Expanding the boundaries of embryonic stem cells

Cell Stem Cell

Volumn 10, Issue 6, 2012, Pages 666-677

  Ben David, Uri ^a   Kopper, Oded ^a   Benvenisty, Nissim ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

UNTRANSLATED RNA;

CARCINOGENICITY; CELL DIFFERENTIATION; CELL FATE; CELL HETEROGENEITY; DISEASE MODEL; EMBRYONIC STEM CELL; EPIGENETICS; GENE CONTROL; GENETIC DISORDER; GENETIC TRANSCRIPTION; GENOMICS; HUMAN; IMMUNOGENICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; STEM CELL RESEARCH; TISSUE ENGINEERING;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HUMANS;

EID: 84862514386     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.05.003     Document Type: Review

References (142)

1. Adewumi, O., Aflatoonian, B., Ahrlund-Richter, L., Amit, M., Andrews, P.W., Beighton, G., Bello, P.A., Benvenisty, N., Berry, L.S., Bevan, S., et al. (2007). Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 25, 803-816.
2. Agarwal, S., Holton, K.L., and Lanza, R. (2008). Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells 26, 1117-1127.
3. Akopian, V., Andrews, P.W., Beil, S., Benvenisty, N., Brehm, J., Christie, M., Ford, A., Fox, V., Gokhale, P.J., Healy, L., et al. (2010). Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. In Vitro Cell. Dev. Biol. Anim. 46, 247-258.
4. Amit, M., Chebath, J., Margulets, V., Laevsky, I., Miropolsky, Y., Shariki, K., Peri, M., Blais, I., Slutsky, G., Revel, M., et al. (2010). Suspension culture of undifferentiated human embryonic and induced pluripotent stem cells. Stem Cell Rev. 6, 248-259.
5. Amps, K., Andrews, P.W., Anyfantis, G., Armstrong, L., Avery, S., Baharvand, H., Baker, J., Baker, D., Munoz, M.B., Beil, S., et al. (2011). Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat. Biotechnol. 29, 1132-1144.
6. Ang, Y.S., Tsai, S.Y., Lee, D.F., Monk, J., Su, J., Ratnakumar, K., Ding, J., Ge, Y., Darr, H., Chang, B., et al. (2011). Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183-197.
7. Baker, D.E., Harrison, N.J., Maltby, E., Smith, K., Moore, H.D., Shaw, P.J., Heath, P.R., Holden, H., and Andrews, P.W. (2007). Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat. Biotechnol. 25, 207-215.
8. Basma, H., Soto-Gutierrez, A., Yannam, G.R., Liu, L., Ito, R., Yamamoto, T., Ellis, E., Carson, S.D., Sato, S., Chen, Y., et al. (2009). Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. Gastroenterology 136, 990-999.
9. Ben-David, U., and Benvenisty, N. (2011). The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat. Rev. Cancer 11, 268-277.
10. Ben-David, U., Mayshar, Y., and Benvenisty, N. (2011). Large-scale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stem cells. Cell Stem Cell 9, 97-102.
11. Ben-Yosef, D., Malcov, M., and Eiges, R. (2008). PGD-derived human embryonic stem cell lines as a powerful tool for the study of human genetic disorders. Mol. Cell. Endocrinol. 282, 153-158.
12. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
13. Bhutani, N., Brady, J.J., Damian, M., Sacco, A., Corbel, S.Y., and Blau, H.M. (2010). Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042-1047.
14. Biancotti, J.C., Narwani, K., Buehler, N., Mandefro, B., Golan-Lev, T., Yanuka, O., Clark, A., Hill, D., Benvenisty, N., and Lavon, N. (2010). Human embryonic stem cells as models for aneuploid chromosomal syndromes. Stem Cells 28, 1530-1540.
15. Blum, B., Bar-Nur, O., Golan-Lev, T., and Benvenisty, N. (2009). The antiapoptotic gene survivin contributes to teratoma formation by human embryonic stem cells. Nat. Biotechnol. 27, 281-287.
16. Bock, C., Kiskinis, E., Verstappen, G., Gu, H., Boulting, G., Smith, Z.D., Ziller, M., Croft, G.F., Amoroso, M.W., Oakley, D.H., et al. (2011). Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 144, 439-452.
17. Borowiak, M., Maehr, R., Chen, S., Chen, A.E., Tang, W., Fox, J.L., Schreiber, S.L., and Melton, D.A. (2009). Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 4, 348-358.
18. Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956.
19. Brill, L.M., Xiong, W., Lee, K.B., Ficarro, S.B., Crain, A., Xu, Y., Terskikh, A., Snyder, E.Y., and Ding, S. (2009). Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5, 204-213.
20. 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., et al. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195.
21. Buecker, C., and Geijsen, N. (2010). Different flavors of pluripotency, molecular mechanisms, and practical implications. Cell Stem Cell 7, 559-564.
22. Buecker, C., Chen, H.H., Polo, J.M., Daheron, L., Bu, L., Barakat, T.S., Okwieka, P., Porter, A., Gribnau, J., Hochedlinger, K., et al. (2010). A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells. Cell Stem Cell 6, 535-546.
23. Canham, M.A., Sharov, A.A., Ko, M.S., and Brickman, J.M. (2010). Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379.
24. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V.B., Wong, E., Orlov, Y.L., Zhang, W., Jiang, J., et al. (2008). Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117.
25. Chen, S., Borowiak, M., Fox, J.L., Maehr, R., Osafune, K., Davidow, L., Lam, K., Peng, L.F., Schreiber, S.L., Rubin, L.L., et al. (2009). A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat. Chem. Biol. 5, 258-265.
26. Chen, G., Hou, Z., Gulbranson, D.R., and Thomson, J.A. (2010). Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 7, 240-248.
27. Cheng, X., Ying, L., Lu, L., Galvao, A.M., Mills, J.A., Lin, H.C., Kotton, D.N., Shen, S.S., Nostro, M.C., Choi, J.K., et al. (2012). Self-renewing endodermal progenitor lines generated from human pluripotent stem cells. Cell Stem Cell 10, 371-384.
28. Cohen, D.E., and Melton, D. (2011). Turning straw into gold: directing cell fate for regenerative medicine. Nat. Rev. Genet. 12, 243-252.
29. Collin, J., and Lako, M. (2011). Concise review: putting a finger on stem cell biology: zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells. Stem Cells 29, 1021-1033.
30. Colman, A., and Dreesen, O. (2009). Pluripotent stem cells and disease modeling. Cell Stem Cell 5, 244-247.
31. Damjanov, I., and Andrews, P.W. (2007). The terminology of teratocarcinomas and teratomas. Nat. Biotechnol. 25, 1212, discussion 1212.
32. Eiges, R., Schuldiner, M., Drukker, M., Yanuka, O., Itskovitz-Eldor, J., and Benvenisty, N. (2001). Establishment of human embryonic stem celltransfected clones carrying a marker for undifferentiated cells. Curr. Biol. 11, 514-518.
33. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., and Sasai, Y. (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532.
34. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., and Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
35. Elling, U., Taubenschmid, J., Wirnsberger, G., O'Malley, R., Demers, S.P., Vanhaelen, Q., Shukalyuk, A.I., Schmauss, G., Schramek, D., Schnuetgen, F., et al. (2011). Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 9, 563-574.
36. Ellis, J., Baum, C., Benvenisty, N., Mostoslavsky, G., Okano, H., Stanford, W.L., Porteus, M., and Sadelain, M. (2010). Benefits of utilizing gene-modified iPSCs for clinical applications. Cell Stem Cell 7, 429-430.
37. Fouse, S.D., Shen, Y., Pellegrini, M., Cole, S., Meissner, A., Van Neste, L., Jaenisch, R., and Fan, G. (2008). Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2, 160-169.
38. Gaspar-Maia, A., Alajem, A., Polesso, F., Sridharan, R., Mason, M.J., Heidersbach, A., Ramalho-Santos, J., McManus, M.T., Plath, K., Meshorer, E., et al. (2009). Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863-868.
39. Gaspar-Maia, A., Alajem, A., Meshorer, E., and Ramalho-Santos, M. (2011). Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36-47.
40. Giudice, A., and Trounson, A. (2008). Genetic modification of human embryonic stem cells for derivation of target cells. Cell Stem Cell 2, 422-433.
41. Goldring, C.E., Duffy, P.A., Benvenisty, N., Andrews, P.W., Ben-David, U., Eakins, R., French, N., Hanley, N.A., Kelly, L., Kitteringham, N.R., et al. (2011). Assessing the safety of stem cell therapeutics. Cell Stem Cell 8, 618-628.
42. Guenther, M.G., Levine, S.S., Boyer, L.A., Jaenisch, R., and Young, R.A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88.
43. Guttman, M., Amit, I., Garber, M., French, C., Lin, M.F., Feldser, D., Huarte, M., Zuk, O., Carey, B.W., Cassady, J.P., et al. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227.
44. Han, D.W., Tapia, N., Joo, J.Y., Greber, B., Arauzo-Bravo, M.J., Bernemann, C., Ko, K., Wu, G., Stehling, M., Do, J.T., et al. (2010). Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell 143, 617-627.
45. Hanna, J., Markoulaki, S., Mitalipova, M., Cheng, A.W., Cassady, J.P., Staerk, J., Carey, B.W., Lengner, C.J., Foreman, R., Love, J., et al. (2009). Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 4, 513-524.
46. 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. USA 107, 9222-9227.
47. Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S., and Saitou, M. (2011). Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146, 519-532.
48. Hockemeyer, D., Soldner, F., Beard, C., Gao, Q., Mitalipova, M., DeKelver, R.C., Katibah, G.E., Amora, R., Boydston, E.A., Zeitler, B., et al. (2009). Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 27, 851-857.
49. Hockemeyer, D., Wang, H., Kiani, S., Lai, C.S., Gao, Q., Cassady, J.P., Cost, G.J., Zhang, L., Santiago, Y., Miller, J.C., et al. (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29, 731-734.
50. Idelson, M., Alper, R., Obolensky, A., Ben-Shushan, E., Hemo, I., Yachimovich-Cohen, N., Khaner, H., Smith, Y., Wiser, O., Gropp, M., et al. (2009). Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 5, 396-408.
51. International Stem Cell Banking Initiative. (2009). Consensus guidance for banking and supply of human embryonic stem cell lines for research purposes. Stem Cell Rev. 5, 301-314.
52. Ito, S., D'Alessio, A.C., Taranova, O.V., Hong, K., Sowers, L.C., and Zhang, Y. (2010). Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133.
53. Jeddeloh, J.A., Greally, J.M., and Rando, O.J. (2008). Reduced-representation methylation mapping. Genome Biol. 9, 231.
54. Kadereit, S., and Trounson, A. (2011). In vitro immunogenicity of undifferentiated pluripotent stem cells (PSC) and derived lineages. Semin. Immunopathol. 33, 551-562.
55. Kim, K., Lerou, P., Yabuuchi, A., Lengerke, C., Ng, K., West, J., Kirby, A., Daly, M.J., and Daley, G.Q. (2007a). Histocompatible embryonic stem cells by parthenogenesis. Science 315, 482-486.
56. Kim, K., Ng, K., Rugg-Gunn, P.J., Shieh, J.H., Kirak, O., Jaenisch, R., Wakayama, T., Moore, M.A., Pedersen, R.A., and Daley, G.Q. (2007b). Recombination signatures distinguish embryonic stem cells derived by parthenogenesis and somatic cell nuclear transfer. Cell Stem Cell 1, 346-352.
57. Kim, J., Chu, J., Shen, X., Wang, J., and Orkin, S.H. (2008). An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132, 1049-1061.
58. Kim, J., Woo, A.J., Chu, J., Snow, J.W., Fujiwara, Y., Kim, C.G., Cantor, A.B., and Orkin, S.H. (2010). A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143, 313-324.
59. Kobayashi, T., Yamaguchi, T., Hamanaka, S., Kato-Itoh, M., Yamazaki, Y., Ibata, M., Sato, H., Lee, Y.S., Usui, J., Knisely, A.S., et al. (2010). Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell 142, 787-799.
60. Koh, K.P., Yabuuchi, A., Rao, S., Huang, Y., Cunniff, K., Nardone, J., Laiho, A., Tahiliani, M., Sommer, C.A., Mostoslavsky, G., et al. (2011). Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8, 200-213.
61. Kolata, G. (2007). Scientists Bypass Need for Embryo to Get Stem Cells. The New York Times: http://www.nytimes.com/2007/11/21/science/21stem.html.
62. Kriks, S., Shim, J.W., Piao, J., Ganat, Y.M., Wakeman, D.R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A., et al. (2011). Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551.
63. Kroon, E., Martinson, L.A., Kadoya, K., Bang, A.G., Kelly, O.G., Eliazer, S., Young, H., Richardson, M., Smart, N.G., Cunningham, J., et al. (2008). Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26, 443-452.
64. Kunarso, G., Chia, N.Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y.S., Ng, H.H., and Bourque, G. (2010). Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42, 631-634.
65. Laustriat, D., Gide, J., and Peschanski, M. (2010). Human pluripotent stem cells in drug discovery and predictive toxicology. Biochem. Soc. Trans. 38, 1051-1057.
66. Lavon, N., Yanuka, O., and Benvenisty, N. (2004). Differentiation and isolation of hepatic-like cells from human embryonic stem cells. Differentiation 72, 230-238.
67. Leavitt, A.D., and Hamlett, I. (2011). Homologous recombination in human embryonic stem cells: a tool for advancing cell therapy and understanding and treating human disease. Clin. Transl. Sci. 4, 298-305.
68. Leeb, M., and Wutz, A. (2011). Derivation of haploid embryonic stem cells from mouse embryos. Nature 479, 131-134.
69. Lefort, N., Feyeux, M., Bas, C., Feraud, O., Bennaceur-Griscelli, A., Tachdjian, G., Peschanski, M., and Perrier, A.L. (2008). Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nat. Biotechnol. 26, 1364-1366.
70. Lei, T., Jacob, S., Ajil-Zaraa, I., Dubuisson, J.B., Irion, O., Jaconi, M., and Feki, A. (2007). Xeno-free derivation and culture of human embryonic stem cells: current status, problems and challenges. Cell Res. 17, 682-688.
71. Lensch, M.W., and Ince, T.A. (2007). The terminology of teratocarcinomas and teratomas. Nat. Biotechnol. 25, 1211, author reply 1211-1212.
72. Li, W., Wei, W., Zhu, S., Zhu, J., Shi, Y., Lin, T., Hao, E., Hayek, A., Deng, H., and Ding, S. (2009). Generation of rat and human induced pluripotent stem cells by combining genetic reprogramming and chemical inhibitors. Cell Stem Cell 4, 16-19.
73. Lister, R., Pelizzola, M., Dowen, R.H., Hawkins, R.D., Hon, G., Tonti-Filippini, J., Nery, J.R., Lee, L., Ye, Z., Ngo, Q.M., et al. (2009). Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322.
74. Loh, Y.H., Wu, Q., Chew, J.L., Vega, V.B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J., et al. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38, 431-440.
75. Loh, Y.H., Yang, L., Yang, J.C., Li, H., Collins, J.J., and Daley, G.Q. (2011). Genomic approaches to deconstruct pluripotency. Annu. Rev. Genomics Hum. Genet. 12, 165-185.
76. Lu, R., Markowetz, F., Unwin, R.D., Leek, J.T., Airoldi, E.M., MacArthur, B.D., Lachmann, A., Rozov, R., Ma'ayan, A., Boyer, L.A., et al. (2009). Systems-level dynamic analyses of fate change in murine embryonic stem cells. Nature 462, 358-362.
77. Mandenius, C.F., Steel, D., Noor, F., Meyer, T., Heinzle, E., Asp, J., Arain, S., Kraushaar, U., Bremer, S., Class, R., et al. (2011). Cardiotoxicity testing using pluripotent stem cell-derived human cardiomyocytes and state-of-the-art bioanalytics: a review. J. Appl. Toxicol. 31, 191-205.
78. Margaritis, T., and Holstege, F.C. (2008). Poised RNA polymerase II gives pause for thought. Cell 133, 581-584.
79. Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.
80. Marson, A., Levine, S.S., Cole, M.F., Frampton, G.M., Brambrink, T., Johnstone, S., Guenther, M.G., Johnston, W.K., Wernig, M., Newman, J., et al. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533.
81. Martinez Arias, A., and Brickman, J.M. (2011). Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr. Opin. Cell Biol. 23, 650-656.
82. Martinez, N.J., and Gregory, R.I. (2010). MicroRNA gene regulatory pathways in the establishment and maintenance of ESC identity. Cell Stem Cell 7, 31-35.
83. Martins-Taylor, K., and Xu, R.H. (2010). Determinants of pluripotency: from avian, rodents, to primates. J. Cell. Biochem. 109, 16-25.
84. Mayshar, Y., Ben-David, U., Lavon, N., Biancotti, J.C., Yakir, B., Clark, A.T., Plath, K., Lowry, W.E., and Benvenisty, N. (2010). Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 7, 521-531.
85. Mayshar, Y., Yanuka, O., and Benvenisty, N. (2011). Teratogen screening using transcriptome profiling of differentiating human embryonic stem cells. J. Cell. Mol. Med. 15, 1393-1401.
86. Meissner, A. (2010). Epigenetic modifications in pluripotent and differentiated cells. Nat. Biotechnol. 28, 1079-1088.
87. Meissner, A., Mikkelsen, T.S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B.E., Nusbaum, C., Jaffe, D.B., et al. (2008). Genomescale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
88. Murry, C.E., and Keller, G. (2008). Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680.
89. Ng, H.H., and Surani, M.A. (2011). The transcriptional and signalling networks of pluripotency. Nat. Cell Biol. 13, 490-496.
90. Nichols, J., and Smith, A. (2009). Naive and primed pluripotent states. Cell Stem Cell 4, 487-492.
91. Noggle, S., Fung, H.L., Gore, A., Martinez, H., Satriani, K.C., Prosser, R., Oum, K., Paull, D., Druckenmiller, S., Freeby, M., et al. (2011). Human oocytes reprogram somatic cells to a pluripotent state. Nature 478, 70-75.
92. Normile, D., Vogel, G., and Couzin, J. (2006). Cloning. South Korean team's remaining human stem cell claim demolished. Science 311, 156-157.
93. Ohgushi, M., Matsumura, M., Eiraku, M., Murakami, K., Aramaki, T., Nishiyama, A., Muguruma, K., Nakano, T., Suga, H., Ueno, M., et al. (2010). Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 7, 225-239.
94. Orkin, S.H., and Hochedlinger, K. (2011). Chromatin connections to pluripotency and cellular reprogramming. Cell 145, 835-850.
95. Oshima, K., Shin, K., Diensthuber, M., Peng, A.W., Ricci, A.J., and Heller, S. (2010). Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell 141, 704-716.
96. Pardo, M., Lang, B., Yu, L., Prosser, H., Bradley, A., Babu, M.M., and Choudhary, J. (2010). An expanded Oct4 interaction network: implications for stem cell biology, development, and disease. Cell Stem Cell 6, 382-395.
97. Pasini, D., Cloos, P.A., Walfridsson, J., Olsson, L., Bukowski, J.P., Johansen, J.V., Bak, M., Tommerup, N., Rappsilber, J., and Helin, K. (2010). JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310.
98. Pastor, W.A., Pape, U.J., Huang, Y., Henderson, H.R., Lister, R., Ko, M., McLoughlin, E.M., Brudno, Y., Mahapatra, S., Kapranov, P., et al. (2011). Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473, 394-397.
99. Peng, J.C., Valouev, A., Swigut, T., Zhang, J., Zhao, Y., Sidow, A., and Wysocka, J. (2009). Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139, 1290-1302.
100. Robertson, N.J., Brook, F.A., Gardner, R.L., Cobbold, S.P., Waldmann, H., and Fairchild, P.J. (2007). Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc. Natl. Acad. Sci. USA 104, 20920-20925.
101. Robinton, D.A., and Daley, G.Q. (2012). The promise of induced pluripotent stem cells in research and therapy. Nature 481, 295-305.
102. Rubin, L.L. (2008). Stem cells and drug discovery: the beginning of a new era? Cell 132, 549-552.
103. Schwartz, S.D., Hubschman, J.P., Heilwell, G., Franco-Cardenas, V., Pan, C.K., Ostrick, R.M., Mickunas, E., Gay, R., Klimanskaya, I., and Lanza, R. (2012). Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379, 713-720.
104. Scott, C.T., McCormick, J.B., DeRouen, M.C., and Owen-Smith, J. (2011). Democracy derived? New trajectories in pluripotent stem cell research. Cell 145, 820-826.
105. Sharon, N., Mor, I., Golan-lev, T., Fainsod, A., and Benvenisty, N. (2011). Molecular and functional characterizations of gastrula organizer cells derived from human embryonic stem cells. Stem Cells 29, 600-608.
106. Sheik Mohamed, J., Gaughwin, P.M., Lim, B., Robson, P., and Lipovich, L. (2010). Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16, 324-337.
107. Singh Roy, N., Nakano, T., Xuing, L., Kang, J., Nedergaard, M., and Goldman, S.A. (2005). Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp. Neurol. 196, 224-234.
108. Song, H., Chung, S.K., and Xu, Y. (2010). Modeling disease in human ESCs using an efficient BAC-based homologous recombination system. Cell Stem Cell 6, 80-89.
109. Spence, J.R., Mayhew, C.N., Rankin, S.A., Kuhar, M.F., Vallance, J.E., Tolle, K., Hoskins, E.E., Kalinichenko, V.V., Wells, S.I., Zorn, A.M., et al. (2011). Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470, 105-109.
110. Steiner, D., Khaner, H., Cohen, M., Even-Ram, S., Gil, Y., Itsykson, P., Turetsky, T., Idelson, M., Aizenman, E., Ram, R., et al. (2010). Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat. Biotechnol. 28, 361-364.
111. Stelzer, Y., Yanuka, O., and Benvenisty, N. (2011). Global analysis of parental imprinting in human parthenogenetic induced pluripotent stem cells. Nat. Struct. Mol. Biol. 18, 735-741.
112. Stewart, M.H., Bendall, S.C., Levadoux-Martin, M., and Bhatia, M. (2010). Clonal tracking of hESCs reveals differential contribution to functional assays. Nat. Methods 7, 917-922.
113. Suga, H., Kadoshima, T., Minaguchi, M., Ohgushi, M., Soen, M., Nakano, T., Takata, N., Wataya, T., Muguruma, K., Miyoshi, H., et al. (2011). Self-formation of functional adenohypophysis in three-dimensional culture. Nature 480, 57-62.
114. Tachibana, M., Sparman, M., Ramsey, C., Ma, H., Lee, H.S., Penedo, M.C., and Mitalipov, S. (2012). Generation of chimeric rhesus monkeys. Cell 148, 285-295.
115. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L., et al. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935.
116. Takahashi, T., Lord, B., Schulze, P.C., Fryer, R.M., Sarang, S.S., Gullans, S.R., and Lee, R.T. (2003). Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107, 1912-1916.
117. Tang, C., Lee, A.S., Volkmer, J.P., Sahoo, D., Nag, D., Mosley, A.R., Inlay, M.A., Ardehali, R., Chavez, S.L., Pera, R.R., et al. (2011). An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratomaforming cells. Nat. Biotechnol. 29, 829-834.
118. 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.
119. 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.
120. Thomson, M., Liu, S.J., Zou, L.N., Smith, Z., Meissner, A., and Ramanathan, S. (2011). Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145, 875-889.
121. Toyooka, Y., Shimosato, D., Murakami, K., Takahashi, K., and Niwa, H. (2008). Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135, 909-918.
122. Trounson, A., Thakar, R.G., Lomax, G., and Gibbons, D. (2011). Clinical trials for stem cell therapies. BMC Med. 9, 52.
123. Tulpule, A., Lensch, M.W., Miller, J.D., Austin, K., D'Andrea, A., Schlaeger, T.M., Shimamura, A., and Daley, G.Q. (2010). Knockdown of Fanconi anemia genes in human embryonic stem cells reveals early developmental defects in the hematopoietic lineage. Blood 115, 3453-3462.
124. Unger, C., Skottman, H., Blomberg, P., Dilber, M.S., and Hovatta, O. (2008). Good manufacturing practice and clinical-grade human embryonic stem cell lines. Hum. Mol. Genet. 17, R48-R53.
125. Urbach, A., Bar-Nur, O., Daley, G.Q., and Benvenisty, N. (2010). Differential modeling of fragile X syndrome by human embryonic stem cells and induced pluripotent stem cells. Cell Stem Cell 6, 407-411.
126. Urbach, A., Schuldiner, M., and Benvenisty, N. (2004). Modeling for Lesch- Nyhan disease by gene targeting in human embryonic stem cells. Stem Cells 22, 635-641.
127. Valamehr, B., Tsutsui, H., Ho, C.M., and Wu, H. (2011). Developing defined culture systems for human pluripotent stem cells. Regen. Med. 6, 623-634.
128. Van Hoof, D., Munoz, J., Braam, S.R., Pinkse, M.W., Linding, R., Heck, A.J., Mummery, C.L., and Krijgsveld, J. (2009). Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5, 214-226.
129. Viré, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., Morey, L., Van Eynde, A., Bernard, D., Vanderwinden, J.M., et al. (2006). The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874.
130. Viswanathan, S.R., Daley, G.Q., and Gregory, R.I. (2008). Selective blockade of microRNA processing by Lin28. Science 320, 97-100.
131. Wakayama, T., Perry, A.C., 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.
132. Wang, J., Rao, S., Chu, J., Shen, X., Levasseur, D.N., Theunissen, T.W., and Orkin, S.H. (2006). A protein interaction network for pluripotency of embryonic stem cells. Nature 444, 364-368.
133. Wang, W., Yang, J., Liu, H., Lu, D., Chen, X., Zenonos, Z., Campos, L.S., Rad, R., Guo, G., Zhang, S., et al. (2011a). Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. Proc. Natl. Acad. Sci. USA 108, 18283-18288.
134. Wang, Y.C., Nakagawa, M., Garitaonandia, I., Slavin, I., Altun, G., Lacharite, R.M., Nazor, K.L., Tran, H.T., Lynch, C.L., Leonardo, T.R., et al. (2011b). Specific lectin biomarkers for isolation of human pluripotent stem cells identified through array-based glycomic analysis. Cell Res. 21, 1551-1563.
135. Wang, Z., Oron, E., Nelson, B., Razis, S., and Ivanova, N. (2012). Distinct Lineage Specification Roles for NANOG, OCT4, and SOX2 in Human Embryonic Stem Cells. Cell Stem Cell 10, 440-454.
136. Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J.B., Nishikawa, S., Muguruma, K., and Sasai, Y. (2007). A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686.
137. Wen, B., Wu, H., Shinkai, Y., Irizarry, R.A., and Feinberg, A.P. (2009). Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat. Genet. 41, 246-250.
138. West, P.R., Weir, A.M., Smith, A.M., Donley, E.L., and Cezar, G.G. (2010). Predicting human developmental toxicity of pharmaceuticals using human embryonic stem cells and metabolomics. Toxicol. Appl. Pharmacol. 247, 18-27.
139. 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.
140. Wobus, A.M., and Loser, P. (2011). Present state and future perspectives of using pluripotent stem cells in toxicology research. Arch. Toxicol. 85, 79-117.
141. Young, R.A. (2011). Control of the embryonic stem cell state. Cell 144, 940-954.
142. Ziller, M.J., Muller, F., Liao, J., Zhang, Y., Gu, H., Bock, C., Boyle, P., Epstein, C.B., Bernstein, B.E., Lengauer, T., et al. (2011). Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet. 7, e1002389.