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

Gene expression profiling of pluripotency and differentiation-related markers in cat oocytes and preimplantation embryos

Muriel Filliers A F , Karen Goossens B , Ann Van Soom A , Barbara Merlo C , Charles Earle Pope D , Hilde de Rooster E , Katrien Smits A , Leen Vandaele A and Luc J. Peelman B
+ Author Affiliations
- Author Affiliations

A Department of Reproduction, Obstetrics, and Herd Health, Faculty of Veterinary Medicine, Ghent University, B-9820 Merelbeke, Belgium.

B Department of Nutrition, Genetics, and Ethology, Faculty of Veterinary Medicine, Ghent University, B-9820 Merelbeke, Belgium.

C Veterinary Clinical Department, Obstetrical-Gynaecologycal Section, University of Bologna, 40064 Ozzano Emilia, Bologna, Italy.

D Audubon Center for Research of Endangered Species, 14001 River Road, New Orleans, LA 70131, USA.

E Department of Small Animal Medicine and Clinical Biology, Faculty of Veterinary Medicine, Ghent University, B-9820 Merelbeke, Belgium.

F Corresponding author. Email: muriel.filliers@ugent.be

Reproduction, Fertility and Development 24(5) 691-703 https://doi.org/10.1071/RD11068
Submitted: 15 March 2011  Accepted: 20 July 2011   Published: 6 December 2011

Abstract

During mammalian preimplantation development, two successive differentiation events lead to the establishment of three committed lineages with separate fates: the trophectoderm, the primitive endoderm and the pluripotent epiblast. In the mouse embryo, the molecular mechanisms underlying these two cell fate decisions have been studied extensively, leading to the identification of lineage-specific transcription factors. Species-specific differences in expression patterns of key regulatory genes have been reported, raising questions regarding their role in different species. The aim of the present study was to characterise the gene expression patterns of pluripotency (OCT4, SOX2, NANOG) and differentiation (CDX2, GATA6)-related markers during feline early development using reverse transcription–quantitative polymerase chain reaction. In addition, we assessed the impact of in vitro development on gene expression by comparing transcript levels of the genes investigated between in vitro and in vivo blastocysts. To normalise quantitative data within different preimplantation embryo stages, we first validated a set of stable reference genes. Transcript levels of all genes investigated were present and changed over the course of preimplantation development; a highly significant embryo-stage effect on gene expression was observed. Transcript levels of OCT4 were significantly reduced in in vitro blastocysts compared with their in vivo counterparts. None of the other genes investigated showed altered expression under in vitro conditions. The different gene expression patterns of OCT4, SOX2, CDX2 and GATA6 in cat embryos resembled those described in mouse embryos, indicative of a preserved role for these genes during early segregation. However, because of the absence of any upregulation of NANOG transcription levels after embryonic genome activation, it is unlikely that NANOG is a key regular of lineage segregation. Such results support the hypothesis that the behaviour of early lineage markers can be species specific. The present study also revealed a pool of maternal NANOG mRNA transcripts, the role of which remains to be elucidated. Comparing transcription levels of these genes between in vivo and in vitro blastocysts revealed low levels of OCT4 mRNA in the latter, which may contribute to the reduced developmental competence of embryos under suboptimal conditions.

Additional keywords: early lineage segregation, in vivo blastocyst, OCT4.


References

Abdel-Rahman, B., Fiddler, M., Rappolee, D., and Pergament, E. (1995). Expression of transcription regulating genes in human preimplantation embryos. Hum. Reprod. 10, 2787–2792.
| 1:CAS:528:DyaK28XktV2muw%3D%3D&md5=4393e5e74cdaec2c3298094fed4ec69fCAS | 8567814PubMed |

Ambrosetti, D. C., Schöler, H. R., Dailey, L., and Basilico, C. (2000). Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J. Biol. Chem. 275, 23 387–23 397.
Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltlGqtbw%3D&md5=b2f3fb96d09378ffdf569d825ff9b19eCAS |

Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N., and Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126–140.
Multipotent cell lineages in early mouse development depend on SOX2 function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlKqtg%3D%3D&md5=56402ed20d763e38fbc8965c2169a593CAS | 12514105PubMed |

Bell, C. E., Calder, M. D., and Watson, A. J. (2008). Genomic RNA profiling and the programme controlling preimplantation mammalian development. Mol. Hum. Reprod. 14, 691–701.
Genomic RNA profiling and the programme controlling preimplantation mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gsQ%3D%3D&md5=adad16081645cea8d123faa5f3c4364aCAS | 19043080PubMed |

Blomberg, L. A., Schreier, L. L., and Talbot, N. C. (2008). Expression analysis of pluripotency factors in the undifferentiated porcine inner cell mass and epiblast during in vitro culture. Mol. Reprod. Dev. 75, 450–463.
Expression analysis of pluripotency factors in the undifferentiated porcine inner cell mass and epiblast during in vitro culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1Cku7k%3D&md5=16c93544c57511241154df3d26d08deaCAS | 17680630PubMed |

Buehr, M., Meek, S., Blair, K., Yang, J., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q. L., and Smith, A. (2008). Capture of authentic embryonic stem cells from rat blastocysts. Cell 135, 1287–1298.
Capture of authentic embryonic stem cells from rat blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFyisA%3D%3D&md5=41f50214e4a88de30ce5a8d9faa8f00fCAS | 19109897PubMed |

Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=d90d1f9594374842fc1ca7214aee8e02CAS | 19246619PubMed |

Cauffman, G., Van de Velde, H., Liebaers, I., and Van Steirteghem, A. (2005). Oct-4 mRNA and protein expression during human preimplantation development. Mol. Hum. Reprod. 11, 173–181.
Oct-4 mRNA and protein expression during human preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitV2jtr8%3D&md5=d67e1206c66c0f778370cc872639b456CAS | 15695770PubMed |

Cauffman, G., De Rycke, M., Sermon, K., Liebaers, I., and Van de Velde, H. (2009). Markers that define stemness in ESC are unable to identify the totipotent cells in human preimplantation embryos. Hum. Reprod. 24, 63–70.
Markers that define stemness in ESC are unable to identify the totipotent cells in human preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWjtbfJ&md5=b12e6e2ad9421faae88796c737242d7aCAS | 18824471PubMed |

Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S., and Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643–655.
Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksFehur8%3D&md5=0f6449932ffded8b5930f809cef01482CAS | 12787505PubMed |

Chazaud, C., Yamanaka, Y., Pawson, T., and Rossant, J. (2006). Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2–MAPK pathway. Dev. Cell 10, 615–624.
Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2–MAPK pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVyktro%3D&md5=a2cdc0855cf4cee1a8d6663e3827ec12CAS | 16678776PubMed |

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 |

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 |

Dard, N., Breuer, M., Maro, B., and Louvet-Vallée, S. (2008). Morphogenesis of the mammalian blastocyst. Mol. Cell. Endocrinol. 282, 70–77.
Morphogenesis of the mammalian blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVegtL0%3D&md5=98071db88cbaccd6a6b81cc3e09cba15CAS | 18155829PubMed |

De Sousa, P. A., Westhusin, M. E., and Watson, A. J. (1998). Analysis of variation in relative mRNA abundance for specific gene transcripts in single bovine oocytes and early embryos. Mol. Reprod. Dev. 49, 119–130.
Analysis of variation in relative mRNA abundance for specific gene transcripts in single bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1Oisw%3D%3D&md5=98bd92334e2ecfd84b346a8e0e750611CAS | 9444655PubMed |

Duranthon, V., Watson, A. J., and Lonergan, P. (2008). Preimplantation embryo programming: transcription, epigenetics, and culture environment. Reproduction 135, 141–150.
Preimplantation embryo programming: transcription, epigenetics, and culture environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1yrt7Y%3D&md5=e71f3ca19dd1c39de972c56558598bceCAS | 18239045PubMed |

Evans, M. J., and Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154–156.
Establishment in culture of pluripotential cells from mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3itV2qsg%3D%3D&md5=f45b2430ae990eda82cd127e24b6a1dbCAS | 7242681PubMed |

Foygel, K., Choi, B., Jun, S., Leong, D. E., Lee, A., Wong, C. C., Zuo, E., Eckart, M., Reijo Pera, R. A., Wong, W. H., and Yao, M. W. (2008). A novel and critical role for Oct4 as a regulator of the maternal–embryonic transition. PLoS ONE 3, e4109.
A novel and critical role for Oct4 as a regulator of the maternal–embryonic transition.Crossref | GoogleScholarGoogle Scholar | 19129941PubMed |

Gómez, M. C., Pope, C. E., Kutner, R. H., Ricks, D. M., Lyons, L. A., Ruhe, M., Dumas, C., Lyons, J., López, M., Dresser, B. L., and Reiser, J. (2008). Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning Stem Cells 10, 469–484.
Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells.Crossref | GoogleScholarGoogle Scholar | 18795868PubMed |

Gómez, M. C., Serrano, M. A., Pope, C. E., Jenkins, J. A., Biancardia, M. N., López, M., Dumas, C., Galiguis, J., and Dresser, B. L. (2010). Derivation of cat embryonic stem-like cells from in vitro-produced blastocysts on homologous and heterologous feeder cells. Theriogenology 74, 498–515.
Derivation of cat embryonic stem-like cells from in vitro-produced blastocysts on homologous and heterologous feeder cells.Crossref | GoogleScholarGoogle Scholar | 20708127PubMed |

Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A., and Peelman, L. (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 | GoogleScholarGoogle Scholar | 16324220PubMed |

Greber, B., Lehrach, H., and Adjaye, J. (2008). Control of early fate decisions in human ES cells by distinct states of TGFbeta pathway activity. Stem Cells Dev. 17, 1065–1078.
Control of early fate decisions in human ES cells by distinct states of TGFbeta pathway activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOju7bK&md5=a1ff425c444b2c1eceea9f50571b6bddCAS | 18393632PubMed |

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlaktA%3D%3D&md5=b29f6c6166456530046857eb35f14c3cCAS | 14723852PubMed |

Harvey, A. J., Armant, D. R., Bavister, B. D., Nichols, S. M., and Brenner, C. A. (2009). Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts. Stem Cells Dev. 18, 1451–1458.
Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslWitg%3D%3D&md5=6edfd1464f15cb9b4b54efdd29eb4be2CAS | 19537945PubMed |

Herrick, J. R., Bond, J. B., Magarey, G. M., Bateman, H. L., Krisher, R. L., Dunford, S. A., and Swanson, W. F. (2007). Toward a feline-optimized culture medium: impact of ions, carbohydrates, essential amino acids, vitamins, and serum on development and metabolism of in vitro fertilization-derived feline embryos relative to embryos grown in vivo. Biol. Reprod. 76, 858–870.
Toward a feline-optimized culture medium: impact of ions, carbohydrates, essential amino acids, vitamins, and serum on development and metabolism of in vitro fertilization-derived feline embryos relative to embryos grown in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1OhsLo%3D&md5=885e4f5031aeceab61096188879e2128CAS | 17267698PubMed |

Hoffert, K. A., Anderson, G. B., Wildt, D. E., and Roth, T. L. (1997). Transition from maternal to embryonic control of development in IVM/IVF domestic cat embryos. Mol. Reprod. Dev. 48, 208–215.
Transition from maternal to embryonic control of development in IVM/IVF domestic cat embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKms7o%3D&md5=397984c8741ed7c0c6caa1d0ae970658CAS | 9291470PubMed |

Imsoonthornruksa, S., Lorthongpanich, C., Sangmalee, A., Srirattana, K., Laowtammathron, C., Tunwattana, W., Somsa, W., Ketudat-Cairns, M., and Parnpai, R. (2010). Abnormalities in the transcription of reprogramming genes related to global epigenetic events of cloned endangered felid embryos. Reprod. Fertil. Dev. 22, 613–624.
Abnormalities in the transcription of reprogramming genes related to global epigenetic events of cloned endangered felid embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvF2isLo%3D&md5=cb6037cae3c33c8911b3fc642a288b5fCAS | 20353721PubMed |

Jedrusik, A., Bruce, A. W., Tan, M. H., Leong, D. E., Skamagki, M., Yao, M., and Zernicka-Goetz, M. (2010). Maternally and zygotically provided Cdx2 have novel and critical roles for early development of the mouse embryo. Dev. Biol. 344, 66–78.
Maternally and zygotically provided Cdx2 have novel and critical roles for early development of the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVClurfJ&md5=74a67a5917f74c05dd061e8c6fddbfcdCAS | 20430022PubMed |

Kessler, Y., Helfer-Hungerbuehler, A. K., Cattori, V., Meli, M. L., Zellweger, B., Ossent, P., Riond, B., Reusch, C. E., Lutz, H., and Hofmann-Lehmann, R. (2009). Quantitative TaqMan real-time PCR assays for gene expression normalisation in feline tissues. BMC Mol. Biol. 10, 106.
Quantitative TaqMan real-time PCR assays for gene expression normalisation in feline tissues.Crossref | GoogleScholarGoogle Scholar | 20003366PubMed |

Kimber, S. J., Sneddon, S. F., Bloor, D. J., El-Bareg, A. M., Hawkhead, J. A., Metcalfe, A. D., Houghton, F. D., Leese, H. J., Rutherford, A., Lieberman, B. A., and Brison, D. R. (2008). Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction 135, 635–647.
Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Wqur4%3D&md5=c88f6e2798384f40bafcaf17ee66b2bbCAS | 18411410PubMed |

Kirchhof, N., Carnwath, J. W., Lemme, E., Anastassiadis, K., Schöler, H., and Niemann, H. (2000). Expression pattern of Oct-4 in preimplantation embryos of different species. Biol. Reprod. 63, 1698–1705.
Expression pattern of Oct-4 in preimplantation embryos of different species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKhtrY%3D&md5=863842f823286619a97fcdd448ffb110CAS | 11090438PubMed |

Kuijk, E. W., Du Puy, L., Van Tol, H. T., Oei, C. H., Haagsman, H. P., Colenbrander, B., and Roelen, B. A. (2008). Differences in early lineage segregation between mammals. Dev. Dyn. 237, 918–927.
Differences in early lineage segregation between mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFaktbY%3D&md5=ec9af44ae6aa3aac8a43da8cf83b927aCAS | 18330925PubMed |

Kumar, B. M., Jin, H. F., Kim, J. G., Ock, S. A., Hong, Y., Balasubramanian, S., Choe, S. Y., and Rho, G. J. (2007). Differential gene expression patterns in porcine nuclear transfer embryos reconstructed with fetal fibroblasts and mesenchymal stem cells. Dev. Dyn. 236, 435–446.
Differential gene expression patterns in porcine nuclear transfer embryos reconstructed with fetal fibroblasts and mesenchymal stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisFamt70%3D&md5=16be06da0b512208a720411f724c0f65CAS | 17191234PubMed |

Kuroda, T., Tada, M., Kubota, H., Kimura, H., Hatano, S. Y., Suemori, H., Nakatsuji, N., and Tada, T. (2005). Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol. Cell. Biol. 25, 2475–2485.
Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVOiu7w%3D&md5=25f1f5edba77bcfd9c530ff9610e11b4CAS | 15743839PubMed |

Kurosaka, S., Eckardt, S., and McLaughlin, K. J. (2004). Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol. Reprod. 71, 1578–1582.
Pluripotent lineage definition in bovine embryos by Oct4 transcript localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1yisb0%3D&md5=177f5ce07d63e234039f084f70616610CAS | 15229144PubMed |

Latino, M. W., Chiang, T. C., Pope, C. E., Gomez, M. C., Giraldo, A. M., Harris, R. F., King, A. L., Dresser, B. L., and McLachlan, J. A. (2004). Estrogen receptor alpha and progesterone receptor expression from reproductive tissue and in vitro produced embryos of the domestic cat Reprod. Fertil. Dev. 16, 240.
Estrogen receptor alpha and progesterone receptor expression from reproductive tissue and in vitro produced embryos of the domestic catCrossref | GoogleScholarGoogle Scholar |

Li, X., Kato, Y., and Tsunoda, Y. (2005). Comparative analysis of development-related gene expression in mouse preimplantation embryos with different developmental potential. Mol. Reprod. Dev. 72, 152–160.
Comparative analysis of development-related gene expression in mouse preimplantation embryos with different developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1ygu7o%3D&md5=15f943ff97da61dbab0a10f869fc2202CAS | 16013066PubMed |

Lonergan, P., Rizos, D., Gutierrez-Adán, A., Moreira, P. M., Pintado, B., de la Fuente, J., and Boland, M. P. (2003). Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol. Reprod. 69, 1424–1431.
Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2ntrw%3D&md5=89b9da86d9c17b20bd7a16f29febca1aCAS | 12826577PubMed |

Magnani, L., and Cabot, R. A. (2008). In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development. Mol. Reprod. Dev. 75, 1726–1735.
In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyqsrzN&md5=9bd804b19fe8a1891dc1c13ca1e27088CAS | 18425776PubMed |

Mamo, S., Gal, A. B., Bodo, S., and Dinnyes, A. (2007). Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro. BMC Dev. Biol. 7, 14.
Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 17341302PubMed |

Mamo, S., Gal, A. B., Polgar, Z., and Dinnyes, A. (2008). Expression profiles of the pluripotency marker gene POU5F1 and validation of reference genes in rabbit oocytes and preimplantation stage embryos. BMC Mol. Biol. 9, 67.
Expression profiles of the pluripotency marker gene POU5F1 and validation of reference genes in rabbit oocytes and preimplantation stage embryos.Crossref | GoogleScholarGoogle Scholar | 18662377PubMed |

Merlo, B., Iacono, E., Regazzini, M., and Zambelli, D. (2008). Cat blastocysts produced in vitro from oocytes vitrified using the cryoloop technique and cryopreserved electroejaculated semen. Theriogenology 70, 126–130.
Cat blastocysts produced in vitro from oocytes vitrified using the cryoloop technique and cryopreserved electroejaculated semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1czms1anuw%3D%3D&md5=aa379e97d226369cb1abf6cdefc5de5eCAS | 18455226PubMed |

Mitalipov, S. M., Kuo, H. C., Hennebold, J. D., and Wolf, D. P. (2003). Oct-4 expression in pluripotent cells of the rhesus monkey. Biol. Reprod. 69, 1785–1792.
Oct-4 expression in pluripotent cells of the rhesus monkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCnsr0%3D&md5=5ae6e83cf3d18213f6c3b2465c3fee28CAS | 12890723PubMed |

Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631–642.
The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksFehur4%3D&md5=592859cd5c5e652ad665ecbcf93bb2c4CAS | 12787504PubMed |

Nganvongpanit, K., Müller, H., Rings, F., Gilles, M., Jennen, D., Hölker, M., Tholen, E., Schellander, K., and Tesfaye, D. (2006). Targeted suppression of E-cadherin gene expression in bovine preimplantation embryo by RNA interference technology using double-stranded RNA. Mol. Reprod. Dev. 73, 153–163.
Targeted suppression of E-cadherin gene expression in bovine preimplantation embryo by RNA interference technology using double-stranded RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjslygtg%3D%3D&md5=e9cf4dbb81605a458a63629ec22e7ad2CAS | 16250007PubMed |

Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H., and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–391.
Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlCqt74%3D&md5=b5fdaf1cbfe07b79c6dc0c202c80be92CAS | 9814708PubMed |

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 |

Niwa, H., Miyazaki, J., and Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372–376.
Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVCjsbo%3D&md5=1458132286cff2b99bc5eb4f875fac6eCAS | 10742100PubMed |

O’Brien, S. J., Menotti-Raymond, M., Murphy, W. J., and Yuhki, N. (2002). The Feline Genome Project. Annu. Rev. Genet. 36, 657–686.
The Feline Genome Project.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslertQ%3D%3D&md5=69236f40484b26bf423438fa0d8decb9CAS | 12359739PubMed |

Okumura-Nakanishi, S., Saito, M., Niwa, H., and Ishikawa, F. (2005). Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J. Biol. Chem. 280, 5307–5317.
Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCmuro%3D&md5=0497343a84eb647ad05a9833a8a6cdd5CAS | 15557334PubMed |

Ovitt, C. E., and Schöler, H. R. (1998). The molecular biology of Oct-4 in the early mouse embryo. Mol. Hum. Reprod. 4, 1021–1031.
The molecular biology of Oct-4 in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnslKntrw%3D&md5=ed8d6d518d485306a0eaaf2b5677f994CAS | 9835353PubMed |

Park, S. H., Park, S. B., and Kim, N. H. (2003). Expression of early development-related genes in bovine nuclear transferred and fertilized embryos. Zygote 11, 355–360.
Expression of early development-related genes in bovine nuclear transferred and fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFWjtLw%3D&md5=303b546a6022be8739e9b4bd575caf5fCAS | 15085736PubMed |

Penning, L. C., Vrieling, H. E., Brinkhof, B., Riemers, F. M., Rothuizen, J., Rutteman, G. R., and Hazewinkel, H. A. (2007). A validation of 10 feline reference genes for gene expression measurements in snap-frozen tissues. Vet. Immunol. Immunopathol. 120, 212–222.
A validation of 10 feline reference genes for gene expression measurements in snap-frozen tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1agsr%2FI&md5=7e29ae55bd2cd5f4ea1ec13b910bf900CAS | 17904230PubMed |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45e.
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar |

Plusa, B., Piliszek, A., Frankenberg, S., Artus, J., and Hadjantonakis, A. K. (2008). Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081–3091.
Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlansrbE&md5=c524f25d6bc38f771c654c2606bef779CAS | 18725515PubMed |

Pope, C. E., Gómez, M. C., and Dresser, B. L. (2006). In vitro production and transfer of cat embryos in the 21st century. Theriogenology 66, 59–71.
In vitro production and transfer of cat embryos in the 21st century.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zls1KmtA%3D%3D&md5=d4e997dbe601946e5a8896dbde41b003CAS | 16620940PubMed |

Ralston, A., and Rossant, J. (2008). Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 313, 614–629.
Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsFGrsA%3D%3D&md5=dbc9c1f7984bda166435c701e93cf877CAS | 18067887PubMed |

Rinaudo, P., and Schultz, R. M. (2004). Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction 128, 301–311.
Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KitLg%3D&md5=7dd92bc8f497d487d44ab18eab19e762CAS | 15333781PubMed |

Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., de la Fuente, J., and Gutiérrez-Adán, 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 |

Rodda, D. J., Chew, J. L., Lim, L. H., Loh, Y. H., Wang, B., Ng, H. H., and Robson, P. (2005). Transcriptional regulation of nanog by OCT4 and SOX2. J. Biol. Chem. 280, 24 731–24 737.
Transcriptional regulation of nanog by OCT4 and SOX2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFyqs78%3D&md5=6dd55bd58034a78bf0f6879e61e6df7fCAS |

Rossant, J., and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701–713.
Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVSrurs%3D&md5=8a8f9bedb343dca19afcb60a195b6176CAS | 19201946PubMed |

Roth, T. L., Swanson, W. F., and Wildt, D. E. (1994). Developmental competence of domestic cat embryos fertilized in vivo versus in vitro. Biol. Reprod. 51, 441–451.
Developmental competence of domestic cat embryos fertilized in vivo versus in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7gtFylsg%3D%3D&md5=7a44ff002ad658983c4e60416223cf57CAS | 7803615PubMed |

Schöler, H. R., Ruppert, S., Suzuki, N., Chowdhury, K., and Gruss, P. (1990). New type of POU domain in germ line-specific protein Oct-4. Nature 344, 435–439.
New type of POU domain in germ line-specific protein Oct-4.Crossref | GoogleScholarGoogle Scholar | 1690859PubMed |

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 |

Sritanaudomchai, H., Sparman, M., Tachibana, M., Clepper, L., Woodward, J., Gokhale, S., Wolf, D., Hennebold, J., Hurlbut, W., Grompe, M., and Mitalipov, S. (2009). CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev. Biol. 335, 179–187.
CDX2 in the formation of the trophectoderm lineage in primate embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OnsrzN&md5=33b47d0f550e3f348d0bf8d52dee8ca1CAS | 19733166PubMed |

Strumpf, D., Mao, C. A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F., and Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093–2102.
Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFagsbs%3D&md5=3dd31832c98b5a1f02edc18f43a20668CAS | 15788452PubMed |

Thomson, J. A., Kalishman, J., Golos, T. G., Durning, M., Harris, C. P., Becker, R. A., and Hearn, J. P. (1995). Isolation of a primate embryonic stem cell line. Proc. Natl Acad. Sci. USA 92, 7844–7848.
Isolation of a primate embryonic stem cell line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsFOnt7w%3D&md5=737913d8af69bf44a491e6741324d859CAS | 7544005PubMed |

Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145–1147.
Embryonic stem cell lines derived from human blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntleisLg%3D&md5=7ba414d405c31a3c4df09740a68297deCAS | 9804556PubMed |

Tielens, S., Verhasselt, B., Liu, J., Dhont, M., Van Der Elst, J., and Cornelissen, M. (2006). Generation of embryonic stem cell lines from mouse blastocysts developed in vivo and in vitro: relation to Oct-4 expression. Reproduction 132, 59–66.
Generation of embryonic stem cell lines from mouse blastocysts developed in vivo and in vitro: relation to Oct-4 expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1Ogtr0%3D&md5=d6f050d203a441bdd31467d26e957548CAS | 16816333PubMed |

van Eijk, M. J., van Rooijen, M. A., Modina, S., Scesi, L., Folkers, G., van Tol, H. T., Bevers, M. M., Fisher, S. R., Lewin, H. A., Rakacolli, D., Galli, C., de Vaureix, C., Trounson, A. O., Mummery, C. L., and Gandolfi, F. (1999). Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol. Reprod. 60, 1093–1103.
Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislegt7k%3D&md5=20cc1fde832b47e09bcb2a4b4e6f9100CAS | 10208969PubMed |

Van Soom, A., and de Kruif, A. (1998). Bovine embryonic development after in vivo and in vitro fertilization. Reprod. Domest. Anim. 33, 261–265.
Bovine embryonic development after in vivo and in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |

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, 34.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |

Waurich, R., Ringleb, J., Braun, B. C., and Jewgenow, K. (2010). Embryonic gene activation in in vitro produced embryos of the domestic cat (Felis catus). Reproduction 140, 531–540.
Embryonic gene activation in in vitro produced embryos of the domestic cat (Felis catus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCqurrP&md5=777bf9e3717cf7feb32b12b76abc45d6CAS | 20660570PubMed |

Wildt, D. E., Chan, S. Y., Seager, S. W., and Chakraborty, P. K. (1981). Ovarian activity, circulating hormones, and sexual behavior in the cat. I. Relationships during the coitus-induced luteal phase and the estrous period without mating. Biol. Reprod. 25, 15–28.
Ovarian activity, circulating hormones, and sexual behavior in the cat. I. Relationships during the coitus-induced luteal phase and the estrous period without mating.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltlSgtb4%3D&md5=3b06b3bd86dbf08e87d15eb3094a873aCAS | 7197173PubMed |

Wood, T. C., and Wildt, D. E. (1997). Effect of the quality of the cumulus–oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize and develop into blastocysts in vitro. J. Reprod. Fertil. 110, 355–360.
Effect of the quality of the cumulus–oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize and develop into blastocysts in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKrsL0%3D&md5=795d6d37397b7d39e2c5ad01ba275bc9CAS | 9306990PubMed |

Yu, X. F., Kim, J. H., Jung, E. J., Jeon, J. T., and Kong, I. K. (2009). Cloning and characterization of cat POU5F1 and NANOG for identification of embryonic stem-like cells. J. Reprod. Dev. 55, 361–366.
Cloning and characterization of cat POU5F1 and NANOG for identification of embryonic stem-like cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOmtLnL&md5=bdeb4f30711a12198e143f97da8087e3CAS | 19293558PubMed |

Zuccotti, M., Merico, V., Sacchi, L., Bellone, M., Brink, T. C., Bellazzi, R., Stefanelli, M., Redi, C. A., Garagna, S., and Adjaye, J. (2008). Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Dev. Biol. 8, 97.
Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 18837968PubMed |