5.9
CiteScore
5.9
Impact Factor
Volume 47 Issue 3
Mar.  2020
Turn off MathJax
Article Contents

Lessons from expanded potential of embryonic stem cells: Moving toward totipotency

doi: 10.1016/j.jgg.2020.02.003
More Information
  • Embryonic stem cells possess fascinating capacity of self-renewal and developmental potential, leading to significant progress in understanding the molecular basis of pluripotency, disease modeling, and reprogramming technology. Recently, 2-cell–like embryonic stem cells (ESCs) and expanded potential stem cells or extended pluripotent stem cells (EPSCs) generated from early-cleavage embryos display some features of totipotent embryos. These cell lines provide valuable in vitro models to study underlying principles of totipotency, cell plasticity, and lineage segregation. In this review, we summarize the current progress in this filed and highlight the application potentials of these cells in the future.
  • loading
  • [1]
    Akiyama, T., Xin, L., Oda, M., Sharov, A.A., Amano, M., Piao, Y., Cadet, J.S., Dudekula, D.B., Qian, Y., Wang, W., Ko, S.B., Ko, M.S., 2015. Transient bursts of Zscan4 expression are accompanied by the rapid derepression of heterochromatin in mouse embryonic stem cells. DNA Res. 22, 307-318.
    [2]
    Alano, C.C., Kauppinen, T.M., Valls, A.V., Swanson, R.A., 2006. Minocycline inhibits poly(adp-ribose) polymerase-1 at nanomolar concentrations. Proc. Nat.l Acad. Sci. U. S. A. 103, 9685-9690.
    [3]
    Azzolin, L., Panciera, T., Soligo, S., Enzo, E., Bicciato, S., Dupont, S., Bresolin, S., Frasson, C., Basso, G., Guzzardo, V., Fassina, A., Cordenonsi, M., Piccolo, S., 2014. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the Wnt response. Cell 158, 157-170.
    [4]
    Bai, L.G., Yang, L., Zhao, C.Q., Song, L.S., Liu, X.F., Bai, C.L., Su, G.H., Wei, Z.Y., Li, G.P., 2019. Histone demethylase UTX is an essential factor for zygotic genome activation and regulates Zscan4 expression in mouse embryos. Int. J. Biol. Sci. 15, 2363-2372.
    [5]
    Boskovic, A., Eid, A., Pontabry, J., Ishiuchi, T., Spiegelhalter, C., Raghu Ram, E.V., Meshorer, E., Torres-Padilla, M.E., 2014. Higher chromatin mobility supports totipotency and precedes pluripotency in vivo. Genes Dev. 28, 1042-1047.
    [6]
    Burton, A., Muller, J., Tu, S.J., Padilla-Longoria, P., Guccione, E., Torres-Padilla, M.E., 2013. Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Rep. 5, 687-701.
    [7]
    Canham, M.A., Sharov, A.A., Ko, M.S.H., Brickman, J.M., 2010. Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379.
    [8]
    Chen, Z., Zhang, Y., 2019. Loss of Dux causes minor defects in zygotic genome activation and is compatible with mouse development. Nat. Genet. 51, 947-951.
    [9]
    Choi, Y.J., Lin, C.P., Ho, J.J., He, X., Okada, N., Bu, P., Zhong, Y., Kim, S.Y., Bennett, M.J., Chen, C., Ozturk, A., Hicks, G.G., Hannon, G.J., He, L., 2011. miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat. Cell Biol. 13, 1353-1360.
    [10]
    Choi, Y.J., Lin, C.P., Risso, D., Chen, S., Kim, T.A., Tan, M.H., Li, J.B., Wu, Y., Chen, C., Xuan, Z., Macfarlan, T., Peng, W., Lloyd, K.C., Kim, S.Y., Speed, T.P., He, L., 2017. Deficiency of microrna miR-34a expands cell fate potential in pluripotent stem cells. Science 355, eaag1927.
    [11]
    Dan, J., Li, M., Yang, J., Li, J., Okuka, M., Ye, X., Liu, L., 2013. Roles for Tbx3 in regulation of two-cell state and telomere elongation in mouse ES cells. Sci. Rep. 3, 3492.
    [12]
    Dan, J., Rousseau, P., Hardikar, S., Veland, N., Wong, J., Autexier, C., Chen, T., 2017. Zscan4 inhibits maintenance DNA methylation to facilitate telomere elongation in mouse embryonic stem cells. Cell Rep. 20, 1936-1949.
    [13]
    Dan, J.M., Liu, Y.F., Liu, N., Chiourea, M., Okuka, M., Wu, T., Ye, X.Y., Mou, C.L., Wang, L., Wang, L.L., Yin, Y., Yuan, J.H., Zuo, B.F., Wang, F., Li, Z.G., Pan, X.H., Yin, Z.N., Chen, L.Y., Keefe, D.L., Gagos, S., Xiao, A., Liu, L., 2014. Rif1 maintains telomere length homeostasis of ESCs by mediating heterochromatin silencing. Dev. Cell 29, 7-19.
    [14]
    De Iaco, A., Coudray, A., Duc, J., Trono, D., 2019. Dppa2 and Dppa4 are necessary to establish a 2C-like state in mouse embryonic stem cells. EMBO Rep. 20, e47382.
    [15]
    De Iaco, A., Planet, E., Coluccio, A., Verp, S., Duc, J., Trono, D., 2017. Dux-family transcription factors regulate zygotic genome activation in placental mammals. Nat. Genet. 49, 941-945.
    [16]
    Deng, Q., Ramskold, D., Reinius, B., Sandberg, R., 2014. Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 343, 193-196.
    [17]
    Eckersley-Maslin, M., Alda-Catalinas, C., Blotenburg, M., Kreibich, E., Krueger, C., Reik, W., 2019. Dppa2 and Dppa4 directly regulate the Dux-driven zygotic transcriptional program. Genes Dev. 33, 194-208.
    [18]
    Eckersley-Maslin, M.A., Svensson, V., Krueger, C., Stubbs, T.M., Giehr, P., Krueger, F., Miragaia, R.J., Kyriakopoulos, C., Berrens, R.V., Milagre, I., Walter, J., Teichmann, S.A., Reik, W., 2016. MERVL/Zscan4 network activation results in transient genome-wide DNA demethylation of mESCs. Cell Rep. 17, 179-192.
    [19]
    Falco, G., Lee, S.L., Stanghellini, I., Bassey, U.C., Hamatani, T., Ko, M.S., 2007. Zscan4: A novel gene expressed exclusively in late 2-cell embryos and embryonic stem cells. Dev. Biol. 307, 539-550.
    [20]
    Fu, X., Wu, X., Djekidel, M.N., Zhang, Y., 2019. Myc and Dnmt1 impede the pluripotent to totipotent state transition in embryonic stem cells. Nat. Cell Biol. 21, 835-844.
    [21]
    Gabriels, J., Beckers, M.C., Ding, H., De Vriese, A., Plaisance, S., van der Maarel, S.M., Padberg, G.W., Frants, R.R., Hewitt, J.E., Collen, D., Belayew, A., 1999. Nucleotide sequence of the partially deleted D4Z4 locus in a patient with FSHD identifies a putative gene within each 3.3 kb element. Gene 236, 25-32.
    [22]
    Gao, X., Nowak-Imialek, M., Chen, X., Chen, D., Herrmann, D., Ruan, D., Chen, A.C.H., Eckersley-Maslin, M.A., Ahmad, S., Lee, Y.L., Kobayashi, T., Ryan, D., Zhong, J., Zhu, J., Wu, J., Lan, G., Petkov, S., Yang, J., Antunes, L., Campos, L.S., Fu, B., Wang, S., Yong, Y., Wang, X., Xue, S.G., Ge, L., Liu, Z., Huang, Y., Nie, T., Li, P., Wu, D., Pei, D., Zhang, Y., Lu, L., Yang, F., Kimber, S.J., Reik, W., Zou, X., Shang, Z., Lai, L., Surani, A., Tam, P.P.L., Ahmed, A., Yeung, W.S.B., Teichmann, S.A., Niemann, H., Liu, P., 2019. Establishment of porcine and human expanded potential stem cells. Nat. Cell Biol. 21, 687-699.
    [23]
    Geng, L.N., Yao, Z., Snider, L., Fong, A.P., Cech, J.N., Young, J.M., van der Maarel, S.M., Ruzzo, W.L., Gentleman, R.C., Tawil, R., Tapscott, S.J., 2012. Dux4 activates germline genes, retroelements, and immune mediators: Implications for facioscapulohumeral dystrophy. Dev. Cell 22, 38-51.
    [24]
    Goolam, M., Scialdone, A., Graham, S.J.L., Macaulay, I.C., Jedrusik, A., Hupalowska, A., Voet, T., Marioni, J.C., Zernicka-Goetz, M., 2016. Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. Cell 165, 61-74.
    [25]
    Guo, M., Zhang, Y., Zhou, J., Bi, Y., Xu, J., Xu, C., Kou, X., Zhao, Y., Li, Y., Tu, Z., Liu, K., Lin, J., Yang, P., Gao, S., Wang, Y., 2019. Precise temporal regulation of Dux is important for embryo development. Cell Res. 29, 956-959.
    [26]
    Hamatani, T., Carter, M.G., Sharov, A.A., Ko, M.S., 2004. Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117-131.
    [27]
    Hayashi, M., Maehara, K., Harada, A., Semba, Y., Kudo, K., Takahashi, H., Oki, S., Meno, C., Ichiyanagi, K., Akashi, K., Ohkawa, Y., 2016. Chd5 regulates MuERV-L/MERVL expression in mouse embryonic stem cells via H3k27me3 modification and histone H3.1/H3.2. J. Cell. Biochem. 117, 780-792.
    [28]
    Hendrickson, P.G., Dorais, J.A., Grow, E.J., Whiddon, J.L., Lim, J.W., Wike, C.L., Weaver, B.D., Pflueger, C., Emery, B.R., Wilcox, A.L., Nix, D.A., Peterson, C.M., Tapscott, S.J., Carrell, D.T., Cairns, B.R., 2017. Conserved roles of mouse Dux and human Dux4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons. Nat. Genet. 49, 925-934.
    [29]
    Herceg, Z., Wang, Z.Q., 2001. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res.-Fundam. Mol. Mech. Mutag. 477, 97-110.
    [30]
    Hu, W.W., Feng, Z.H., Teresky, A.K., Levine, A.J., 2007. P53 regulates maternal reproduction through lif. Nature 450, 721-U728.
    [31]
    Huang, S.M., Mishina, Y.M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G.A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S., Hild, M., Shi, X., Wilson, C.J., Mickanin, C., Myer, V., Fazal, A., Tomlinson, R., Serluca, F., Shao, W., Cheng, H., Shultz, M., Rau, C., Schirle, M., Schlegl, J., Ghidelli, S., Fawell, S., Lu, C., Curtis, D., Kirschner, M.W., Lengauer, C., Finan, P.M., Tallarico, J.A., Bouwmeester, T., Porter, J.A., Bauer, A., Cong, F., 2009. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461, 614-620.
    [32]
    Huang, Y., Kim, J.K., Do, D.V., Lee, C., Penfold, C.A., Zylicz, J.J., Marioni, J.C., Hackett, J.A., Surani, M.A., 2017. Stella modulates transcriptional and endogenous retrovirus programs during maternal-to-zygotic transition. eLife 6, e22345.
    [33]
    Ishiuchi, T., Enriquez-Gasca, R., Mizutani, E., Boskovic, A., Ziegler-Birling, C., Rodriguez-Terrones, D., Wakayama, T., Vaquerizas, J.M., Torres-Padilla, M.E., 2015. Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat. Struct. Mol. Biol. 22, 662-671.
    [34]
    Johnson, W.H., Loskutoff, N.M., Plante, Y., Betteridge, K.J., 1995. Production of four identical calves by the separation of blastomeres from an in vitro derived four-cell embryo. Vet. Rec. 137, 15-16.
    [35]
    Kapoor, A., Yao, W., Ying, H., Hua, S., Liewen, A., Wang, Q., Zhong, Y., Wu, C.J., Sadanandam, A., Hu, B., Chang, Q., Chu, G.C., Al-Khalil, R., Jiang, S., Xia, H., Fletcher-Sananikone, E., Lim, C., Horwitz, G.I., Viale, A., Pettazzoni, P., Sanchez, N., Wang, H., Protopopov, A., Zhang, J., Heffernan, T., Johnson, R.L., Chin, L., Wang, Y.A., Draetta, G., DePinho, R.A., 2014. Yap1 activation enables bypass of oncogenic kras addiction in pancreatic cancer. Cell 158, 185-197.
    [36]
    Karimi, M.M., Goyal, P., Maksakova, I.A., Bilenky, M., Leung, D., Tang, J.X., Shinkai, Y., Mager, D.L., Jones, S., Hirst, M., Lorincz, M.C., 2011. DNA methylation and SETDB1/H3k9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8, 676-687.
    [37]
    Ko, M.S., 2016. Zygotic genome activation revisited: Looking through the expression and function of Zscan4. Curr. top. Dev. Biol. 120, 103-124.
    [38]
    Leidenroth, A., Clapp, J., Mitchell, L.M., Coneyworth, D., Dearden, F.L., Iannuzzi, L., Hewitt, J.E., 2012. Evolution of Dux gene macrosatellites in placental mammals. Chromosoma 121, 489-497.
    [39]
    Li, R., Zhong, C., Yu, Y., Liu, H., Sakurai, M., Yu, L., Min, Z., Shi, L., Wei, Y., Takahashi, Y., Liao, H.K., Qiao, J., Deng, H., Nunez-Delicado, E., Rodriguez Esteban, C., Wu, J., Izpisua Belmonte, J.C., 2019. Generation of blastocyst-like structures from mouse embryonic and adult cell cultures. Cell 179, 687-702. e618.
    [40]
    Macfarlan, T.S., Gifford, W.D., Driscoll, S., Lettieri, K., Rowe, H.M., Bonanomi, D., Firth, A., Singer, O., Trono, D., Pfaff, S.L., 2012. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487, 57-63.
    [41]
    Maksakova, I.A., Thompson, P.J., Goyal, P., Jones, S.J., Singh, P.B., Karimi, M.M., Lorincz, M.C., 2013. Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenet. Chromatin 6, 15.
    [42]
    Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A.F., Smith, A., Stunnenberg, H.G., 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
    [43]
    Martello, G., Sugimoto, T., Diamanti, E., Joshi, A., Hannah, R., Ohtsuka, S., Gottgens, B., Niwa, H., Smith, A., 2012. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 11, 491-504.
    [44]
    Matsui, T., Leung, D., Miyashita, H., Maksakova, I.A., Miyachi, H., Kimura, H., Tachibana, M., Lorincz, M.C., Shinkai, Y., 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase eset. Nature 464, 927-931.
    [45]
    Mitalipov, S.M., Yeoman, R.R., Kuo, H.C., Wolf, D.P., 2002. Monozygotic twinning in rhesus monkeys by manipulation of in vitro-derived embryos. Biol. Reprod. 66, 1449-1455.
    [46]
    Moore, N.W., Adams, C.E., Rowson, L.E., 1968. Developmental potential of single blastomeres of the rabbit egg. J. Reprod. Fertil. 17, 527-531.
    [47]
    Morgani, S.M., Canham, M.A., Nichols, J., Sharov, A.A., Migueles, R.P., Ko, M.S., Brickman, J.M., 2013. Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep. 3, 1945-1957.
    [48]
    Nakai-Futatsugi, Y., Niwa, H., 2016. Zscan4 is activated after telomere shortening in mouse embryonic stem cells. Stem Cell Rep. 6, 483-495.
    [49]
    Pearson, G., Robinson, F., Beers Gibson, T., Xu, B.E., Karandikar, M., Berman, K., Cobb, M.H., 2001. Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr. Rev. 22, 153-183.
    [50]
    Pfaff, O., Hildebrandt, C., Waelbroeck, M., Hou, X., Moser, U., Mutschler, E., Lambrecht, G., 1995. The (s)-(+)-enantiomer of dimethindene: A novel M2-selective muscarinic receptor antagonist. Eur. J. Pharmacol. 286, 229-240.
    [51]
    Piotrowska-Nitsche, K., Perea-Gomez, A., Haraguchi, S., Zernicka-Goetz, M., 2005. Four-cell stage mouse blastomeres have different developmental properties. Development 132, 479-490.
    [52]
    Plachta, N., Bollenbach, T., Pease, S., Fraser, S.E., Pantazis, P., 2011. Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat. Cell Biol. 13, 117-123.
    [53]
    Rodriguez-Terrones, D., Gaume, X., Ishiuchi, T., Weiss, A., Kopp, A., Kruse, K., Penning, A., Vaquerizas, J.M., Brino, L., Torres-Padilla, M.E., 2018. A molecular roadmap for the emergence of early-embryonic-like cells in culture. Nat. Genet. 50, 106-119.
    [54]
    Rossant, J., 1976. Postimplantation development of blastomeres isolated from 4- and 8-cell mouse eggs. J. Embryol. Exp. Morphol. 36, 283-290.
    [55]
    Rossant, J., Tam, P.P., 2009. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
    [56]
    Shao, D.D., Xue, W., Krall, E.B., Bhutkar, A., Piccioni, F., Wang, X., Schinzel, A.C., Sood, S., Rosenbluh, J., Kim, J.W., Zwang, Y., Roberts, T.M., Root, D.E., Jacks, T., Hahn, W.C., 2014. KRAS and YAP1 converge to regulate EMT and tumor survival. Cell 158, 171-184.
    [57]
    Shi, J.C., Chen, Q., Li, X., Zheng, X.D., Zhang, Y., Qiao, J., Tang, F.C., Tao, Y., Zhou, Q., Duan, E.K., 2015. Dynamic transcriptional symmetry-breaking in pre-implantation mammalian embryo development revealed by single-cell RNA-seq. Development 142, 3468-3477.
    [58]
    Singh, A.M., Hamazaki, T., Hankowski, K.E., Terada, N., 2007. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25, 2534-2542.
    [59]
    Smith, A.G., 2001. Embryo-derived stem cells: Of mice and men. Annu. Rev. Cell. Dev. Biol. 17, 435-462.
    [60]
    Storm, M.P., Kumpfmueller, B., Bone, H.K., Buchholz, M., Ripoll, Y.S., Chaudhuri, J.B., Niwa, H., Tosh, D., Welham, M.J., 2014. Zscan4 is regulated by PI3-kinase and DNA-damaging agents and directly interacts with the transcriptional repressors LSD1 and CtBP2 in mouse embryonic stem cells. Plos One 9, e89821.
    [61]
    Tabansky, I., Lenarcic, A., Draft, R.W., Loulier, K., Keskin, D.B., Rosains, J., Rivera-Feliciano, J., Lichtman, J.W., Livet, J., Stern, J.N.H., Sanes, J.R., Eggan, K., 2013. Developmental bias in cleavage-stage mouse blastomeres. Curr. Biol. 23, 21-31.
    [62]
    Takahashi, K., Yamanaka, S., 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
    [63]
    Tarkowski, A.K., 1959. Experiments on the development of isolated blastomers of mouse eggs. Nature 184, 1286-1287.
    [64]
    Tian, Q., Wang, X.F., Xie, S.M., Yin, Y., Zhou, L.Q., 2020. H3.3 impedes zygotic transcriptional program activated by Dux. Biochem. Biophys. Res. Commun. 522, 422-427.
    [65]
    Torres-Padilla, M.E., Parfitt, D.E., Kouzarides, T., Zernicka-Goetz, M., 2007. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214-218.
    [66]
    Wang, W., Li, N., Li, X., Tran, M.K., Han, X., Chen, J., 2015. Tankyrase inhibitors target YAP by stabilizing angiomotin family proteins. Cell Rep. 13, 524-532.
    [67]
    Whiddon, J.L., Langford, A.T., Wong, C.J., Zhong, J.W., Tapscott, S.J., 2017. Conservation and innovation in the Dux4-family gene network. Nat. Genet. 49, 935-940.
    [68]
    White, M.D., Angiolini, J.F., Alvarez, Y.D., Kaur, G., Zhao, Z.P.W., Mocskos, E., Bruno, L., Bissiere, S., Levi, V., Plachta, N., 2016. Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165, 75-87.
    [69]
    Willadsen, S.M., 1981. The developmental capacity of blastomeres from 4-cell and 8-cell sheep embryos. J. Embryol. Exp. Morphol. 65, 165-172.
    [70]
    Wilson, M.B., Schreiner, S.J., Choi, H.J., Kamens, J., Smithgall, T.E., 2002. Selective pyrrolo-pyrimidine inhibitors reveal a necessary role for Src family kinases in Bcr-Abl signal transduction and oncogenesis. Oncogene 21, 8075-8088.
    [71]
    Xu, Q., Xie, W., 2018. Epigenome in early mammalian development: Inheritance, reprogramming and establishment. Trends Cell Biol. 28, 237-253
    [72]
    Yan, Y.L., Zhang, C., Hao, J., Wang, X.L., Ming, J., Mi, L., Na, J., Hu, X., Wang, Y., 2019. Dppa2/4 and SUMO E3 ligase PIAS4 opposingly regulate zygotic transcriptional program. PLoS Biol. 17, e3000324.
    [73]
    Yang, J., Guo, R.P., Wang, H., Ye, X.Y., Zhou, Z.C., Dan, J.M., Wang, H.Y., Gong, P., Deng, W., Yin, Y., Mao, S.Q., Wang, L.B., Ding, J.J., Li, J.S., Keefe, D.L., Dawlaty, M.M., Wang, J.L., Xu, G.L., Liu, L., 2016. Tet enzymes regulate telomere maintenance and chromosomal stability of mouse ESCs. Cell Rep. 15, 1809-1821.
    [74]
    Yang, J., Ryan, D.J., Lan, G., Zou, X., Liu, P., 2019. In vitro establishment of expanded-potential stem cells from mouse pre-implantation embryos or embryonic stem cells. Nat. Protoc. 14, 350-378.
    [75]
    Yang, J., Ryan, D.J., Wang, W., Tsang, J.C., Lan, G., Masaki, H., Gao, X., Antunes, L., Yu, Y., Zhu, Z., Wang, J., Kolodziejczyk, A.A., Campos, L.S., Wang, C., Yang, F., Zhong, Z., Fu, B., Eckersley-Maslin, M.A., Woods, M., Tanaka, Y., Chen, X., Wilkinson, A.C., Bussell, J., White, J., Ramirez-Solis, R., Reik, W., Gottgens, B., Teichmann, S.A., Tam, P.P.L., Nakauchi, H., Zou, X., Lu, L., Liu, P., 2017a. Establishment of mouse expanded potential stem cells. Nature 550, 393-397.
    [76]
    Yang, Y., Liu, B., Xu, J., Wang, J., Wu, J., Shi, C., Xu, Y., Dong, J., Wang, C., Lai, W., Zhu, J., Xiong, L., Zhu, D., Li, X., Yang, W., Yamauchi, T., Sugawara, A., Li, Z., Sun, F., Li, X., Li, C., He, A., Du, Y., Wang, T., Zhao, C., Li, H., Chi, X., Zhang, H., Liu, Y., Li, C., Duo, S., Yin, M., Shen, H., Belmonte, J.C.I., Deng, H., 2017b. Derivation of pluripotent stem cells with in vivo embryonic and extraembryonic potency. Cell 169, 243-257. e225.
    [77]
    Zalzman, M., Falco, G., Sharova, L.V., Nishiyama, A., Thomas, M., Lee, S.L., Stagg, C.A., Hoang, H.G., Yang, H.T., Indig, F.E., Wersto, R.P., Ko, M.S., 2010. Zscan4 regulates telomere elongation and genomic stability in ES cells. Nature 464, 858-863.
    [78]
    Zhang, Q., Dan, J.M., Wang, H., Guo, R.P., Mao, J., Fu, H.F., Wei, X.W., Liu, L., 2016. Tcstv1 and Tcstv3 elongate telomeres of mouse ES cells. Sci. Rep. 6, 19852
    [79]
    Zhang, W., Chen, F., Chen, R., Xie, D., Yang, J., Zhao, X., Guo, R., Zhang, Y., Shen, Y., Goke, J., Liu, L., Lu, X., 2019. Zscan4c activates endogenous retrovirus MERVL and cleavage embryo genes. Nucleic Acids Res. 47, 8485-8501.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures (1)  / Tables (2)

    Article Metrics

    Article views (105) PDF downloads (5) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return