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Vertebrate reproductive science and technology
RESEARCH ARTICLE

In vitro culture of stem-like cells derived from somatic cell nuclear transfer bovine embryos of the Korean beef cattle species, HanWoo

Daehwan Kim A , Sangkyu Park A , Yeon-Gil Jung B and Sangho Roh A C
+ Author Affiliations
- Author Affiliations

A Cellular Reprogramming and Embryo Biotechnology Laboratory, Dental Research Institute, Seoul National University School of Dentistry, 101, Daehak-ro, Jongno-gu, Seoul 110-744, Republic of Korea.

B ET Biotech Co. Ltd, 560-34, Ssarijae-ro, Jangsu-gun, Jeollabuk-do 597-851, Republic of Korea.

C Corresponding author. Email: sangho@snu.ac.kr

Reproduction, Fertility and Development 28(11) 1762-1780 https://doi.org/10.1071/RD14071
Submitted: 22 February 2014  Accepted: 12 April 2015   Published: 13 May 2015

Abstract

We established and maintained somatic cell nuclear transfer embryo-derived stem-like cells (SCNT-eSLCs) from the traditional Korean beef cattle species, HanWoo (Bos taurus coreanae). Each SCNT blastocyst was placed individually on a feeder layer with culture medium containing three inhibitors of differentiation (3i). Primary colonies formed after 2–3 days of culture and the intact colonies were passaged every 5–6 days. The cells in each colony showed embryonic stem cell-like morphologies with a distinct boundary and were positive to alkaline phosphatase staining. Immunofluorescence and reverse transcription–polymerase chain reaction analyses also confirmed that these colonies expressed pluripotent markers. The colonies were maintained over 50 passages for more than 270 days. The cells showed normal karyotypes consisting of 60 chromosomes at Passage 50. Embryoid bodies were formed by suspension culture to analyse in vitro differentiation capability. Marker genes representing the differentiation into three germ layers were expressed. Typical embryonal carcinoma was generated after injecting cells under the testis capsule of nude mice, suggesting that the cultured cells may also have the potential of in vivo differentiation. In conclusion, we generated eSLCs from SCNT bovine embryos, using a 3i system that sustained stemness, normal karyotype and pluripotency, which was confirmed by in vitro and in vivo differentiation.

Additional keywords: bovine, embryonic stem cell, small molecule.


References

Amit, M., Carpenter, M. K., Inokuma, M. S., Chiu, C. P., Harris, C. P., Waknitz, M. A., Itskovitz-Eldor, J., and Thomson, J. A. (2000). Clonally derived human embryonic stem-cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev. Biol. 227, 271–278.
Clonally derived human embryonic stem-cell lines maintain pluripotency and proliferative potential for prolonged periods of culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVeks70%3D&md5=9d9a2c4bdd9fb5f678c65b990cba0b22CAS | 11071754PubMed |

Anand, T., Kumar, D., Singh, M. K., Shah, R. A., Chauhan, M. S., Manik, R. S., Singla, S. K., and Palta, P. (2011). Buffalo (Bubalus bubalis) embryonic stem cell-like cells and preimplantation embryos exhibit comparable expression of pluripotency-related antigens. Reprod. Domest. Anim. 46, 50–58.
Buffalo (Bubalus bubalis) embryonic stem cell-like cells and preimplantation embryos exhibit comparable expression of pluripotency-related antigens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itlChuw%3D%3D&md5=7a6e29388c419133c4382cc8365ec564CAS | 20042025PubMed |

Baguisi, A., Behboodi, E., Melican, D. T., Pollock, J. S., Destrempes, M. M., Cammuso, C., Williams, J. L., Nims, S. D., Porter, C. A., Midura, P., Palacios, M. J., Ayres, S. L., Denniston, R. S., Hayes, M. L., Ziomek, C. A., Meade, H. M., Godke, R. A., Gavin, W. G., Overstrom, E. W., and Echelard, Y. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–461.
Production of goats by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFWrsbY%3D&md5=93cb13cd2d050dd80cdb25060ce9056eCAS | 10331804PubMed |

Barber, A. L., and Foran, D. R. (2006). The utility of whole-genome amplification for typing compromised forensic samples. J. Forensic Sci. 51, 1344–1349.
The utility of whole-genome amplification for typing compromised forensic samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt12rt78%3D&md5=15a76086453fddecfb13ea4173c90099CAS | 17199620PubMed |

Böttcher, R. T., and Niehrs, C. (2005). Fibroblast growth factor signalling during early vertebrate development. Endocr. Rev. 26, 63–77.
Fibroblast growth factor signalling during early vertebrate development.Crossref | GoogleScholarGoogle Scholar | 15689573PubMed |

Brons, I. G., Smithers, L. E., Trotter, M. W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S. M., Howlett, S. K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R. A., and Vallier, L. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191–195.
Derivation of pluripotent epiblast stem cells from mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsFeisbw%3D&md5=05e3cb2588f5ecfddec217c858d913a9CAS | 17597762PubMed |

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=6254c42e0c11121f48f8573cb113a554CAS | 19109897PubMed |

Burdon, T., Stracey, C., Chambers, I., Nichols, J., and Smith, A. (1999). Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol. 210, 30–43.
Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1Gntr4%3D&md5=50dc6e0756f4733c261c2c5cedc68edaCAS | 10364425PubMed |

Cao, S., Wang, F., Chen, Z., Liu, Z., Mei, C., Wu, H., Huang, J., Li, C., Zhou, L., and Liu, L. (2009). Isolation and culture of primary bovine embryonic stem-cell colonies by a novel method. J. Exp. Zool. A. Ecol. Genet. Physiol. 311A, 368–376.
Isolation and culture of primary bovine embryonic stem-cell colonies by a novel method.Crossref | GoogleScholarGoogle Scholar |

Cao, H., Yang, P., Pu, Y., Sun, X., Yin, H., Zhang, Y., Zhang, Y., Li, Y., Liu, Y., Fang, F., Zhang, Z., Tao, Y., and Zhang, X. (2012). Characterisation of bovine induced pluripotent stem cells by lentiviral transduction of reprogramming factor fusion proteins. Int. J. Biol. Sci. 8, 498–511.
Characterisation of bovine induced pluripotent stem cells by lentiviral transduction of reprogramming factor fusion proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVOmt7s%3D&md5=37eeb453abf456bbcdbe31352649bd46CAS | 22457605PubMed |

Carpenter, M. K., Rosler, E. S., Fisk, G. J., Brandenberger, R., Ares, X., Miura, T., Lucero, M., and Rao, M. S. (2004). Properties of four human embryonic stem-cell lines maintained in a feeder-free culture system. Dev. Dyn. 229, 243–258.
Properties of four human embryonic stem-cell lines maintained in a feeder-free culture system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvVektbo%3D&md5=5d1fedd85021b40771e53de14bf979a1CAS | 14745950PubMed |

Cibelli, J. B., Stice, S. L., Golueke, P. J., Kane, J. J., Jerry, J., Blackwell, C., de Leon, F. A. P., and Robl, J. M. (1998). Transgenic bovine chimeric offspring produced from somatic cell-derived stem-like cells. Nat. Biotechnol. 16, 642–646.
Transgenic bovine chimeric offspring produced from somatic cell-derived stem-like cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkt1Gntbo%3D&md5=624bbd266e72d3ad4a3ad5f9c144a5c3CAS | 9661197PubMed |

Denicol, A. C., Dobbs, K. B., McLean, K. M., Carambula, S. F., Loureiro, B., and Hansen, P. J. (2013). Canonical WNT signalling regulates development of bovine embryos to the blastocyst stage. Sci. Rep. 3, 1266.
Canonical WNT signalling regulates development of bovine embryos to the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 23405280PubMed |

Desmarais, J. A., Demers, S. P., Suzuki, J., Laflamme, S., Vincent, P., Laverty, S., and Smith, L. C. (2011). Trophoblast stem-cell marker gene expression in inner cell mass-derived cells from parthenogenetic equine embryos. Reproduction 141, 321–332.
Trophoblast stem-cell marker gene expression in inner cell mass-derived cells from parthenogenetic equine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1Crtrg%3D&md5=2910f922eeb44f3e237a3bd0f4dbab7aCAS | 21209071PubMed |

Edwards, J. L., Powell, A. M., and Rexroad, C. E. (2003). Alkaline phosphatase activity in bovine oocytes and preimplantation embryos as affected by removal of the zona pellucida and culture medium constituents. Reprod. Fertil. Dev. 15, 285–292.
Alkaline phosphatase activity in bovine oocytes and preimplantation embryos as affected by removal of the zona pellucida and culture medium constituents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Cgtbc%3D&md5=593b847f918d9cb7ab40fff85f7fafa1CAS | 14588186PubMed |

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=53e8a1254021955c54e881d5472d75f8CAS | 7242681PubMed |

Fujii, T., Moriyasu, S., Hirayama, H., Hashizume, T., and Sawai, K. (2010). Aberrant expression patterns of genes involved in segregation of inner cell mass and trophectoderm lineages in bovine embryos derived from somatic cell nuclear transfer. Cell. Reprogram. 12, 617–625.
Aberrant expression patterns of genes involved in segregation of inner cell mass and trophectoderm lineages in bovine embryos derived from somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2nt7jJ&md5=d1db9c3e9070834e5603f7ce8dd4c2d5CAS | 20726774PubMed |

Garry, F. B., Adams, R., McCann, J. P., and Odde, K. G. (1996). Postnatal characteristics of calves produced by nuclear transfer cloning. Theriogenology 45, 141–152.
Postnatal characteristics of calves produced by nuclear transfer cloning.Crossref | GoogleScholarGoogle Scholar |

Gjørret, J. O., and Maddox-Hyttel, P. (2005). Attempts towards derivation and establishment of bovine embryonic stem cell-like cultures. Reprod. Fertil. Dev. 17, 113–124.
Attempts towards derivation and establishment of bovine embryonic stem cell-like cultures.Crossref | GoogleScholarGoogle Scholar | 15745636PubMed |

Gong, G., Roach, M. L., Jiang, L., Yang, X., and Tian, X. C. (2010). Culture conditions and enzymatic passaging of bovine ESC-like cells. Cell. Reprogram. 12, 151–160.
Culture conditions and enzymatic passaging of bovine ESC-like cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVahtL4%3D&md5=0457d0714dc7f8acbdfa151f49af8db9CAS | 20677930PubMed |

Hasler, J. F., Henderson, W. B., Hurtgen, P. J., Jin, Z. Q., Mccauley, A. D., Mower, S. A., Neely, B., Shuey, L. S., Stokes, J. E., and Trimmer, S. A. (1995). Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43, 141–152.
Production, freezing and transfer of bovine IVF embryos and subsequent calving results.Crossref | GoogleScholarGoogle Scholar |

Hayashi, K., Lopes, S. M., Tang, F., and Surani, M. A. (2008). Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3, 391–401.
Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12it7bJ&md5=c781cecd54f6a6f0a2c737419811c0c8CAS | 18940731PubMed |

Huang, B., Li, T., Alonso-Gonzalez, L., Gorre, R., Keatley, S., Green, A., Turner, P., Kallingappa, P. K., Verma, V., and Oback, B. (2011). A virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition. PLoS One 6, e24501.
A virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1alur7L&md5=6118b5c8e23dd24cf1a0d5e28a158605CAS | 21912700PubMed |

Huang, X., Han, X., Uyunbilig, B., Zhang, M., Duo, S., Zuo, Y., Zhao, Y., Yun, T., Tai, D., Wang, C., Li, J., Li, X., and Li, R. (2014). Establishment of bovine trophoblast stem-like cells from in vitro-produced blastocyst-stage embryos using two inhibitors. Stem Cells Dev , .
Establishment of bovine trophoblast stem-like cells from in vitro-produced blastocyst-stage embryos using two inhibitors.Crossref | GoogleScholarGoogle Scholar | 24605918PubMed |

Jin, M., Wu, A., Dorzhin, S., Yue, Q., Ma, Y., and Liu, D. (2012). Culture conditions for bovine embryonic stem cell-like cells isolated from blastocysts after external fertilisation. Cytotechnology 64, 379–389.
Culture conditions for bovine embryonic stem cell-like cells isolated from blastocysts after external fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGhtLnL&md5=502c6cbb16859218a52117a1b2b135b8CAS | 22438181PubMed |

Kato, Y., Tani, T., Sotomaru, Y., Kurokawa, K., Kato, J., Doguchi, H., Yasue, H., and Tsunoda, Y. (1998). Eight calves cloned from somatic cells of a single adult. Science 282, 2095–2098.
Eight calves cloned from somatic cells of a single adult.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVyisro%3D&md5=17caba6a2a32ce9fc785e8acb0206d00CAS | 9851933PubMed |

Kim, M. K., Jang, G., Oh, H. J., Yuda, F., Kim, H. J., Hwang, W. S., Hossein, M. S., Kim, J. J., Shin, N. S., Kang, S. K., and Lee, B. C. (2007). Endangered wolves cloned from adult somatic cells. Cloning Stem Cells 9, 130–137.
Endangered wolves cloned from adult somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVWrtLs%3D&md5=abd3ef53e3c3320099ad97f7ca1f9231CAS | 17386020PubMed |

Kim, D., Park, S., and Roh, S. (2012). Comparison of three different culture systems for establishment and long-term culture of embryonic stem-like cells from in vitro-produced bovine embryos. J. Emb. Trans. 27, 189–192.

Kirchhof, N., Carnwath, J. W., Lemme, E., Anastassiadis, K., Scholer, 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=cef974602365f0f39dfa0869280df1d7CAS | 11090438PubMed |

Kuckenberg, P., Peitz, M., Kubaczka, C., Becker, A., Egert, A., Wardelmann, E., Zimmer, A., Brustle, O., and Schorle, H. (2011). Lineage conversion of murine extraembryonic trophoblast stem cells to pluripotent stem cells. Mol. Cell. Biol. 31, 1748–1756.
Lineage conversion of murine extraembryonic trophoblast stem cells to pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFSjtr8%3D&md5=cc9ff425751c85f2362769236753f2d7CAS | 21300784PubMed |

Kuijk, E. W., van Tol, L. T., Van de Velde, H., Wubbolts, R., Welling, M., Geijsen, N., and Roelen, B. A. (2012). The roles of FGF and MAP kinase signalling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 139, 871–882.
The roles of FGF and MAP kinase signalling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmsl2hu7c%3D&md5=8f8577234fbc3bf76abfbf413b724921CAS | 22278923PubMed |

Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S., and Smith, A. (2007). FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895–2902.
FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2qtL3O&md5=30ac22ae98b2d5e6aa48ff5f6073428bCAS | 17660198PubMed |

Kwon, D. K., Hong, S. G., Park, H. J., Kang, J. T., Koo, O. J., and Lee, B. C. (2009). Epiblast isolation by a new four-stage method (peeling) from whole bovine cloned blastocysts. Cell Biol. Int. 33, 309–317.
Epiblast isolation by a new four-stage method (peeling) from whole bovine cloned blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWmu7Y%3D&md5=bb29e5dc5f6edfe5acf168300d16891aCAS | 19166954PubMed |

Lai, L., Park, K. W., Cheong, H. T., Kuhholzer, B., Samuel, M., Bonk, A., Im, G. S., Rieke, A., Day, B. N., Murphy, C. N., Carter, D. B., and Prather, R. S. (2002). Transgenic pig expressing the enhanced green fluorescent protein produced by nuclear transfer using colchicine-treated fibroblasts as donor cells. Mol. Reprod. Dev. 62, 300–306.
Transgenic pig expressing the enhanced green fluorescent protein produced by nuclear transfer using colchicine-treated fibroblasts as donor cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWkurc%3D&md5=10f7cd07ee25758f8eaa734111218c61CAS | 12112592PubMed |

Li, M., Zhang, D., Hou, Y., Jiao, L., Zheng, X., and Wang, W. H. (2003). Isolation and culture of embryonic stem cells from porcine blastocysts. Mol. Reprod. Dev. 65, 429–434.
Isolation and culture of embryonic stem cells from porcine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVKqu70%3D&md5=dfc0e1444c3e36974ac42cf215dece69CAS | 12840816PubMed |

Lim, M. L., Vassiliev, I., Richings, N. M., Firsova, A. B., Zhang, C., and Verma, P. J. (2011). A novel, efficient method to derive bovine and mouse embryonic stem cells with in vivo differentiation potential by treatment with 5-azacytidine. Theriogenology 76, 133–142.
A novel, efficient method to derive bovine and mouse embryonic stem cells with in vivo differentiation potential by treatment with 5-azacytidine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFKitbs%3D&md5=81ca89934e14ebd2f128b18e8d9469d6CAS | 21396694PubMed |

Liu, J., Gotherstrom, C., Forsberg, M., Samuelsson, E. B., Wu, J., Calzarossa, C., Hovatta, O., Sundstrom, E., and Akesson, E. (2013). Human neural stem/progenitor cells derived from embryonic stem cells and fetal nervous system present differences in immunogenicity and immunomodulatory potentials in vitro. Stem Cell Res. 10, 325–337.
Human neural stem/progenitor cells derived from embryonic stem cells and fetal nervous system present differences in immunogenicity and immunomodulatory potentials in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1Cis7k%3D&md5=3591a0c55164f014324206f262d7e270CAS | 23416350PubMed |

Madeja, Z. E., Sosnowski, J., Hryniewicz, K., Warzych, E., Pawlak, P., Rozwadowska, N., Plusa, B., and Lechniak, D. (2013). Changes in sub-cellular localisation of trophoblast- and inner cell mass-specific transcription factors during bovine preimplantation development. BMC Dev. Biol. 13, 32.
Changes in sub-cellular localisation of trophoblast- and inner cell mass-specific transcription factors during bovine preimplantation development.Crossref | GoogleScholarGoogle Scholar | 23941255PubMed |

Martin, G. R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 78, 7634–7638.
Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387ltV2htg%3D%3D&md5=2cf6022623569f56e272f079daaf126aCAS | 6950406PubMed |

McLean, Z., Meng, F., Henderson, H., Turner, P., and Oback, B. (2014). Increased MAP kinase inhibition enhances epiblast-specific gene expression in bovine blastocysts. Biol. Reprod. 91, 49.
Increased MAP kinase inhibition enhances epiblast-specific gene expression in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 25009207PubMed |

Mitalipova, M., Beyhan, Z., and First, N. L. (2001). Pluripotency of bovine embryonic cell line derived from precompacting embryos. Cloning 3, 59–67.
Pluripotency of bovine embryonic cell line derived from precompacting embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387mvFSltg%3D%3D&md5=0f5718048d8feba46a7d66d6c34d05e5CAS | 11900640PubMed |

Muñoz, M., Diez, C., Caamaño, J. N., Jouneau, A., Hue, I., and Gómez, E. (2008a). Embryonic stem cells in cattle. Reprod. Domest. Anim. 43, 32–37.
Embryonic stem cells in cattle.Crossref | GoogleScholarGoogle Scholar | 18803754PubMed |

Muñoz, M., Rodríguez, A., De Frutos, C., Caamaño, J. N., Díez, C., Facal, N., and Gómez, E. (2008b). Conventional pluripotency markers are unspecific for bovine embryonic-derived cell lines. Theriogenology 69, 1159–1164.
Conventional pluripotency markers are unspecific for bovine embryonic-derived cell lines.Crossref | GoogleScholarGoogle Scholar | 18420262PubMed |

Nichols, J., and Smith, A. (2009). Naive and primed pluripotent states. Cell Stem Cell 4, 487–492.
Naive and primed pluripotent states.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt1Ggt7c%3D&md5=82e5e044fc4d310cbebad136e49c1e79CAS | 19497275PubMed |

Niemann, H., and Kues, W. A. (2007). Transgenic farm animals: an update. Reprod. Fertil. Dev. 19, 762–770.
Transgenic farm animals: an update.Crossref | GoogleScholarGoogle Scholar | 17714630PubMed |

Nordhoff, V., Hubner, K., Bauer, A., Orlova, I., Malapetsa, A., and Scholer, H. R. (2001). Comparative analysis of human, bovine and murine Oct-4 upstream promoter sequences. Mamm. Genome 12, 309–317.
Comparative analysis of human, bovine and murine Oct-4 upstream promoter sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis12jsL8%3D&md5=1063b99ea8aa63f5736618166cb7611eCAS | 11309664PubMed |

Nouspikel, T. (2013). Genetic instability in human embryonic stem cells: prospects and caveats. Future Oncol. 9, 867–877.
Genetic instability in human embryonic stem cells: prospects and caveats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotlChsb4%3D&md5=9f758aace9e14661559c05d8875d544eCAS | 23718307PubMed |

Ozawa, M., Sakatani, M., Yao, J., Shanker, S., Yu, F., Yamashita, R., Wakabayashi, S., Nakai, K., Dobbs, K. B., Sudano, M. J., Farmerie, W. G., and Hansen, P. J. (2012). Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev. Biol. 12, 33.
Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvA%3D%3D&md5=2084b46dd55b69f4f02702b642c2de63CAS | 23126590PubMed |

Palmieri, S. L., Peter, W., Hess, H., and Scholer, H. R. (1994). Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev. Biol. 166, 259–267.
Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Olu74%3D&md5=1742a50828a97d75d4670596e970442eCAS | 7958450PubMed |

Pashaiasl, M., Khodadadi, K., Holland, M. K., and Verma, P. J. (2010). The efficient generation of cell lines from bovine parthenotes. Cell. Reprogram. 12, 571–579.
The efficient generation of cell lines from bovine parthenotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2nt7jM&md5=a9cd6d6db5ef51b8b81d90ce789510f2CAS | 20936907PubMed |

Pashaiasl, M., Khodadadi, K., Richings, N. M., Holland, M. K., and Verma, P. J. (2013). Cryopreservation and long-term maintenance of bovine embryo-derived cell lines. Reprod. Fertil. Dev. 25, 707–718.
Cryopreservation and long-term maintenance of bovine embryo-derived cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1Cgs7c%3D&md5=7a63996b6cdf832d0d4625faf76b44c0CAS | 22951106PubMed |

Roach, M., Wang, L., Yang, X., and Tian, X. C. (2006). Bovine embryonic stem cells. Methods Enzymol. 418, 21–37.
Bovine embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtFKisbY%3D&md5=00b9b1f57969479753653525f72546f3CAS | 17141027PubMed |

Roberts, R. M., and Fisher, S. J. (2011). Trophoblast stem cells. Biol. Reprod. 84, 412–421.
Trophoblast stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1Omtr0%3D&md5=41eae03869e07a76761022fc4cd9ef20CAS | 21106963PubMed |

Saito, S., Strelchenko, N., and Niemann, H. (1992). Bovine embryonic stem cell-like cell lines cultured over several passages. Rouxs Arch. Dev. Biol. 201, 134–141.
Bovine embryonic stem cell-like cell lines cultured over several passages.Crossref | GoogleScholarGoogle Scholar |

Sato, N., Sanjuan, I. M., Heke, M., Uchida, M., Naef, F., and Brivanlou, A. H. (2003). Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev. Biol. 260, 404–413.
Molecular signature of human embryonic stem cells and its comparison with the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1WqtL0%3D&md5=b468e072b216c01fbc479bb72bd5e066CAS | 12921741PubMed |

Schiffmacher, A. T., and Keefer, C. L. (2013). CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT-1 cells. Mol. Reprod. Dev. 80, 826–839.
CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT-1 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGltb%2FL&md5=400fbf25b969e52175fc7961361ee78fCAS | 23836438PubMed |

Seabright, M. (1971). A rapid banding technique for human chromosomes. Lancet 298, 971–972.
A rapid banding technique for human chromosomes.Crossref | GoogleScholarGoogle Scholar |

Semb, H. (2005). Human embryonic stem cells: origin, properties and applications. APMIS 113, 743–750.
Human embryonic stem cells: origin, properties and applications.Crossref | GoogleScholarGoogle Scholar | 16480446PubMed |

Semino, C. E., Merok, J. R., Crane, G. G., Panagiotakos, G., and Zhang, S. (2003). Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71, 262–270.
Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsl2ru7s%3D&md5=5a04c8264cd48642214ea29b7cc03b64CAS | 12823227PubMed |

Silva, J., Nichols, J., Theunissen, T. W., Guo, G., van Oosten, A. L., Barrandon, O., Wray, J., Yamanaka, S., Chambers, I., and Smith, A. (2009). Nanog is the gateway to the pluripotent ground state. Cell 138, 722–737.
Nanog is the gateway to the pluripotent ground state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjs7rI&md5=09ac9dd4e6111fb58f9fb7be60d6359fCAS | 19703398PubMed |

Sineva, G. S., and Pospelov, V. A. (2010). Inhibition of GSK3beta enhances both adhesive and signalling activities of beta-catenin in mouse embryonic stem cells. Biol. Cell 102, 549–564.
Inhibition of GSK3beta enhances both adhesive and signalling activities of beta-catenin in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSntb%2FJ&md5=368a3acd734fd755f1110d906cb712fdCAS | 20626347PubMed |

Sperger, J. M., Chen, X., Draper, J. S., Antosiewicz, J. E., Chon, C. H., Jones, S. B., Brooks, J. D., Andrews, P. W., Brown, P. O., and Thomson, J. A. (2003). Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc. Natl. Acad. Sci. USA 100, 13350–13355.
Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFOisL0%3D&md5=cf65b6afa237260fbc02a621da1f4d30CAS | 14595015PubMed |

Stavridis, M. P., Lunn, J. S., Collins, B. J., and Storey, K. G. (2007). A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 134, 2889–2894.
A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2qtL3M&md5=1f88cc23b37ca059ad1d66ed5488429fCAS | 17660197PubMed |

Stewart, M. H., Bosse, M., Chadwick, K., Menendez, P., Bendall, S. C., and Bhatia, M. (2006). Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem-cell compartment. Nat. Methods 3, 807–815.
Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem-cell compartment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVCmtbo%3D&md5=248f90e399adc1a920f45e5ddf1a515dCAS | 16990813PubMed |

Stice, S. L., Strelchenko, N. S., Keefer, C. L., and Matthews, L. (1996). Pluripotent bovine embryonic cell lines direct embryonic development following nuclear transfer. Biol. Reprod. 54, 100–110.
Pluripotent bovine embryonic cell lines direct embryonic development following nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLvN&md5=8298dbeac213d52eba60ad4bd79cd84aCAS | 8838006PubMed |

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=0cfe0d4dae2d8fceef58b5a27fdd9d0aCAS | 15788452PubMed |

Suadi, Z., Siew, L. C., Tie, R., Hui, W. B., Asam, A., Thiew, S. H., and Boon, L. K. (2007). STR data for the AmpFlSTR Identifiler loci from the three main ethnic indigenous population groups (Iban, Bidayuh and Melanau) in Sarawak, Malaysia. J. Forensic Sci. 52, 231–234.
STR data for the AmpFlSTR Identifiler loci from the three main ethnic indigenous population groups (Iban, Bidayuh and Melanau) in Sarawak, Malaysia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1anu74%3D&md5=092c6a463546aa0fdf5aaa369cfb164bCAS | 17209948PubMed |

Tachibana, M., Amato, P., Sparman, M., Gutierrez, N. M., Tippner-Hedges, R., Ma, H., Kang, E., Fulati, A., Lee, H. S., Sritanaudomchai, H., Masterson, K., Larson, J., Eaton, D., Sadler-Fredd, K., Battaglia, D., Lee, D., Wu, D., Jensen, J., Patton, P., Gokhale, S., Stouffer, R. L., Wolf, D., and Mitalipov, S. (2013). Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 153, 1228–1238.
Human embryonic stem cells derived by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsleqsro%3D&md5=7ddd9b33a4ca689025763ce30ed092c6CAS | 23683578PubMed |

Talbot, N. C., Powell, A. M., and Rexroad, C. E. (1995). In vitro pluripotency of epiblasts derived from bovine blastocysts. Mol. Reprod. Dev. 42, 35–52.
In vitro pluripotency of epiblasts derived from bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnvVGlu78%3D&md5=786180639ca31f6e95ef299bc78ff335CAS | 8562049PubMed |

Talbot, N. C., Caperna, T. J., Edwards, J. L., Garrett, W., Wells, K. D., and Ealy, A. D. (2000). Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers. Biol. Reprod. 62, 235–247.
Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOktw%3D%3D&md5=34f8e3f37924cb6ad56a6c92f0934e0eCAS | 10642558PubMed |

Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A., and Rossant, J. (1998). Promotion of trophoblast stem-cell proliferation by FGF4. Science 282, 2072–2075.
Promotion of trophoblast stem-cell proliferation by FGF4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVOqsrk%3D&md5=c09caf969726ad3b38609f6ac10a2833CAS | 9851926PubMed |

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=11f035eb174df39c86d69e2936df0b09CAS | 9804556PubMed |

Tiruthani, K., Sarkar, P., and Rao, B. (2013). Trophoblast differentiation of human embryonic stem cells. Biotechnol. J. 8, 421–433.
Trophoblast differentiation of human embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlGgtA%3D%3D&md5=c9b7d810fe8a62571b060bc76a47bb0cCAS | 23325630PubMed |

Ushizawa, K., Takahashi, T., Kaneyama, K., Tokunaga, T., Tsunoda, Y., and Hashizume, K. (2005). Gene-expression profiles of bovine trophoblastic cell line (BT-1) analysed by a custom cDNA microarray. J. Reprod. Dev. 51, 211–220.
Gene-expression profiles of bovine trophoblastic cell line (BT-1) analysed by a custom cDNA microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFKiur4%3D&md5=d075b67910f34e4d47f7b564d5d631abCAS | 15613779PubMed |

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=a749ad4b98ea050566d2edb6068eb5a3CAS | 10208969PubMed |

Van Stekelenburg-Hamers, A. E., Van Achterberg, T. A., Rebel, H. G., Flechon, J. E., Campbell, K. H., Weima, S. M., and Mummery, C. L. (1995). Isolation and characterisation of permanent cell lines from inner cell mass cells of bovine blastocysts. Mol. Reprod. Dev. 40, 444–454.
Isolation and characterisation of permanent cell lines from inner cell mass cells of bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvV2gsbo%3D&md5=71169fd014ddcaa6e0f8862fcccb9d5dCAS | 7598910PubMed |

Vejlsted, M., Avery, B., Schmidt, M., Greve, T., Alexopoulos, N., and Maddox-Hyttel, P. (2005). Ultrastructural and immunohistochemical characterisation of the bovine epiblast. Biol. Reprod. 72, 678–686.
Ultrastructural and immunohistochemical characterisation of the bovine epiblast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVeisLg%3D&md5=02c18c15f826d63e43fee66f44cc01dcCAS | 15537864PubMed |

Verma, V., Huang, B., Kallingappa, P. K., and Oback, B. (2013). Dual kinase inhibition promotes pluripotency in finite bovine embryonic cell lines. Stem Cells Dev. 22, 1728–1742.
Dual kinase inhibition promotes pluripotency in finite bovine embryonic cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvFyntb4%3D&md5=92125fa002f3c59a47e049c5c3924905CAS | 23282176PubMed |

Wakayama, T., Perry, A. C. F., Zuccotti, M., Johnson, K. R., and Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–374.
Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFKnsbs%3D&md5=8470f76c21c9e0d4e4c028b2ced43f20CAS | 9690471PubMed |

Wang, L., Duan, E. K., Sung, L. Y., Jeong, B. S., Yang, X. Z., and Tian, X. C. (2005). Generation and characterisation of pluripotent stem cells from cloned bovine embryos. Biol. Reprod. 73, 149–155.
Generation and characterisation of pluripotent stem cells from cloned bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1Srt7Y%3D&md5=1e0ff500d2117dcb6fe8575cc12c391cCAS | 15744021PubMed |

Watanabe, Y., Kameoka, S., Gopalakrishnan, V., Aldape, K. D., Pan, Z. Z., Lang, F. F., and Majumder, S. (2004). Conversion of myoblasts to physiologically active neuronal phenotype. Genes Dev. 18, 889–900.
Conversion of myoblasts to physiologically active neuronal phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKksL8%3D&md5=dbc97596c9a8c89b13c8939501383355CAS | 15078815PubMed |

Wilmut, I., Schnieke, A. E., McWhir, J., Kind, A. J., and Campbell, K. H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–813.
Viable offspring derived from fetal and adult mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFamsLs%3D&md5=b342bc4ed2627defdfde20d0e99d7404CAS | 9039911PubMed |

Yadav, P. S., Kues, W. A., Herrmann, D., Carnwath, J. W., and Niemann, H. (2005). Bovine ICM-derived cells express the Oct4 orthologue. Mol. Reprod. Dev. 72, 182–190.
Bovine ICM-derived cells express the Oct4 orthologue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1ygu7k%3D&md5=62ab812f2b9668ca35f9956b20eb5ccbCAS | 15973686PubMed |

Yagi, R., Kohn, M. J., Karavanova, I., Kaneko, K. J., Vullhorst, D., DePamphilis, M. L., and Buonanno, A. (2007). Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827–3836.
Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVeku7rL&md5=ceda079bf81f4b9c80fc79f2a09caef1CAS | 17913785PubMed |

Ying, Q. L., Nichols, J., Chambers, I., and Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem-cell self-renewal in collaboration with STAT3. Cell 115, 281–292.
BMP induction of Id proteins suppresses differentiation and sustains embryonic stem-cell self-renewal in collaboration with STAT3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFClu7c%3D&md5=b8f6f3d318bab733aa0f72751c73eb72CAS | 14636556PubMed |

Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., and Smith, A. (2008). The ground state of embryonic stem-cell self-renewal. Nature 453, 519–523.
The ground state of embryonic stem-cell self-renewal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Ortbg%3D&md5=233e7dbb216884ab8d02cf6f5a98beb6CAS | 18497825PubMed |

Young, L. E., Sinclair, K. D., and Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. Reprod. 3, 155–163.
Large offspring syndrome in cattle and sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlaltL8%3D&md5=f8b310dcfcc67e4119d2de803ac03ef6CAS | 9829550PubMed |

Zuccotti, M., Merico, V., Sacchi, L., Bellone, M., Brink, T. C., Stefanelli, M., Redi, C. A., Bellazzi, R., Adjaye, J., and Garagna, S. (2009). Oct-4 regulates the expression of Stella and Foxj2 at the Nanog locus: implications for the developmental competence of mouse oocytes. Hum. Reprod. 24, 2225–2237.
Oct-4 regulates the expression of Stella and Foxj2 at the Nanog locus: implications for the developmental competence of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtValsbjJ&md5=4915a69ad4f72454dac96a37227af193CAS | 19477878PubMed |