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Effect of NANOG overexpression on porcine embryonic development and pluripotent embryonic stem cell formation in vitro

Published online by Cambridge University Press:  09 December 2021

Gerelchimeg Bou Open the ORCID record for Gerelchimeg Bou [Opens in a new window] ,
Shimeng Guo ,
Jia Guo ,
Zhuang Chai ,
Jianchao Zhao ,
Yan Li  and
Zhonghua Liu
Gerelchimeg Bou*
Affiliation:
College of Animal Science, Inner Mongolia Agricultural University, Hohhot010018, China
Shimeng Guo
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
Jia Guo
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
Zhuang Chai
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
Jianchao Zhao
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
Yan Li
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
Zhonghua Liu
Affiliation:
College of Life Science, Northeast Agricultural University, Harbin150030, China
*
Author for correspondence: Gerelchimeg Bou. College of Animal Science, Inner Mongolia Agricultural University, Hohhot010018, China. E-mail: gerelchimeg@imau.edu.cn
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Summary

The efficiency of establishing pig pluripotent embryonic stem cell clones from blastocysts is still low. The transcription factor Nanog plays an important role in maintaining the pluripotency of mouse and human embryonic stem cells. Adequate activation of Nanog has been reported to increase the efficiency of establishing mouse embryonic stem cells from 3.5 day embryos. In mouse, Nanog starts to be strongly expressed as early as the morula stage, whereas in porcine NANOG starts to be strongly expressed by the late blastocyst stage. Therefore, here we investigated both the effect of expressing NANOG on porcine embryos early from the morula stage and the efficiency of porcine pluripotent embryonic stem cell clone formation. Compared with intact porcine embryos, NANOG overexpression induced a lower blastocyst rate, and did not show any advantages for embryo development and pluripotent embryonic stem cell line formation. These results indicated that, although NANOG is important pluripotent factor, NANOG overexpression is unnecessary for the initial formation of porcine pluripotent embryonic stem cell clones in vitro.

Keywords

NanogOverexpressionPluripotent cellPorcine early development
Type
Research Article
Information
Zygote , Volume 30 , Issue 3 , June 2022 , pp. 324 - 329
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Beckmann, LS and Day, BN (1993). Effects of media NaCl concentration and osmolarity on the culture of early-stage porcine embryos and the viability of embryos cultured in a selected superior medium. Theriogenology 39, 611–22.CrossRefGoogle Scholar
Bou, G, Liu, S, Sun, M, Zhu, J, Xue, B, Guo, J, Zhao, Y, Qu, B, Weng, X, Wei, Y, Lei, L and Liu, Z (2017). CDX2 is essential for cell proliferation and polarity in porcine blastocysts. Development 144, 1296–306.Google ScholarPubMed
Boyer, LA, Lee, TI, Cole, MF, Johnstone, SE, Levine, SS, Zucker, JP, Guenther, MG, Kumar, RM, Murray, HL, Jenner, RG, Gifford, DK, Melton, DA, Jaenisch, R and Young, RA (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947–56.CrossRefGoogle ScholarPubMed
Brevini, T, Pennarossa, G, Maffei, S and Gandolfi, F (2012). Pluripotency network in porcine embryos and derived cell lines. [Reprod Domest Anim] Zuchthygiene, 47(Suppl. 4), 86–91.CrossRefGoogle ScholarPubMed
Carey, TS, Cao, Z, Choi, I, Ganguly, A, Wilson, CA, Paul, S and Knott, JG (2015). BRG1 governs Nanog transcription in early mouse embryos and embryonic stem cells via antagonism of histone H3 lysine 9/14 acetylation. Mol Cell Biol 35, 4158–69.CrossRefGoogle ScholarPubMed
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, 643–55.CrossRefGoogle ScholarPubMed
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, 615–24.CrossRefGoogle ScholarPubMed
Chen, Q, Zhang, H, Jiang, H, Zhang, M, Wang, J, Zhao, L, Wang, C, Liu, M and Li, R (2020). Conversion between porcine naive-like and primed ESCs and specific pluripotency marker identification. In Vitro Cell Dev Biol Anim 56, 412–23.CrossRefGoogle ScholarPubMed
Cole, MF, Johnstone, SE, Newman, JJ, Kagey, MH and Young, RA (2008). Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 22, 746–55.CrossRefGoogle ScholarPubMed
du Puy, L, Lopes, SM, Haagsman, HP and Roelen, BA (2011). Analysis of co-expression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro . Theriogenology 75, 513–26.CrossRefGoogle ScholarPubMed
Evans, MJ and Kaufman, MH (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819), 154–6.CrossRefGoogle ScholarPubMed
Frankenberg, S, Gerbe, F, Bessonnard, S, Belville, C, Pouchin, P, Bardot, O and Chazaud, C (2011). Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev Cell 21, 1005–13.CrossRefGoogle Scholar
Habibi, R, Hosseini, SM, Zadegan, FG, Hajian, M, Ostadhosseini, S, Vash, NT, Naddafpour, A and Nasr Esfahani, MH (2018). Functional characterization of NANOG in goat pre-implantation embryonic development. Theriogenology 120, 33–9.CrossRefGoogle ScholarPubMed
Hall, VJ, Christensen, J, Gao, Y, Schmidt, MH and Hyttel, P (2009). Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev Dynam 238, 2014–24.CrossRefGoogle Scholar
Kues, WA, Nowak-Imialek, M, Haridoss, S and Niemann, H (2010). Strategies for the derivation of pluripotent cells from farm animals. [Reprod Domest Anim] Zuchthygiene 45, Suppl. 3, 25–31.CrossRefGoogle ScholarPubMed
Lee, K, Hamm, J, Whitworth, K, Spate, L, Park, KW, Murphy, CN and Prather, RS (2014). Dynamics of TET family expression in porcine preimplantation embryos is related to zygotic genome activation and required for the maintenance of NANOG. Dev Biol 386, 86–95.CrossRefGoogle ScholarPubMed
Liu, J, An, L, Wang, J, Liu, Z, Dai, Y, Liu, Y, Yang, L and Du, F (2019). Dynamic patterns of H3K4me3, H3K27me3, and Nanog during rabbit embryo development. American J Trans Res 11, 430–41Google ScholarPubMed
Loh, YH, Wu, Q, Chew, JL, Vega, VB, Zhang, W, Chen, X, Bourque, G, George, J, Leong, B, Liu, J, Wong, KY, Sung, KW, Lee, CW, Zhao, XD, Chiu, KP, Lipovich, L, Kuznetsov, VA, Robson, P et al. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38, 431–40.CrossRefGoogle ScholarPubMed
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, 631–42.CrossRefGoogle ScholarPubMed
Nowak-Imialek, M and Niemann, H (2012). Pluripotent cells in farm animals: State of the art and future perspectives. Reprod Fertil Dev 25, 103–28.CrossRefGoogle ScholarPubMed
Ortega, MS, Kelleher, AM, O’Neil, E, Benne, J, Cecil, R and Spencer, TE (2020). NANOG is required to form the epiblast and maintain pluripotency in the bovine embryo. Mol Reprod Dev 87, 152–160.CrossRefGoogle ScholarPubMed
Pálfy, M, Schulze, G, Valen, E and Vastenhouw, NL (2020). Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation. PLOS Genetics, 16, e1008546.CrossRefGoogle ScholarPubMed
Selokar, NL and Kues, WA (2018). How farm animals are improving human health and welfare. Rev Sci Tech 37, 83–96.CrossRefGoogle ScholarPubMed
Simmet, K, Zakhartchenko, V, Philippou-Massier, J, Blum, H, Klymiuk, N and Wolf, E (2018). OCT4/POU5F1 is required for NANOG expression in bovine blastocysts. Proc Natl Acad Sci USA 115, 2770–5.CrossRefGoogle ScholarPubMed
Su, Y, Zhu, J, Salman, S and Tang, Y (2020). Induced pluripotent stem cells from farm animals. J Anim Sci 98, skaa343.CrossRefGoogle ScholarPubMed
Takahashi, K and Yamanaka, S (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–76.CrossRefGoogle ScholarPubMed
Uh, K, Ryu, J, Farrell, K, Wax, N and Lee, K (2020). TET family regulates the embryonic pluripotency of porcine preimplantation embryos by maintaining the DNA methylation level of NANOG. Epigenetics 15, 1228–42.CrossRefGoogle ScholarPubMed
Veil, M, Yampolsky, LY, Grüning, B and Onichtchouk, D (2019). Pou5f3, SoxB1, and Nanog remodel chromatin on high nucleosome affinity regions at zygotic genome activation. Genome Res 29, 383–95.CrossRefGoogle ScholarPubMed
Wang, J, Rao, S, Chu, J, Shen, X, Levasseur, DN, Theunissen, TW and Orkin, SH (2006). A protein interaction network for pluripotency of embryonic stem cells. Nature 444(7117), 364–8.CrossRefGoogle ScholarPubMed
Wolf, XA, Serup, P and Hyttel, P (2011). Three-dimensional localisation of NANOG, OCT4, and E-cadherin in porcine pre- and peri-implantation embryos. Dev Dynam 240, 204–10.CrossRefGoogle ScholarPubMed
Xue, B, Li, Y, He, Y, Wei, R, Sun, R, Yin, Z, Bou, G and Liu, Z (2016). Porcine pluripotent stem cells derived from IVF embryos contribute to chimeric development in vivo . PLoS One 11, e0151737.CrossRefGoogle ScholarPubMed