, P., and King, W. A. (2012). A novel approach to sexing bovine blastocysts using male-specific gene expression. Theriogenology 77, 1587–1596.
A novel approach to sexing bovine blastocysts using male-specific gene expression.CrossRef | 1:CAS:528:DC%2BC38XltVKmt70%3D&md5=65d2e2d60510131795e88d734f3e4bcdCAS |

Heldring, N., Pike, A., Andersson, S., Matthews, J., Cheng, G., Hartman, J., Tujague, M., Ström, A., Treuter, E., and Warner, M. (2007). Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87, 905–931.
Estrogen receptors: how do they signal and what are their targets.CrossRef | 1:CAS:528:DC%2BD2sXptFGls7k%3D&md5=7c42e8c15e7d9faa373af53d98979916CAS |

Hörlein, A. J., Näär, A. M., Heinzel, T., Torchia, J., Gloss, B., Kurokawa, R., Ryan, A., Kamei, Y., Söderström, M., Glass, C. K., and Rosenfeld, M. G. (1995). Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377, 397–404.
Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor.CrossRef |

Hsu, J. H., and Brent, G. A. (1998). Thyroid hormone receptor gene knockouts. Trends Endocrinol. Metab. 9, 103–112.
Thyroid hormone receptor gene knockouts.CrossRef | 1:CAS:528:DyaK1cXjs1OrsbY%3D&md5=233d9936a5f95e93a787fd7e4d117433CAS |

Izumo, S., and Mahdavi, V. (1988). Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin +HC gene transcription. Nature 334, 539–542.
Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin +HC gene transcription.CrossRef | 1:CAS:528:DyaL1cXlt1eltbY%3D&md5=58d55de672c117981b2ea9da3e458399CAS |

Jeong, Y. J., Choi, H. W., Shin, H. S., Cui, X. S., Kim, N. H., Gerton, G. L., and Jun, J. H. (2005). Optimization of real-time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. Mol. Reprod. Dev. 71, 284–289.
Optimization of real-time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD2MXltFyiu7c%3D&md5=b626dbeaab99f0ca3752d98c734d95fbCAS |

Katz, D., Reginato, M. J., and Lazar, M. A. (1995). Functional regulation of thyroid hormone receptor variant TR alpha 2 by phosphorylation. Mol. Cell. Biol. 15, 2341–2348.
Functional regulation of thyroid hormone receptor variant TR alpha 2 by phosphorylation.CrossRef | 1:CAS:528:DyaK2MXltFagt7w%3D&md5=b38dd8d20ba1eb6d55fcd525be9a77d3CAS |

King, W. A., and Ashkar, F. A. (2013) Embryo culture media containing thyroid hormone. US Patent 8,492,080.

Koehler, D., Zakhartchenko, V., Froenicke, L., Stone, G., Stanyon, R., Wolf, E., Cremer, T., and Brero, A. (2009). Changes of higher order chromatin arrangements during major genome activation in bovine preimplantation embryos. Exp. Cell Res. 315, 2053–2063.
Changes of higher order chromatin arrangements during major genome activation in bovine preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD1MXntVKjtbg%3D&md5=2c34a7a1c5de2aad0b605dae1b5b53f4CAS |

Koenig, R. J., Lazar, M. A., Hodin, R. A., Brent, G. A., Larsen, P. R., Chin, W. W., and Moore, D. D. (1989). Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing. Nature 337, 659–661.
Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing.CrossRef | 1:CAS:528:DyaL1MXhs1Ohs7w%3D&md5=2a392b77c71ae27d6d0ca0e0898fd0f4CAS |

Kowalik, M. A., Perra, A., Pibiri, M., Cocco, M. T., Samarut, J., Plateroti, M., Ledda-Columbano, G. M., and Columbano, A. (2010). TRbeta is the critical thyroid hormone receptor isoform in T3-induced proliferation of hepatocytes and pancreatic acinar cells. J. Hepatol. 53, 686–692.
TRbeta is the critical thyroid hormone receptor isoform in T3-induced proliferation of hepatocytes and pancreatic acinar cells.CrossRef | 1:CAS:528:DC%2BC3cXhtV2gtbnJ&md5=4bb97e9ccca17c96c3f10435b0f83253CAS |

Kues, W. A., Sudheer, S., Herrmann, D., Carnwath, J. W., Havlicek, V., Besenfelder, U., Lehrach, H., Adjaye, J., and Niemann, H. (2008). Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc. Natl Acad. Sci. USA 105, 19768–19773.
Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo.CrossRef | 1:CAS:528:DC%2BD1cXhsFCltrrL&md5=708108855d6016d78455d2f2983777ffCAS |

Latham, K. E., and Schultz, R. M. (2001). Embryonic genome activation. Frontiers in Bioscience 6, D748–D759.
Embryonic genome activation.CrossRef | 1:CAS:528:DC%2BD3MXlslKhuro%3D&md5=a1d98960c96a24681efe99c9e8dab9c5CAS |

Latham, K. E., Garrels, J. I., Chang, C., and Solter, D. (1991). Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development 112, 921–932.
| 1:CAS:528:DyaK3MXmtVCht70%3D&md5=4ef04ecfbbf6a85bd28378699275b675CAS |

Laudet, V., Hanni, C., Coll, J., Catzeflis, F., and Stehelin, D. (1992). Evolution of the nuclear receptor gene superfamily. EMBO J. 11, 1003–1013.
| 1:CAS:528:DyaK38Xks1Gitrc%3D&md5=ce841b91d494184c4b922256c571bf08CAS |

Lazar, M. A. (2003). Thyroid hormone action: a binding contract. J. Clin. Invest. 112, 497.
Thyroid hormone action: a binding contract.CrossRef | 1:CAS:528:DC%2BD3sXms1Wntbo%3D&md5=97827bdbe03b2a4f46e9c0003b4eb358CAS |

Lindell, T. J., Weinberg, F., Morris, P. W., Roeder, R. G., and Rutter, W. J. (1970). Specific inhibition of nuclear RNA polymerase II by α-amanitin. Science 170, 447–449.
Specific inhibition of nuclear RNA polymerase II by α-amanitin.CrossRef | 1:CAS:528:DyaE3MXhvFOhsQ%3D%3D&md5=76329e2ac0cb9db9921ea509601cf0ccCAS |

Lonergan, P., Rizos, D., Gutierrez‐Adan, A., Fair, T., and Boland, M. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.CrossRef | 1:STN:280:DC%2BD3svis1SrsA%3D%3D&md5=908969d519d8f5d1540979fa2b53df15CAS |

Memili, E., and First, N. L. (1998). Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of α-amanitin on embryo development. Mol. Reprod. Dev. 51, 381–389.
Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of α-amanitin on embryo development.CrossRef | 1:CAS:528:DyaK1cXnt1Ortrw%3D&md5=253415537c491702ad86a23c98343c8aCAS |

Memili, E., and First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species.CrossRef | 1:CAS:528:DC%2BD3cXjvVemtLo%3D&md5=586fe0c714e4002102a484dc436da5d9CAS |

Misirlioglu, M., Page, G., Sagirkaya, H., Kaya, A., Parrish, J., First, N., and Memili, E. (2006). Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc. Natl Acad. Sci. USA 103, 18905–18910.
Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD28XhtlChu77M&md5=2252cb59afd622ea1ffa6b9a970892eaCAS |

Mullur, R., Liu, Y. Y., and Brent, G. A. (2014). Thyroid hormone regulation of metabolism. Physiol. Rev. 94, 355–382.
Thyroid hormone regulation of metabolism.CrossRef | 1:CAS:528:DC%2BC2cXptFygt78%3D&md5=abe6a7b1e246bdac8b4c13a4978d3e84CAS |

Nan, X., Campoy, F. J., and Bird, A. (1997). MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88, 471–481.
MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin.CrossRef | 1:CAS:528:DyaK2sXhtlKqur8%3D&md5=680f22dd4f8a5663ce6e8358e0c7cd35CAS |

O’Meara, C. M., Murray, J. D., Mamo, S., Gallagher, E., Roche, J., and Lonergan, P. (2011). Gene silencing in bovine zygotes: siRNA transfection versus microinjection. Reprod. Fertil. Dev. 23, 534–543.
Gene silencing in bovine zygotes: siRNA transfection versus microinjection.CrossRef | 1:CAS:528:DC%2BC3MXlsFKnsLc%3D&md5=f7be09e47eb7d7f652892a1098852987CAS |

Pavani, K. C., Baron, E., Correia, P., Lourenço, J., Bettencourt, B. F., Sousa, M., and da Silva, F. M. (2016). Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock. Zygote 24, 748–759.
Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock.CrossRef | 1:CAS:528:DC%2BC28XhsFaku7fI&md5=3c92fd8fdfdc8af1ae1385e6e53de418CAS |

Plante, L., Plante, C., Shepard, D. L., and King, W. A. (1994). Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential. Mol. Reprod. Dev. 39, 375–383.
| 1:CAS:528:DyaK2MXisFWjtro%3D&md5=162f53bc50b87d0bb2720cfa8364aaaeCAS |

Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.CrossRef | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=826b69327963ea41db6cd141a10ae5e0CAS |

Reginato, M. J., Zhang, J., and Lazar, M. A. (1996). DNA-independent and DNA-dependent mechanisms regulate the differential heterodimerization of the isoforms of the thyroid hormone receptor with retinoid X receptor. J. Biol. Chem. 271, 28199–28205.
DNA-independent and DNA-dependent mechanisms regulate the differential heterodimerization of the isoforms of the thyroid hormone receptor with retinoid X receptor.CrossRef | 1:CAS:528:DyaK28XmvVWksLk%3D&md5=88c94369417d7f1cda7a733f9eb9d092CAS |

Robert, C., McGraw, S., Massicotte, L., Pravetoni, M., Gandolfi, F., and Sirard, M. (2002). Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos. Biol. Reprod. 67, 1465–1472.
Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD38Xot1Kjs78%3D&md5=30fd6543a6af9ae0f6ed763a114decf4CAS |

Schier, A. F. (2007). The maternal–zygotic transition: death and birth of RNAs. Science 316, 406–407.
The maternal–zygotic transition: death and birth of RNAs.CrossRef | 1:CAS:528:DC%2BD2sXktlSku7Y%3D&md5=05052af60f56eee205e402a9e1dd628aCAS |

Schultz, R. M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update 8, 323–331.
The molecular foundations of the maternal to zygotic transition in the preimplantation embryo.CrossRef | 1:CAS:528:DC%2BD38XnsVOgtLY%3D&md5=55b5a5000be75749a02f7e4ad373bbc3CAS |

Stroebech, L., Mazzoni, G., Pedersen, H. S., Freude, K. K., Kadarmideen, H., Callesen, H., and Hyttel, P. (2015). In vitro production of bovine embryos: revisiting oocyte development and application of systems biology. Anim. Reprod. 12, 465–472.

Telford, N. A., Watson, A. J., and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
Transition from maternal to embryonic control in early mammalian development: a comparison of several species.CrossRef | 1:STN:280:DyaK3c3mslOhtQ%3D%3D&md5=ee309600372fcb094d3f5d9cda8cc093CAS |

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 | 1:CAS:528:DC%2BD2cXktlOmt74%3D&md5=a8d2e9e445990218767ae69c058c7fa4CAS |

Wang, F., Tian, X., Zhou, Y., Tan, D., Zhu, S., Dai, Y., and Liu, G. (2014). Melatonin improves the quality of in vitro produced (IVP) bovine embryos: implications for blastocyst development, cryotolerance, and modifications of relevant gene expression. PLoS One 9, e93641.
Melatonin improves the quality of in vitro produced (IVP) bovine embryos: implications for blastocyst development, cryotolerance, and modifications of relevant gene expression.CrossRef |

Waung, J. A., Bassett, J. H., and Williams, G. R. (2012). Thyroid hormone metabolism in skeletal development and adult bone maintenance. Trends Endocrinol. Metab. 23, 155–162.
Thyroid hormone metabolism in skeletal development and adult bone maintenance.CrossRef | 1:CAS:528:DC%2BC38XktlOjtLk%3D&md5=f0b7d141ff78043c25a38f0b38c6e7aeCAS |

Wu, Y., and Koenig, R. J. (2000). Gene regulation by thyroid hormone. Trends Endocrinol. Metab. 11, 207–211.
Gene regulation by thyroid hormone.CrossRef | 1:CAS:528:DC%2BD3cXks12rtb0%3D&md5=10c91efbe882986337a1a065e5b991b2CAS |

Zimin, A. V., Delcher, A. L., Florea, L., Kelley, D. R., Schatz, M. C., Puiu, D., Hanrahan, F., Pertea, G., Van Tassell, C. P., Sonstegard, T. S., Marcais, G., Roberts, M., Subramanian, P., Yorke, J. A., and Salzberg, S. L. (2009). A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 10, R42. https://doi.org/10.1186/gb-2009-10-4-r42



Export Citation