Rapid conversion of human ESCs into mouse ESC-like pluripotent state by optimizing culture conditions

doi:10.1007/s13238-012-2007-8

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Protein Cell ›› 2012, Vol. 3 ›› Issue (1) : 71-79. DOI: 10.1007/s13238-012-2007-8

RESEARCH ARTICLE

Rapid conversion of human ESCs into mouse ESC-like pluripotent state by optimizing culture conditions

Qi Gu^1,2, Jie Hao¹, Xiao-yang Zhao¹, Wei Li¹, Lei Liu¹, Liu Wang¹, Zhong-hua Liu², Qi Zhou¹()

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Abstract

The pluripotent state between human and mouse embryonic stem cells is different. Pluripotent state of human embryonic stem cells (ESCs) is believed to be primed and is similar with that of mouse epiblast stem cells (EpiSCs), which is different from the na?ve state of mouse ESCs. Human ESCs could be converted into a na?ve state through exogenous expression of defined transcription factors (Hanna et al., 2010). Here we report a rapid conversion of human ESCs to mouse ESC-like na?ve states only by modifying the culture conditions. These converted human ESCs, which we called mhESCs (mouse ESC-like human ESCs), have normal karyotype, allow single cell passage, exhibit domed morphology like mouse ESCs and express some pluripotent markers similar with mouse ESCs. Thus the rapid conversion established a na?ve pluripotency in human ESCs like mouse ESCs, and provided a new model to study the regulation of pluripotency.

Keywords

human embryonic stem cells (hESCs) / mouse ESCs / na?ve / pluripotent state

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Qi Gu, Jie Hao, Xiao-yang Zhao, Wei Li, Lei Liu, Liu Wang, Zhong-hua Liu, Qi Zhou. Rapid conversion of human ESCs into mouse ESC-like pluripotent state by optimizing culture conditions. Prot Cell, 2012, 3(1): 71‒79 https://doi.org/10.1007/s13238-012-2007-8

References

[1] Bao, L., He, L., Chen, J., Wu, Z., Liao, J., Rao, L., Ren, J., Li, H., Zhu, H., Qian, L., (2011). Reprogramming of ovine adult fibroblasts to pluripotency via drug-inducible expression of defined factors. Cell Res 21, 600–608 .
[2] Bao, S., Tang, F., Li, X., Hayashi, K., Gillich, A., Lao, K., and Surani, M.A. (2009). Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 461, 1292–1295 19816418.
[3] Bendall, S.C., Stewart, M.H., Menendez, P., George, D., Vijayaragavan, K., Werbowetski-Ogilvie, T., Ramos-Mejia, V., Rouleau, A., Yang, J., Bossé, M., (2007). IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448, 1015–1021 17625568.
[4] 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., (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191–195 17597762.
[5] 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 19109897.
[6] Buryanov, Y.I., and Shevchuk, T.V. (2005). DNA methyltransferases and structural-functional specificity of eukaryotic DNA modification. Biochemistry (Mosc) 70, 730–742 16097936.
[7] Chen, G., Gulbranson, D.R., Hou, Z., Bolin, J.M., Ruotti, V., Probasco, M.D., Smuga-Otto, K., Howden, S.E., Diol, N.R., Propson, N.E., (2011). Chemically defined conditions for human iPSC derivation and culture. Nat Methods 8, 424–429 .
[8] Dvorak, P., Dvorakova, D., Koskova, S., Vodinska, M., Najvirtova, M., Krekac, D., and Hampl, A. (2005). Expression and potential role of fibroblast growth factor 2 and its receptors in human embryonic stem cells. Stem Cells 23, 1200–1211 15955829.
[9] Eiges, R., Schuldiner, M., Drukker, M., Yanuka, O., Itskovitz-Eldor, J., and Benvenisty, N. (2001). Establishment of human embryonic stem cell-transfected clones carrying a marker for undifferentiated cells. Curr Biol 11, 514–518 11413002.
[10] Esteban, M.A., Wang, T., Qin, B., Yang, J., Qin, D., Cai, J., Li, W., Weng, Z., Chen, J., Ni, S., (2010). Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6, 71–79 20036631.
[11] Evans, M.J., and Kaufman, M.H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154–156 7242681.
[12] Ezashi, T., Telugu, B.P., Alexenko, A.P., Sachdev, S., Sinha, S., and Roberts, R.M. (2009). Derivation of induced pluripotent stem cells from pig somatic cells. Proc Natl Acad Sci U S A 106, 10993–10998 19541600.
[13] Folch, J., Cocero, M.J., Chesné, P., Alabart, J.L., Domínguez, V., Cognié, Y., Roche, A., Ferníndez-Arias, A., Martí, J.I., Sánchez, P., (2009). First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71, 1026–1034 19167744.
[14] Guo, G., Yang, J., Nichols, J., Hall, J.S., Eyres, I., Mansfield, W., and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063–1069 19224983.
[15] Han, X., Han, J., Ding, F., Cao, S., Lim, S.S., Dai, Y., Zhang, R., Zhang, Y., Lim, B., and Li, N. (2011). Generation of induced pluripotent stem cells from bovine embryonic fibroblast cells. Cell Res 21, 1509–1512 .
[16] Hanna, J., Cheng, A.W., Saha, K., Kim, J., Lengner, C.J., Soldner, F., Cassady, J.P., Muffat, J., Carey, B.W., and Jaenisch, R. (2010). Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci U S A .
[17] Hanna, J., Markoulaki, S., Mitalipova, M., Cheng, A.W., Cassady, J.P., Staerk, J., Carey, B.W., Lengner, C.J., Foreman, R., Love, J., (2009). Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 4, 513–524 19427283.
[18] Hao, J., Zhu, W., Sheng, C., Yu, Y., and Zhou, Q. (2009). Human parthenogenetic embryonic stem cells: one potential resource for cell therapy. Sci China C Life Sci 52, 599–602 19641863.
[19] Honda, A., Hirose, M., Hatori, M., Matoba, S., Miyoshi, H., Inoue, K., and Ogura, A. (2010). Generation of induced pluripotent stem cells in rabbits: potential experimental models for human regenerative medicine. J Biol Chem 285, 31362–31369 20670936.
[20] Lengner, C.J., Gimelbrant, A.A., Erwin, J.A., Cheng, A.W., Guenther, M.G., Welstead, G.G., Alagappan, R., Frampton, G.M., Xu, P., Muffat, J., (2010). Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell 141, 872–883 20471072.
[21] Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R.E., Schulze, E.N., Song, H., Hsieh, C.L., (2008). Germline competent embryonic stem cells derived from rat blastocysts. Cell 135, 1299–1310 19109898.
[22] Li, Z.K., and Zhou, Q. (2010). Cellular models for disease exploring and drug screening. Protein Cell 1, 355–362 21203947.
[23] Liao, J., Cui, C., Chen, S., Ren, J., Chen, J., Gao, Y., Li, H., Jia, N., Cheng, L., Xiao, H., (2009). Generation of induced pluripotent stem cell lines from adult rat cells. Cell Stem Cell 4, 11–15 19097959.
[24] Liu, H., Zhu, F., Yong, J., Zhang, P., Hou, P., Li, H., Jiang, W., Cai, J., Liu, M., Cui, K., (2008). Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem Cell 3, 587–590 19041774.
[25] Liu, Y., Song, Z., Zhao, Y., Qin, H., Cai, J., Zhang, H., Yu, T., Jiang, S., Wang, G., Ding, M., (2006). A novel chemical-defined medium with bFGF and N2B27 supplements supports undifferentiated growth in human embryonic stem cells. Biochem Biophys Res Commun 346, 131–139 16753134.
[26] Lu, Z., Zhu, W., Yu, Y., Jin, D., Guan, Y., Yao, R., Zhang, Y.A., Zhang, Y., and Zhou, Q. (2010). Derivation and long-term culture of human parthenogenetic embryonic stem cells using human foreskin feeders. J Assist Reprod Genet 27, 285–291 20393797.
[27] Luo, J., Suhr, S.T., Chang, E.A., Wang, K., Ross, P.J., Nelson, L.L., Venta, P.J., Knott, J.G., and Cibelli, J.B. (2011). Generation of leukemia inhibitory factor and basic fibroblast growth factor-dependent induced pluripotent stem cells from canine adult somatic cells. Stem Cells Dev 20, 1669–1678 .
[28] 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 U S A 78, 7634–7638 6950406.
[29] Matsuda, T., Nakamura, T., Nakao, K., Arai, T., Katsuki, M., Heike, T., and Yokota, T. (1999). STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J 18, 4261–4269 10428964.
[30] Najm, F.J., Chenoweth, J.G., Anderson, P.D., Nadeau, J.H., Redline, R.W., McKay, R.D., and Tesar, P.J. (2011). Isolation of epiblast stem cells from preimplantation mouse embryos. Cell Stem Cell 8, 318–325 21362571.
[31] Nichols, J., and Smith, A. (2009). Naive and primed pluripotent states. Cell Stem Cell 4, 487–492 19497275.
[32] Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B., and Zhang, Y. (2003). Role of histone H3 lysine 27 methylation in X inactivation. Science 300, 131–135 12649488.
[33] Rossant, J. (2008). Stem cells and early lineage development. Cell 132, 527–531 18295568.
[34] Smith, A.G., Heath, J.K., Donaldson, D.D., Wong, G.G., Moreau, J., Stahl, M., and Rogers, D. (1988). Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336, 688–690 3143917.
[35] Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–872 18035408.
[36] Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 16904174.
[37] Tesar, P.J., Chenoweth, J.G., Brook, F.A., Davies, T.J., Evans, E.P., Mack, D.L., Gardner, R.L., and McKay, R.D. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196–199 17597760.
[38] 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 9804556.
[39] 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 U S A 92, 7844–7848 7544005.
[40] Vallier, L., Alexander, M., and Pedersen, R.A. (2005). Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118, 4495–4509 16179608.
[41] Wang, S., Tang, X., Niu, Y., Chen, H., Li, B., Li, T., Zhang, X., Hu, Z., Zhou, Q., and Ji, W. (2007). Generation and characterization of rabbit embryonic stem cells. Stem Cells 25, 481–489 17038672.
[42] Williams, R.L., Hilton, D.J., Pease, S., Willson, T.A., Stewart, C.L., Gearing, D.P., Wagner, E.F., Metcalf, D., Nicola, N.A., and Gough, N.M. (1988). Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336, 684–687 3143916.
[43] Xu, R.H., Sampsell-Barron, T.L., Gu, F., Root, S., Peck, R.M., Pan, G., Yu, J., Antosiewicz-Bourget, J., Tian, S., Stewart, R., (2008). NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3, 196–206 18682241.
[44] Xu, Y., Zhu, X., Hahm, H.S., Wei, W., Hao, E., Hayek, A., and Ding, S. (2010). Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci U S A 107, 8129–8134 20406903.
[45] 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 14636556.
[46] 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 18497825.
[47] Zhao, X.Y., Li, W., Lv, Z., Liu, L., Tong, M., Hai, T., Hao, J., Guo, C.L., Ma, Q.W., Wang, L., (2009). iPS cells produce viable mice through tetraploid complementation. Nature 461, 86–90 .
[48] Zhao, X.Y., Lv, Z., Li, W., Zeng, F., and Zhou, Q. (2010). Production of mice using iPS cells and tetraploid complementation. Nat Protoc 5, 963–971 20431542.
[49] Zwaka, T.P., and Thomson, J.A. (2003). Homologous recombination in human embryonic stem cells. Nat Biotechnol 21, 319–321 12577066.