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

Expression and function of transcription factor AP-2γ in early embryonic development of porcine parthenotes

Sung-Hyun Lee A , Jung-Woo Kwon A , Inchul Choi B C and Nam-Hyung Kim A C
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, Chungbuk National University, Gaesin-dong, Cheongju, Chungbuk 361-763, Republic of Korea.

B Department of Animal Biosystem Sciences, College of Agriculture and Life Sciences, Chungnam National University, Daejeon 305-764, Republic of Korea.

C Corresponding authors. Email: nhkim@chungbuk.ac.kr; icchoi@cnu.ac.kr

Reproduction, Fertility and Development 28(8) 1197-1205 https://doi.org/10.1071/RD14198
Submitted: 9 June 2014  Accepted: 3 December 2014   Published: 7 January 2015

Abstract

Transcription factor AP-2γ (TFAP2C) is a member of the transcription factor activating enhancer binding protein (AP) family. In the present study we determined the temporal and spatial expression patterns of TFAP2C in porcine parthenotes during preimplantation development. Porcine TFAP2C transcripts were expressed at all stages of preimplantation development, with highest expression at the 8-cell stage. In contrast with the mouse, TFAP2C protein was not restricted to the trophectoderm and was also detected in the ICM in blastocyst stage porcine parthenotes. In knockdown (KD) experiments, most TFAP2C-depleted embryos were arrested before the compacted 8-cell stage. This developmental failure is attributed to abnormal expression of genes involved in cell adhesion, tight junction biogenesis and cell proliferation. Interestingly, although the conserved region 4 (CR4) of the porcine OCT4 5′ upstream regionlacked the AP2C-binding motif, OCT4 transcript levels were elevated in porcine TFAP2C-KD 8-cell embryos, suggesting TFAP2C may be involved in the regulation of OCT4 in porcine embryos through other mechanisms. In summary, the results suggest that TFAP2C is necessary for the transition from de novo transcript synthesis by activation to compaction and further development, and the different expression patterns of TFAP2C in porcine embryos may reflect species-specific functions during preimplantation embryo development.

Additional keywords: cell adhesion, cell polarity, compaction, pig embryos.


References

Alarcon, V. B. (2010). Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo. Biol. Reprod. 83, 347–358.
Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrsrrJ&md5=3ff77d3745ee28b2b4ad39c9c6cb6ee3CAS | 20505164PubMed |

Aston, K. I., Li, G. P., Hicks, B. A., Winger, Q. A., and White, K. L. (2009). Genetic reprogramming of transcription factor ap-2gamma in bovine somatic cell nuclear transfer preimplantation embryos and placentomes. Cloning Stem Cells 11, 177–186.
Genetic reprogramming of transcription factor ap-2gamma in bovine somatic cell nuclear transfer preimplantation embryos and placentomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1CmtL4%3D&md5=db9a379aafc7b4a657bdbfb4f2b5edfaCAS | 19226219PubMed |

Auman, H. J., Nottoli, T., Lakiza, O., Winger, Q., Donaldson, S., and Williams, T. (2002). Transcription factor AP-2gamma is essential in the extra-embryonic lineages for early postimplantation development. Development 129, 2733–2747.
| 1:CAS:528:DC%2BD38XltVyhtr8%3D&md5=f3a8e16507fd6b35c37967ae2de9e712CAS | 12015300PubMed |

Berg, D. K., Smith, C. S., Pearton, D. J., Wells, D. N., Broadhurst, R., Donnison, M., and Pfeffer, P. L. (2011). Trophectoderm lineage determination in cattle. Dev. Cell 20, 244–255.
Trophectoderm lineage determination in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFeit7Y%3D&md5=00d6ecfe9d0c886e8153cc10498f409bCAS | 21316591PubMed |

Choi, I., Carey, T. S., Wilson, C. A., and Knott, J. G. (2012). Transcription factor AP-2γ is a core regulator of tight junction biogenesis and cavity formation during mouse early embryogenesis. Development 139, 4623–4632.
Transcription factor AP-2γ is a core regulator of tight junction biogenesis and cavity formation during mouse early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Oht7k%3D&md5=936a14b2f7112afda8b143653caf6188CAS |

Choi, I., Carey, T. S., Wilson, C. A., and Knott, J. G. (2013). Evidence that transcription factor AP-2gamma is not required for Oct4 repression in mouse blastocysts. PLoS ONE 8, e65771.
Evidence that transcription factor AP-2gamma is not required for Oct4 repression in mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslOmsbg%3D&md5=90578134acb09e1daf2a3f83056c5b0fCAS | 23741512PubMed |

de Vries, W. N., Evsikov, A. V., Haac, B. E., Fancher, K. S., Holbrook, A. E., Kemler, R., Solter, D., and Knowles, B. B. (2004). Maternal beta-catenin and E-cadherin in mouse development. Development 131, 4435–4445.
Maternal beta-catenin and E-cadherin in mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVehtL8%3D&md5=4e95e954b6c876115fcb65dabce74f81CAS | 15306566PubMed |

Dietrich, J. E., and Hiiragi, T. (2007). Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219–4231.
Stochastic patterning in the mouse pre-implantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtFegtw%3D%3D&md5=37140a9917f6554b1b2f7f630384a7ccCAS | 17978007PubMed |

Ducibella, T., Ukena, T., Karnovsky, M., and Anderson, E. (1977). Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo. J. Cell Biol. 74, 153–167.
Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3gslaqsg%3D%3D&md5=16cb20d3af42cb42617ccc07e412a293CAS | 873999PubMed |

Eckert, J. J., and Fleming, T. P. (2008). Tight junction biogenesis during early development. Biochim. Biophys. Acta 1778, 717–728.
Tight junction biogenesis during early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVSqt7c%3D&md5=74e35db34ff59fe17a4eb7bcdd66f3c9CAS | 18339299PubMed |

Eckert, D., Buhl, S., Weber, S., Jager, R., and Schorle, H. (2005). The AP-2 family of transcription factors. Genome Biol. 6, 246.
The AP-2 family of transcription factors.Crossref | GoogleScholarGoogle Scholar | 16420676PubMed |

Ezashi, T., Matsuyama, H., Telugu, B. P., and Roberts, R. M. (2011). Generation of colonies of induced trophoblast cells during standard reprogramming of porcine fibroblasts to induced pluripotent stem cells. Biol. Reprod. 85, 779–787.
Generation of colonies of induced trophoblast cells during standard reprogramming of porcine fibroblasts to induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12ht73F&md5=b49d5d610d2a799149843e6c112cd806CAS | 21734265PubMed |

Kim, J., Gye, M. C., and Kim, M. K. (2004). Role of occludin, a tight junction protein, in blastocoel formation, and in the paracellular permeability and differentiation of trophectoderm in preimplantation mouse embryos. Mol. Cells 17, 248–254.
| 1:CAS:528:DC%2BD2cXks1Cmsbc%3D&md5=2d41c461f7a01e6d469d69d2882e49a9CAS | 15179038PubMed |

Kirchhof, K., and Groth, T. (2008). Surface modification of biomaterials to control adhesion of cells. Clin. Hemorheol. Microcirc. 39, 247–251.
| 1:CAS:528:DC%2BD1cXlvFSjt7k%3D&md5=1bc3073a6971aa9ca5f7f2575e83fa81CAS | 18503133PubMed |

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., Buhl, S., Woynecki, T., van Furden, B., Tolkunova, E., Seiffe, F., Moser, M., Tomilin, A., Winterhager, E., and Schorle, H. (2010). The transcription factor TCFAP2C/AP-2gamma cooperates with CDX2 to maintain trophectoderm formation. Mol. Cell. Biol. 30, 3310–3320.
The transcription factor TCFAP2C/AP-2gamma cooperates with CDX2 to maintain trophectoderm formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVensr4%3D&md5=df525bd42debe289ca8ebe6b96d12486CAS | 20404091PubMed |

Larue, L., Ohsugi, M., Hirchenhain, J., and Kemler, R. (1994). E-Cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl Acad. Sci. USA 91, 8263–8267.
E-Cadherin null mutant embryos fail to form a trophectoderm epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFCjur8%3D&md5=bc615dc846c4ead576f74f0add802037CAS | 8058792PubMed |

Lelièvre, S. A. (2010). Tissue polarity-dependent control of mammary epithelial homeostasis and cancer development: an epigenetic perspective. J. Mammary Gland Biol. Neoplasia 15, 49–63.
Tissue polarity-dependent control of mammary epithelial homeostasis and cancer development: an epigenetic perspective.Crossref | GoogleScholarGoogle Scholar | 20101444PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=6db539426b70529f14f65734e4c1d0f6CAS | 11846609PubMed |

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=69be01962ccbaed83f949ec7e47dee5aCAS | 18425776PubMed |

Magnani, L., Johnson, C. M., and Cabot, R. A. (2008). Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential. Reprod. Fertil. Dev. 20, 818–825.
Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWmsb7N&md5=2c724faa7e064af474a4894e4e26f73dCAS | 18842184PubMed |

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=a25a109be135ac7d54897e4fae8b8c06CAS | 12787504PubMed |

Moriwaki, K., Tsukita, S., and Furuse, M. (2007). Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos. Dev. Biol. 312, 509–522.
Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSktrvI&md5=28ce4c5ab83550456523324d5d54b0d7CAS | 17980358PubMed |

Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, 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=9a478dd2bd2facd0ee174019c3f4a0a5CAS | 9814708PubMed |

Parfitt, D. E., and Zernicka-Goetz, M. (2010). Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol. Biol. Cell 21, 2649–2660.
Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGlt7bE&md5=1866b48d9c5cb1ecfb90261ab0311c15CAS | 20554762PubMed |

Pratt, H. P., Ziomek, C. A., Reeve, W. J., and Johnson, M. H. (1982). Compaction of the mouse embryo: an analysis of its components. J. Embryol. Exp. Morphol. 70, 113–132.
| 1:STN:280:DyaL3s%2FlvVGjug%3D%3D&md5=a4de46574d3f88a313de5bf10d72bd36CAS | 7142893PubMed |

Riethmacher, D., Brinkmann, V., and Birchmeier, C. (1995). A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl Acad. Sci. USA 92, 855–859.
A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsVKiu70%3D&md5=b9380bc3d34553b769ef1edcd53c7510CAS | 7846066PubMed |

Sherr, C. J., and Roberts, J. M. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501–1512.
CDK inhibitors: positive and negative regulators of G1-phase progression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlOhsLs%3D&md5=0e25f1b69b24a969e77d60f8110bb3f8CAS | 10385618PubMed |

Sheth, B., Moran, B., Anderson, J. M., and Fleming, T. P. (2000). Post-translational control of occludin membrane assembly in mouse trophectoderm: a mechanism to regulate timing of tight junction biogenesis and blastocyst formation. Development 127, 831–840.
| 1:CAS:528:DC%2BD3cXkt1aku7k%3D&md5=cf01c82130c93e5d6a62192a45cdfa40CAS | 10648241PubMed |

Sheth, B., Nowak, R. L., Anderson, R., Kwong, W. Y., Papenbrock, T., and Fleming, T. P. (2008). Tight junction protein ZO-2 expression and relative function of ZO-1 and ZO-2 during mouse blastocyst formation. Exp. Cell Res. 314, 3356–3368.
Tight junction protein ZO-2 expression and relative function of ZO-1 and ZO-2 during mouse blastocyst formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12kurbI&md5=245fe6bcc6c7f0f3c7d43d7ea3268cddCAS | 18817772PubMed |

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 |

Vinot, S., Le, T., Ohno, S., Pawson, T., Maro, B., and Louvet-Vallee, S. (2005). Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev. Biol. 282, 307–319.
Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFSqsr8%3D&md5=ccff2032e68657ffab4e9cdb578cc425CAS | 15950600PubMed |

Winger, Q., Huang, J., Auman, H. J., Lewandoski, M., and Williams, T. (2006). Analysis of transcription factor AP-2 expression and function during mouse preimplantation development. Biol. Reprod. 75, 324–333.
Analysis of transcription factor AP-2 expression and function during mouse preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWmtb8%3D&md5=3356ea691c1ad888c4126a08322972c6CAS | 16672719PubMed |

Zheng, Z., Zhao, M. H., Jia, J. L., Heo, Y. T., Cui, X. S., Oh, J. S., and Kim, N. H. (2013). Knockdown of maternal homeobox transcription factor SEBOX gene impaired early embryonic development in porcine parthenotes. J. Reprod. Dev. 59, 557–562.
Knockdown of maternal homeobox transcription factor SEBOX gene impaired early embryonic development in porcine parthenotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFWjsrg%3D&md5=8386c782b693aae001432c04cb9a269bCAS | 24018616PubMed |