Table of Contents
ISRN Stem Cells
Volume 2014 (2014), Article ID 208067, 19 pages
http://dx.doi.org/10.1155/2014/208067
Review Article

The States of Pluripotency: Pluripotent Lineage Development in the Embryo and in the Dish

The Menzies Research Institute and the University of Tasmania, 17 Liverpool Street, Hobart, TAS 7000, Australia

Received 10 September 2013; Accepted 22 October 2013; Published 24 March 2014

Academic Editors: K. Guan, H. Koide, and S. Ottolenghi

Copyright © 2014 Joy Rathjen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. J. Kelly, “Studies of the developmental potential of 4- and 8-cell stage mouse blastomeres,” Journal of Experimental Zoology, vol. 200, no. 3, pp. 365–376, 1977. View at Google Scholar · View at Scopus
  2. W. Garner and A. McLaren, “Cell distribution in chimaeric mouse embryos before implantation,” Journal of Embryology and Experimental Morphology, vol. 32, no. 2, pp. 495–503, 1974. View at Google Scholar · View at Scopus
  3. H. Balakier and R. A. Pedersen, “Allocation of cells to inner cell mass and trophectoderm lineages in preimplantation mouse embryos,” Developmental Biology, vol. 90, no. 2, pp. 352–362, 1982. View at Google Scholar · View at Scopus
  4. G. Guo, M. Huss, G. Q. Tong et al., “Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst,” Developmental Cell, vol. 18, no. 4, pp. 675–685, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. J. B. Levy, M. H. Johnson, H. Goodall, and B. Maro, “The timing of compaction: control of a major developmental transition in mouse early embryogenesis,” Journal of Embryology and Experimental Morphology, vol. 95, pp. 213–237, 1986. View at Google Scholar · View at Scopus
  6. T. Ducibella, T. Ukena, M. Karnovsky, and E. Anderson, “Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo,” Journal of Cell Biology, vol. 74, no. 1, pp. 153–167, 1977. View at Google Scholar · View at Scopus
  7. W. J. Reeve and C. A. Ziomek, “Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction,” Journal of Embryology and Experimental Morphology, vol. 62, pp. 339–350, 1981. View at Google Scholar · View at Scopus
  8. E. Lehtonen and R. A. Badley, “Localization of cytoskeletal proteins in preimplantation mouse embryos,” Journal of Embryology and Experimental Morphology, vol. 55, pp. 211–225, 1980. View at Google Scholar · View at Scopus
  9. A. H. Handyside, “Distribution of antibody and lectin-binding sites on dissociated blastomeres from mouse morulae: evidence for polarization at compaction,” Journal of Embryology and Experimental Morphology, vol. 60, pp. 99–116, 1980. View at Google Scholar · View at Scopus
  10. J. R. McLachlin, S. Caveney, and G. M. Kidder, “Control of gap junction formation in early mouse embryos,” Developmental Biology, vol. 98, no. 1, pp. 155–164, 1983. View at Google Scholar · View at Scopus
  11. F. D. Houghton, K. J. Barr, G. Walter et al., “Functional significance of Gap junctional coupling in preimplantation development,” Biology of Reproduction, vol. 66, no. 5, pp. 1403–1412, 2002. View at Google Scholar · View at Scopus
  12. D. Riethmacher, V. Brinkmanni, and C. Birchmeier, “A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 3, pp. 855–859, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Larue, M. Ohsugi, J. Hirchenhain, and R. Kemler, “E-cadherin null mutant embryos fail to form a trophectoderm epithelium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 17, pp. 8263–8267, 1994. View at Publisher · View at Google Scholar · View at Scopus
  14. N. G. Kan, M. P. Stemmler, D. Junghans et al., “Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm,” Development, vol. 134, no. 1, pp. 31–41, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Hyenne, S. Louvet-Vallée, A. El-Amraoui, C. Petit, B. Maro, and M. Simmler, “Vezatin, a protein associated to adherens junctions, is required for mouse blastocyst morphogenesis,” Developmental Biology, vol. 287, no. 1, pp. 180–191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. I. Khang, S. Sonn, J. Park, K. Rhee, D. Park, and K. Kim, “Expression of epithin in mouse preimplantation development: its functional role in compaction,” Developmental Biology, vol. 281, no. 1, pp. 134–144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. W. N. De Vries, A. V. Evsikov, B. E. Haac et al., “Maternal β-catenin and E-cadherin in mouse development,” Development, vol. 131, no. 18, pp. 4435–4445, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Chen, D. Wang, Z. Wu, L. Ma, and G. Q. Daley, “Molecular basis of the first cell fate determination in mouse embryogenesis,” Cell Research, vol. 20, no. 9, pp. 982–993, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Kurotaki, K. Hatta, K. Nakao, Y. Nabeshima, and T. Fujimori, “Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape,” Science, vol. 316, no. 5825, pp. 719–723, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. M. H. Johnson and C. A. Ziomek, “The foundation of two distinct cell lineages within the mouse morula,” Cell, vol. 24, no. 1, pp. 71–80, 1981. View at Google Scholar · View at Scopus
  21. T. P. Fleming, “A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst,” Developmental Biology, vol. 119, no. 2, pp. 520–531, 1987. View at Google Scholar · View at Scopus
  22. R. A. Pedersen, K. Wu, and H. Balakier, “Origin of the inner cell mass in mouse embryos: cell lineage analysis by microinjection,” Developmental Biology, vol. 117, no. 2, pp. 581–595, 1986. View at Google Scholar · View at Scopus
  23. R. L. Gardner, “Contributions of blastocyst micromanipulation to the study of mammalian development,” Bioessays, vol. 20, no. 2, pp. 168–180, 1998. View at Google Scholar
  24. A. Suwińska, R. Czołowska, W. Ozdzeński, and A. K. Tarkowski, “Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos,” Developmental Biology, vol. 322, no. 1, pp. 133–144, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. S. A. Morris, R. T. Y. Teo, H. Li, P. Robson, D. M. Glover, and M. Zernicka-Goetz, “Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 14, pp. 6364–6369, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Yamanaka, F. Lanner, and J. Rossant, “FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst,” Development, vol. 137, no. 5, pp. 715–724, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Dietrich and T. Hiiragi, “Stochastic patterning in the mouse pre-implantation embryo,” Development, vol. 134, no. 23, pp. 4219–4231, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Dyce, M. George, H. Goodall, and T. P. Fleming, “Do trophectoderm and inner cell mass cells in the mouse blastocyst maintain discrete lineages,” Development, vol. 100, no. 4, pp. 685–698, 1987. View at Google Scholar · View at Scopus
  29. N. Nishioka, S. Yamamoto, H. Kiyonari et al., “Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos,” Mechanisms of Development, vol. 125, no. 3-4, pp. 270–283, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Yagi, M. J. Kohn, I. Karavanova et al., “Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development,” Development, vol. 134, no. 21, pp. 3827–3836, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Nishioka, K. Inoue, K. Adachi et al., “The hippo signaling pathway components Lats and Yap pattern tead4 activity to distinguish mouse trophectoderm from inner cell mass,” Developmental Cell, vol. 16, no. 3, pp. 398–410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Lorthongpanich, T. P. Doris, V. Limviphuvadh, B. B. Knowles, and D. Solter, “Developmental fate and lineage commitment of singled mouse blastomeres,” Development, vol. 139, no. 20, pp. 3722–3731, 2012. View at Publisher · View at Google Scholar
  33. I. Chambers and S. R. Tomlinson, “The transcriptional foundation of pluripotency,” Development, vol. 136, no. 14, pp. 2311–2322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Nichols, B. Zevnik, K. Anastassiadis et al., “Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4,” Cell, vol. 95, no. 3, pp. 379–391, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Mitsui, Y. Tokuzawa, H. Itoh et al., “The homeoprotein nanog is required for maintenance of pluripotency in mouse epiblast and ES cells,” Cell, vol. 113, no. 5, pp. 631–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Silva, J. Nichols, T. W. Theunissen et al., “Nanog is the gateway to the pluripotent ground state,” Cell, vol. 138, no. 4, pp. 722–737, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. A. Avilion, S. K. Nicolis, L. H. Pevny, L. Perez, N. Vivian, and R. Lovell-Badge, “Multipotent cell lineages in early mouse development depend on SOX2 function,” Genes and Development, vol. 17, no. 1, pp. 126–140, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Keramari, J. Razavi, K. A. Ingman et al., “Sox2 is essential for formation of trophectoderm in the preimplantation embryo,” PLoS ONE, vol. 5, no. 11, Article ID e13952, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Ralston and J. Rossant, “Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo,” Developmental Biology, vol. 313, no. 2, pp. 614–629, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Chen, A. Yabuuchi, S. Eminli et al., “Cross-regulation of the nanog and Cdx2 promoters,” Cell Research, vol. 19, no. 9, pp. 1052–1061, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Niwa, Y. Toyooka, D. Shimosato et al., “Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation,” Cell, vol. 123, no. 5, pp. 917–929, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Wang, S. Sengupta, L. Magnani, C. A. Wilson, R. W. Henry, and J. G. Knott, “Brg1 is required for Cdx2-mediated repression of Oct4 expression in mouse blastocysts,” PLoS ONE, vol. 5, no. 5, Article ID e10622, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Nishiyama, L. Xin, A. A. Sharov et al., “Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors,” Cell Stem Cell, vol. 5, no. 4, pp. 420–433, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Chazaud, Y. Yamanaka, T. Pawson, and J. Rossant, “Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway,” Developmental Cell, vol. 10, no. 5, pp. 615–624, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Plusa, A. Piliszek, S. Frankenberg, J. Artus, and A. Hadjantonakis, “Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst,” Development, vol. 135, no. 18, pp. 3081–3091, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Artus, A. Piliszek, and A. Hadjantonakis, “The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17,” Developmental Biology, vol. 350, no. 2, pp. 393–404, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. P. J. Rugg-Gunn, B. J. Cox, F. Lanner et al., “Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells,” Developmental Cell, vol. 22, no. 4, pp. 887–901, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. A. M. Laeno, D. A. Tamashiro, and V. B. Alarcon, “Rho-associated kinase activity is required for proper morphogenesis of the inner cell mass in the mouse blastocyst,” Biology of Reproduction, vol. 89, no. 5, p. 122, 2013. View at Publisher · View at Google Scholar
  49. R. L. Gardner, “Regeneration of endoderm from primitive ectoderm in the mouse embryo: fact or artifact?” Journal of Embryology and Experimental Morphology, vol. 88, pp. 303–326, 1985. View at Google Scholar · View at Scopus
  50. J. Nichols, J. Silva, M. Roode, and A. Smith, “Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo,” Development, vol. 136, no. 19, pp. 3215–3222, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Frankenberg, F. Gerbe, S. Bessonnard et al., “Primitive endoderm differentiates via a three-step mechanism involving nanog and RTK signaling,” Developmental Cell, vol. 21, no. 6, pp. 1005–1013, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. A. M. Cheng, T. M. Saxton, R. Sakai et al., “Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation,” Cell, vol. 95, no. 6, pp. 793–803, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Arman, R. Haffner-Krausz, Y. Chen, J. K. Heath, and P. Lonai, “Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 9, pp. 5082–5087, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. S. N. Goldin and V. E. Papaioannou, “Paracrine action of FGF4 during periimplantation development maintains trophectoderm and primitive endoderm,” Genesis, vol. 36, no. 1, pp. 40–47, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Yuan, N. Corbi, C. Basilico, and L. Dailey, “Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3,” Genes and Development, vol. 9, no. 21, pp. 2635–2645, 1995. View at Google Scholar · View at Scopus
  56. M. H. L. Snow, “Gastrulation in the mouse: growth and regionalization of the epiblast,” Journal of Embryology and Experimental Morphology, vol. 42, pp. 293–303, 1977. View at Google Scholar · View at Scopus
  57. D. Solter, N. Škreb, and I. Damjanov, “Cell cycle analysis in the mouse egg-cylinder,” Experimental Cell Research, vol. 64, no. 2, pp. 331–334, 1971. View at Google Scholar · View at Scopus
  58. E. Stead, J. White, R. Faast et al., “Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities,” Oncogene, vol. 21, no. 54, pp. 8320–8333, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Coucouvanis and G. R. Martin, “Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo,” Cell, vol. 83, no. 2, pp. 279–287, 1995. View at Google Scholar · View at Scopus
  60. R. L. Gardner and J. Rossant, “Investigation of the fate of 4.5 day post-coitum mouse inner cell mass cells by blastocyst injection,” Journal of Embryology and Experimental Morphology, vol. 52, pp. 141–152, 1979. View at Google Scholar · View at Scopus
  61. F. A. Brook and R. L. Gardner, “The origin and efficient derivation of embryonic stem cells in the mouse,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 11, pp. 5709–5712, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. R. S. Beddington, “The origin of foetal tissues during gastrulation in the rodent,” in Development in Mammals, M. H. Johnson, Ed., pp. 1–32, Elesevier, Amsterdam, The Netherlands, 1983. View at Google Scholar
  63. J. Rossant, “Cell commitment in early rodent development,” in Development in Mammals, M. H. Johnson, Ed., pp. 119–150, Elesevier, Amsterdam, The Netherlands, 1977. View at Google Scholar
  64. R. L. Gardner, “Manipulations on the blastocyst,” Advances in Bioscience, vol. 6, pp. 279–296, 1971. View at Google Scholar
  65. T. A. Pelton, S. Sharma, T. C. Schulz, J. Rathjen, and P. D. Rathjen, “Transient pluripotent cell populations during primitive ectoderm formation: correlation of in vivo and in vitro pluripotent cell development,” Journal of Cell Science, vol. 115, no. 2, pp. 329–339, 2002. View at Google Scholar · View at Scopus
  66. A. H. Hart, L. Hartley, M. Ibrahim, and L. Robb, “Identification, cloning and expression analysis of the pluripotency promoting nanog genes in mouse and human,” Developmental Dynamics, vol. 230, no. 1, pp. 187–198, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. I. Chambers, D. Colby, M. Robertson et al., “Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells,” Cell, vol. 113, no. 5, pp. 643–655, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. O. Haub and M. Goldfarb, “Expression of the fibroblast growth factor-5 gene in the mouse embryo,” Development, vol. 112, no. 2, pp. 397–406, 1991. View at Google Scholar · View at Scopus
  69. P. Gu, B. Goodwin, A. C.-K. Chung et al., “Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development,” Molecular and Cellular Biology, vol. 25, no. 9, pp. 3492–3505, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Sugimoto, S. Tan, and N. Takagi, “X chromosome inactivation revealed by the X-linked lacZ transgene activity in periimplantation mouse embryos,” International Journal of Developmental Biology, vol. 44, no. 2, pp. 177–182, 2000. View at Google Scholar · View at Scopus
  71. R. L. Gardner and M. F. Lyon, “Biological sciences: X chromosome inactivation studied by injection of a single cell into the mouse blastocyst,” Nature, vol. 231, no. 5302, pp. 385–386, 1971. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Rastan, “Timing of X-chromosome inactivation in postimplanation mouse embryos,” Journal of Embryology and Experimental Morphology, vol. 71, pp. 11–24, 1982. View at Google Scholar · View at Scopus
  73. M. Monk and M. I. Harper, “Sequential X chromosome inactivation coupled with cellular differentiation in early mouse embryos,” Nature, vol. 281, no. 5729, pp. 311–313, 1979. View at Google Scholar · View at Scopus
  74. E. Heard, “Recent advances in X-chromosome inactivation,” Current Opinion in Cell Biology, vol. 16, no. 3, pp. 247–255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Borgel, S. Guibert, Y. Li et al., “Targets and dynamics of promoter DNA methylation during early mouse development,” Nature Genetics, vol. 42, no. 12, pp. 1093–1100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Williams, C. Burdsal, A. Periasamy, M. Lewandoski, and A. Sutherland, “Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population,” Developmental Dynamics, vol. 241, no. 2, pp. 270–283, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. S. S. Tanaka, Y. Kojima, Y. L. Yamaguchi, R. Nishinakamura, and P. P. L. Tam, “Impact of WNT signaling on tissue lineage differentiation in the early mouse embryo,” Development Growth and Differentiation, vol. 53, no. 7, pp. 843–856, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. P. P. Tam, D. A. Loebel, and S. S. Tanaka, “Building the mouse gastrula: signals, asymmetry and lineages,” Current Opinion in Genetics and Development, vol. 16, no. 4, pp. 419–425, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. B. Ciruna and J. Rossant, “FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak,” Developmental Cell, vol. 1, no. 1, pp. 37–49, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. P. P. L. Tam, P. Khoo, S. L. Lewis et al., “Seqeuential allocation and global pattern of movement of the definitive endoderm in the mouse embryo during gastrulation,” Development, vol. 134, no. 2, pp. 251–260, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. R. Osorno, A. Tsakiridis, F. Wong et al., “The developmental dismantling of pluripotency is reversed by ectopic Oct4 expression,” Development, vol. 139, no. 13, pp. 2288–2298, 2012. View at Publisher · View at Google Scholar
  82. Y. Kojima, K. Kaufman-Francis, J. B. Studdert et al., “The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak,” Cell Stem Cell, 2013. View at Publisher · View at Google Scholar
  83. K. A. Ewen and P. Koopman, “Mouse germ cell development: from specification to sex determination,” Molecular and Cellular Endocrinology, vol. 323, no. 1, pp. 76–93, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. W. S. Chen, K. Manova, D. C. Weinstein et al., “Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos,” Genes and Development, vol. 8, no. 20, pp. 2466–2477, 1994. View at Google Scholar · View at Scopus
  85. D. D. Spyropoulos and M. R. Capecchi, “Targeted disruption of the even-skipped gene, evx1, causes early postimplantation lethality of the mouse conceptus,” Genes and Development, vol. 8, no. 16, pp. 1949–1961, 1994. View at Google Scholar · View at Scopus
  86. M. Sugimoto, M. Kondo, M. Hirose et al., “Molecular identification of tw5: Vps52 promotes pluripotential cell differentiation through cell-cell interactions,” Cell Reports, vol. 2, no. 5, pp. 1363–1374, 2012. View at Publisher · View at Google Scholar
  87. L. C. Stevens, “The development of transplantable teratocarcinomas from intratesticular grafts of pre- and postimplantation mouse embryos,” Developmental Biology, vol. 21, no. 3, pp. 364–382, 1970. View at Google Scholar · View at Scopus
  88. D. Solter, N. Škreb, and I. Damjanov, “Extrauterine growth of mouse egg-cylinders results in malignant teratoma,” Nature, vol. 227, no. 5257, pp. 503–504, 1970. View at Publisher · View at Google Scholar · View at Scopus
  89. R. L. Gardner, “Mouse chimaeras obtained by the injection of cells into the blastocyst,” Nature, vol. 220, no. 5167, pp. 596–597, 1968. View at Publisher · View at Google Scholar · View at Scopus
  90. M. J. Evans and M. H. Kaufman, “Establishment in culture of pluripotential cells from mouse embryos,” Nature, vol. 292, no. 5819, pp. 154–156, 1981. View at Google Scholar · View at Scopus
  91. G. R. Martin, “Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, no. 12, pp. 7634–7638, 1981. View at Google Scholar · View at Scopus
  92. B. Ledermann and K. Burki, “Establishment of a germ-line competent C57BL/6 embryonic stem cell line,” Experimental Cell Research, vol. 197, no. 2, pp. 254–258, 1991. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Kawase, H. Suemori, N. Takahashi, K. Okazaki, K. Hashimoto, and N. Nakatsuji, “Strain difference in establishment of mouse embryonic stem (ES) cell lines,” International Journal of Developmental Biology, vol. 38, no. 2, pp. 385–390, 1994. View at Google Scholar · View at Scopus
  94. J. McWhir, A. E. Schnieke, R. Ansell et al., “Selective ablation of differentiated cells permits isolation of embryonic stem cell lines from murine embryos with a non-permissive genetic background,” Nature Genetics, vol. 14, no. 2, pp. 223–226, 1996. View at Publisher · View at Google Scholar · View at Scopus
  95. H. R. Eistetter, “Pluripotent embryonal stem cell lines can be established from disaggregated mouse morulae,” Development Growth and Differentiation, vol. 31, no. 3, pp. 275–282, 1989. View at Google Scholar · View at Scopus
  96. Y. Matsui, K. Zsebo, and B. L. M. Hogan, “Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture,” Cell, vol. 70, no. 5, pp. 841–847, 1992. View at Publisher · View at Google Scholar · View at Scopus
  97. J. L. Resnick, L. S. Bixler, L. Cheng, and P. J. Donovan, “Long-term proliferation of mouse primordial germ cells in culture,” Nature, vol. 359, no. 6395, pp. 550–551, 1992. View at Publisher · View at Google Scholar · View at Scopus
  98. A. G. Smith and M. L. Hooper, “Buffalo rat liver cells produce a diffusible activity which inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells,” Developmental Biology, vol. 121, no. 1, pp. 1–9, 1987. View at Google Scholar · View at Scopus
  99. A. G. Smith, J. K. Heath, D. D. Donaldson et al., “Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides,” Nature, vol. 336, no. 6200, pp. 688–690, 1988. View at Google Scholar · View at Scopus
  100. R. L. Williams, D. J. Hilton, S. Pease et al., “Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells,” Nature, vol. 336, no. 6200, pp. 684–687, 1988. View at Google Scholar · View at Scopus
  101. H. Niwa, T. Burdon, I. Chambers, and A. Smith, “Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3,” Genes and Development, vol. 12, no. 13, pp. 2048–2060, 1998. View at Google Scholar · View at Scopus
  102. T. Matsuda, T. Nakamura, K. Nakao et al., “STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells,” EMBO Journal, vol. 18, no. 15, pp. 4261–4269, 1999. View at Publisher · View at Google Scholar · View at Scopus
  103. G. Martello, P. Bertone, and A. Smith, “Identification of the missing pluripotency mediator downstream of leukaemia inhibitory factor,” The EMBO Journal, vol. 32, no. 19, pp. 2561–2574, 2013. View at Publisher · View at Google Scholar
  104. S. Ye, P. Li, C. Tong, and Q.-L. Ying, “Embryonic stem cell self-renewal pathways converge on the transcription factor Tfcp2l1,” The EMBO Journal, vol. 32, no. 19, pp. 2548–2560, 2013. View at Publisher · View at Google Scholar
  105. Q. Ying, J. Nichols, I. Chambers, and A. Smith, “BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3,” Cell, vol. 115, no. 3, pp. 281–292, 2003. View at Publisher · View at Google Scholar · View at Scopus
  106. D. P. Gearing and A. G. Bruce, “Oncostatin M binds the high-affinity leukemia inhibitory factor receptor,” New Biologist, vol. 4, no. 1, pp. 61–65, 1992. View at Google Scholar · View at Scopus
  107. J. C. Conover, N. Y. Ip, W. T. Poueymirou et al., “Ciliary neurotrophic factor maintains the pluripotentiality of embryonic stem cells,” Development, vol. 119, no. 3, pp. 559–565, 1993. View at Google Scholar · View at Scopus
  108. D. Pennica, K. J. Shaw, T. A. Swanson et al., “Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex,” Journal of Biological Chemistry, vol. 270, no. 18, pp. 10915–10922, 1995. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Nichols, I. Chambers, and A. Smith, “Derivation of germline competent embryonic stem cells with a combination of interleukin-6 and soluble interleukin-6 receptor,” Experimental Cell Research, vol. 215, no. 1, pp. 237–239, 1994. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Nichols, D. Davidson, T. Taga, K. Yoshida, I. Chambers, and A. Smith, “Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis,” Mechanisms of Development, vol. 57, no. 2, pp. 123–131, 1996. View at Publisher · View at Google Scholar · View at Scopus
  111. J.-L. Escary, J. Perreau, D. Dumenil, S. Ezine, and P. Brulet, “Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation,” Nature, vol. 363, no. 6427, pp. 361–364, 1993. View at Publisher · View at Google Scholar · View at Scopus
  112. M. Li, M. Sendtner, and A. Smith, “Essential function of LIF receptor in motor neurons,” Nature, vol. 378, no. 6558, pp. 724–727, 1995. View at Publisher · View at Google Scholar · View at Scopus
  113. K. Yoshida, T. Taga, M. Saito et al., “Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 1, pp. 407–411, 1996. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Kawasaki, Y. Gao, S. Yokose et al., “Osteoclasts are present in gp130-deficient mice,” Endocrinology, vol. 138, no. 11, pp. 4959–4965, 1997. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Takeda, K. Noguchi, W. Shi et al., “Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 8, pp. 3801–3804, 1997. View at Publisher · View at Google Scholar · View at Scopus
  116. J. Nichols, I. Chambers, T. Taga, and A. Smith, “Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines,” Development, vol. 128, no. 12, pp. 2333–2339, 2001. View at Google Scholar · View at Scopus
  117. G. R. Martin, “Teratocarcinomas and mammalian embryogenesis,” Science, vol. 209, no. 4458, pp. 768–776, 1980. View at Google Scholar · View at Scopus
  118. K. R. Thomas and M. R. Capecchi, “Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells,” Cell, vol. 51, no. 3, pp. 503–512, 1987. View at Google Scholar · View at Scopus
  119. E. Robertson, A. Bradley, M. Kuehn, and M. Evans, “Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector,” Nature, vol. 323, no. 6087, pp. 445–448, 1986. View at Google Scholar · View at Scopus
  120. A. Bradley, M. Evans, M. H. Kaufman, and E. Robertson, “Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines,” Nature, vol. 309, no. 5965, pp. 255–256, 1984. View at Google Scholar · View at Scopus
  121. C. L. Stewart, “Formation of viable chimaeras by aggregation between teratocarcinomas and preimplantation mouse embryos,” Journal of Embryology and Experimental Morphology, vol. 67, pp. 167–179, 1982. View at Google Scholar · View at Scopus
  122. M. J. Dewey, D. W. Martin Jr., G. R. Martin, and B. Mintz, “Mosaic mice with teratocarcinoma-derived mutant cells deficient in hypoxanthine phosphoribosyltransferase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 12, pp. 5564–5568, 1977. View at Google Scholar · View at Scopus
  123. G. Chapman, J. L. Remiszewski, G. C. Webb, T. C. Schulz, C. D. K. Bottema, and P. D. Rathjen, “The mouse homeobox gene, Gbx2: genomic organization and expression in pluripotent cells in vitro and in vivo,” Genomics, vol. 46, no. 2, pp. 223–233, 1997. View at Publisher · View at Google Scholar · View at Scopus
  124. H. Niwa, J. Miyazaki, and A. G. Smith, “Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells,” Nature Genetics, vol. 24, no. 4, pp. 372–376, 2000. View at Publisher · View at Google Scholar · View at Scopus
  125. S. Masui, Y. Nakatake, Y. Toyooka et al., “Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells,” Nature Cell Biology, vol. 9, no. 6, pp. 625–635, 2007. View at Publisher · View at Google Scholar · View at Scopus
  126. N. Ivanova, R. Dobrin, R. Lu et al., “Dissecting self-renewal in stem cells with RNA interference,” Nature, vol. 442, no. 7102, pp. 533–538, 2006. View at Publisher · View at Google Scholar · View at Scopus
  127. I. Chambers, J. Silva, D. Colby et al., “Nanog safeguards pluripotency and mediates germline development,” Nature, vol. 450, no. 7173, pp. 1230–1234, 2007. View at Publisher · View at Google Scholar · View at Scopus
  128. Y. Toyooka, D. Shimosato, K. Murakami, K. Takahashi, and H. Niwa, “Identification and characterization of subpopulations in undifferentiated ES cell culture,” Development, vol. 135, no. 5, pp. 909–918, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. K. Hayashi, S. M. C. D. S. Lopes, F. Tang, and M. A. Surani, “Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states,” Cell Stem Cell, vol. 3, no. 4, pp. 391–401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. T. Furusawa, K. Ohkoshi, C. Honda, S. Takahashi, and T. Tokunaga, “Embryonic stem cells expressing both platelet endothelial cell adhesion molecule-1 and stage-specific embryonic antigen-1 differentiate predominantly into epiblast cells in a chimeric embryo,” Biology of Reproduction, vol. 70, no. 5, pp. 1452–1457, 2004. View at Publisher · View at Google Scholar · View at Scopus
  131. D. Acampora, L. G. Di Giovannantonio, and A. Simeone, “Otx2 is an intrinsic determinant of the embryonic stem cell state and is required for transition to a stable epiblast stem cell condition,” Development, vol. 140, no. 1, pp. 43–55, 2013. View at Publisher · View at Google Scholar
  132. J. Silva and A. Smith, “Capturing pluripotency,” Cell, vol. 132, no. 4, pp. 532–536, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. B. D. MacArthur, A. Ana, M. Lenz et al., “Nanog-dependent feedback loops regulate murine embryonic stem cell heterogeneity,” Nature Cell Biology, vol. 14, no. 11, pp. 1139–1147, 2012. View at Publisher · View at Google Scholar
  134. A. Smith, “Nanog heterogeneity: tilting at windmills?” Cell Stem Cell, vol. 13, no. 1, pp. 6–7, 2013. View at Publisher · View at Google Scholar
  135. J. Rathjen, J. M. Washington, M. D. Bettess, and P. D. Rathjen, “Identification of a biological activity that supports maintenance and proliferation of pluripotent cells from the primitive ectoderm of the mouse,” Biology of Reproduction, vol. 69, no. 6, pp. 1863–1871, 2003. View at Publisher · View at Google Scholar · View at Scopus
  136. P. J. Tesar, J. G. Chenoweth, F. A. Brook et al., “New cell lines from mouse epiblast share defining features with human embryonic stem cells,” Nature, vol. 448, no. 7150, pp. 196–199, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. I. G. M. Brons, L. E. Smithers, M. W. B. Trotter et al., “Derivation of pluripotent epiblast stem cells from mammalian embryos,” Nature, vol. 448, no. 7150, pp. 191–195, 2007. View at Publisher · View at Google Scholar · View at Scopus
  138. F. J. Najm, J. G. Chenoweth, P. D. Anderson et al., “Isolation of epiblast stem cells from preimplantation mouse embryos,” Cell Stem Cell, vol. 8, no. 3, pp. 318–325, 2011. View at Publisher · View at Google Scholar · View at Scopus
  139. G. M. Beattie, A. D. Lopez, N. Bucay et al., “Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers,” Stem Cells, vol. 23, no. 4, pp. 489–495, 2005. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Amit, M. K. Carpenter, M. S. Inokuma et al., “Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture,” Developmental Biology, vol. 227, no. 2, pp. 271–278, 2000. View at Publisher · View at Google Scholar · View at Scopus
  141. T. E. Ludwig, V. Bergendahl, M. E. Levenstein, J. Yu, M. D. Probasco, and J. A. Thomson, “Feeder-independent culture of human embryonic stem cells,” Nature Methods, vol. 3, no. 8, pp. 637–646, 2006. View at Publisher · View at Google Scholar · View at Scopus
  142. M. Sakaki-Yumoto, J. Liu, M. Ramalho-Santos, N. Yoshida, and R. Derynck, “Smad2 is essential for maintenance of the human and mouse primed pluripotent stem cell state,” Journal of Biological Chemistry, vol. 288, no. 25, pp. 18546–18560, 2013. View at Publisher · View at Google Scholar
  143. J. Rathjen, J. Lake, M. D. Bettess, J. M. Washington, G. Chapman, and P. D. Rathjen, “Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors,” Journal of Cell Science, vol. 112, no. 5, pp. 601–612, 1999. View at Google Scholar · View at Scopus
  144. R. L. Gardner, M. F. Lyon, E. P. Evans, and M. D. Burtenshaw, “Clonal analysis of X-chromosome inactivation and the origin of the germ line in the mouse embryo,” Journal of Embryology and Experimental Morphology, vol. 88, pp. 349–363, 1985. View at Google Scholar · View at Scopus
  145. K. A. Lawson, J. J. Meneses, and R. A. Pedersen, “Clonal analysis of epiblast fate during germ layer formation in the mouse embryo,” Development, vol. 113, no. 3, pp. 891–911, 1991. View at Google Scholar · View at Scopus
  146. E. Tzouanacou, A. Wegener, F. J. Wymeersch, V. Wilson, and J. Nicolas, “Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis,” Developmental Cell, vol. 17, no. 3, pp. 365–376, 2009. View at Publisher · View at Google Scholar · View at Scopus
  147. J. Rathjen, B. P. Haines, K. M. Hudson, A. Nesci, S. Dunn, and P. D. Rathjen, “Directed differentiation of pluripotent cells to neural lineages: homogeneous formation and differentiation of a neurectoderm population,” Development, vol. 129, no. 11, pp. 2649–2661, 2002. View at Google Scholar · View at Scopus
  148. J. Lake, J. Rathjen, J. Remiszewski, and P. D. Rathjen, “Reversible programming of pluripotent cell differentiation,” Journal of Cell Science, vol. 113, no. 3, pp. 555–566, 2000. View at Google Scholar · View at Scopus
  149. S. Vassilieva, H. N. Goh, K. X. Lau et al., “A system to enrich for primitive streak-derivatives, definitive endoderm and mesoderm, from pluripotent cells in culture,” PLoS ONE, vol. 7, no. 6, Article ID e38645, 2012. View at Google Scholar
  150. D. W. Han, N. Tapia, J. Y. Joo et al., “Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages,” Cell, vol. 143, no. 4, pp. 617–627, 2010. View at Publisher · View at Google Scholar · View at Scopus
  151. S. Ohtsuka, S. Nishikawa-Torikai, and H. Niwa, “E-cadherin promotes incorporation of mouse epiblast stem cells into normal development,” PLoS ONE, vol. 7, no. 9, Article ID e45220, 2012. View at Google Scholar
  152. Y. Huang, R. Osorno, A. Tsakiridis, and V. Wilson, “In Vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation,” Cell Reports, vol. 2, no. 6, pp. 1571–1578, 2012. View at Publisher · View at Google Scholar
  153. J. G. Chenoweth, R. D. G. McKay, and P. J. Tesar, “Epiblast stem cells contribute new insight into pluripotency and gastrulation,” Development Growth and Differentiation, vol. 52, no. 3, pp. 293–301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  154. J. Nichols and A. Smith, “Naive and primed pluripotent states,” Cell Stem Cell, vol. 4, no. 6, pp. 487–492, 2009. View at Publisher · View at Google Scholar · View at Scopus
  155. G. Guo, J. Yang, J. Nichols et al., “Klf4 reverts developmentally programmed restriction of ground state pluripotency,” Development, vol. 136, no. 7, pp. 1063–1069, 2009. View at Publisher · View at Google Scholar · View at Scopus
  156. I. Hiratani, T. Ryba, M. Itoh et al., “Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis,” Genome Research, vol. 20, no. 2, pp. 155–169, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. W. Zhou, M. Choi, D. Margineantu et al., “HIF1α induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition,” EMBO Journal, vol. 31, no. 9, pp. 2103–2116, 2012. View at Publisher · View at Google Scholar · View at Scopus
  158. S. Bao, F. Tang, X. Li et al., “Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells,” Nature, vol. 461, no. 7268, pp. 1292–1295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  159. C. Bernemann, B. Greber, K. Ko et al., “Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features,” Stem Cells, vol. 29, no. 10, pp. 1496–1503, 2011. View at Publisher · View at Google Scholar · View at Scopus
  160. Q. Ying, J. Wray, J. Nichols et al., “The ground state of embryonic stem cell self-renewal,” Nature, vol. 453, no. 7194, pp. 519–523, 2008. View at Publisher · View at Google Scholar · View at Scopus
  161. J. Silva, O. Barrandon, J. Nichols, J. Kawaguchi, T. W. Theunissen, and A. Smith, “Promotion of reprogramming to ground state pluripotency by signal inhibition,” PLoS Biology, vol. 6, no. 10, p. e253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  162. J. Nichols, K. Jones, J. M. Phillips et al., “Validated germline-competent embryonic stem cell lines from nonobese diabetic mice,” Nature Medicine, vol. 15, no. 7, pp. 814–818, 2009. View at Publisher · View at Google Scholar · View at Scopus
  163. M. Buehr, S. Meek, K. Blair et al., “Capture of authentic embryonic stem cells from rat blastocysts,” Cell, vol. 135, no. 7, pp. 1287–1298, 2008. View at Publisher · View at Google Scholar · View at Scopus
  164. F. Faunes, P. Hayward, S. M. Descalzo et al., “A membrane-associated beta-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells,” Development, vol. 140, no. 6, pp. 1171–1183, 2013. View at Publisher · View at Google Scholar
  165. T. Shimizu, J. Ueda, J. C. Ho et al., “Dual inhibition of Src and GSK3 maintains mouse embryonic stem cells, whose differentiation is mechanically regulated by Src signaling,” Stem Cells, vol. 30, no. 7, pp. 1394–1404, 2012. View at Publisher · View at Google Scholar
  166. X. Li, L. Zhu, A. Yang et al., “Calcineurin-NFAT signaling critically regulates early lineage specification in mouse embryonic stem cells and embryos,” Cell Stem Cell, vol. 8, no. 1, pp. 46–58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  167. M. A. Meyn III and T. E. Smithgall, “Chemical genetics identifies c-Src as an activator of primitive ectoderm formation in murine embryonic stem cells,” Science Signaling, vol. 2, no. 92, p. ra64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  168. M. A. Meyn III, S. J. Schreiner, T. P. Dumitrescu, G. J. Nau, and T. E. Smithgall, “Src family kinase activity is required for murine embryonic stem cell growth and differentiation,” Molecular Pharmacology, vol. 68, no. 5, pp. 1320–1330, 2005. View at Publisher · View at Google Scholar · View at Scopus
  169. P. D. Rathjen, J. Lake, L. M. Whyatt, M. D. Bettess, and J. Rathjen, “Properties and uses of embryonic stem cells: prospects for application to human biology and gene therapy,” Reproduction, Fertility and Development, vol. 10, no. 1, pp. 31–47, 1998. View at Google Scholar · View at Scopus
  170. R. G. Edwards, “Human embryo as a source of cells,” Bone Marrow Transplantation, vol. 9, supplement 1, pp. 90–92, 1992. View at Google Scholar · View at Scopus
  171. N. T. Harvey, J. N. Hughes, A. Lonic et al., “Response to BMP4 signalling during ES cell differentiation defines intermediates of the ectoderm lineage,” Journal of Cell Science, vol. 123, no. 10, pp. 1796–1804, 2010. View at Publisher · View at Google Scholar · View at Scopus
  172. J. N. Hughes, N. Dodge, P. D. Rathjen, and J. Rathjen, “A novel role for γ-secretase in the formation of primitive streak-like intermediates from ES cells in culture,” Stem Cells, vol. 27, no. 12, pp. 2941–2951, 2009. View at Publisher · View at Google Scholar · View at Scopus
  173. M. F. Pera and P. P. L. Tam, “Extrinsic regulation of pluripotent stem cells,” Nature, vol. 465, no. 7299, pp. 713–720, 2010. View at Publisher · View at Google Scholar · View at Scopus
  174. B. V. Johnson, N. Shindo, P. D. Rathjen, J. Rathjen, and R. A. Keough, “Understanding pluripotency—how embryonic stem cells keep their options open,” Molecular Human Reproduction, vol. 14, no. 9, pp. 513–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  175. T. Kunath, M. K. Saba-El-Leil, M. Almousailleakh, J. Wray, S. Meloche, and A. Smith, “FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment,” Development, vol. 134, no. 16, pp. 2895–2902, 2007. View at Publisher · View at Google Scholar · View at Scopus
  176. J. M. Washington, J. Rathjen, F. Felquer et al., “L-proline induces differentiation of ES cells: a novel role for an amino acid in the regulation of pluripotent cells in culture,” American Journal of Physiology, vol. 298, no. 5, pp. C982–C992, 2010. View at Publisher · View at Google Scholar · View at Scopus
  177. B. S. N. Tan, A. Lonic, M. B. Morris, P. D. Rathjen, and J. Rathjen, “The amino acid transporter SNAT2 mediates l-proline-induced differentiation of ES cells,” American Journal of Physiology, vol. 300, no. 6, pp. C1270–C1279, 2011. View at Publisher · View at Google Scholar · View at Scopus
  178. L. Casalino, S. Comes, G. Lambazzi et al., “Control of embryonic stem cell metastability by L-proline catabolism,” Journal of Molecular Cell Biology, vol. 3, no. 2, pp. 108–122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  179. T. C. Doetschman, H. Eistetter, and M. Katz, “The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium,” Journal of Embryology and Experimental Morphology, vol. 87, pp. 27–45, 1985. View at Google Scholar · View at Scopus
  180. C. Coffinier, D. Thépot, C. Babinet, M. Yaniv, and J. Barra, “Essential role for the homeoprotein vHNF1/HNF1β in visceral endoderm differentiation,” Development, vol. 126, no. 21, pp. 4785–4794, 1999. View at Google Scholar · View at Scopus
  181. E. Coucouvanis and G. R. Martin, “BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo,” Development, vol. 126, no. 3, pp. 535–546, 1999. View at Google Scholar · View at Scopus
  182. E. Barbacci, M. Reber, M. Ott, C. Breillat, F. Huetz, and S. Cereghini, “Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification,” Development, vol. 126, no. 21, pp. 4795–4805, 1999. View at Google Scholar · View at Scopus
  183. A. Bruhat, C. Jousse, V. Carraro, A. M. Reimold, M. Ferrara, and P. Fafournoux, “Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter,” Molecular and Cellular Biology, vol. 20, no. 19, pp. 7192–7204, 2000. View at Publisher · View at Google Scholar · View at Scopus
  184. E. Kim, “Mechanisms of amino acid sensing in mTOR signaling pathway,” Nutrition Research and Practice, vol. 3, no. 1, pp. 64–71, 2009. View at Publisher · View at Google Scholar
  185. S. P. Donald, X.-Y. Sun, C.-A. A. Hu et al., “Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species,” Cancer Research, vol. 61, no. 5, pp. 1810–1815, 2001. View at Google Scholar · View at Scopus
  186. Y. Liu, G. L. Borchert, A. Surazynski, C.-A. Hu, and J. M. Phang, “Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: the role of ROS/superoxides, NFAT and MEK/ERK signaling,” Oncogene, vol. 25, no. 41, pp. 5640–5647, 2006. View at Publisher · View at Google Scholar · View at Scopus
  187. E. Giannoni, F. Buricchi, G. Raugei, G. Ramponi, and P. Chiarugi, “Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth,” Molecular and Cellular Biology, vol. 25, no. 15, pp. 6391–6403, 2005. View at Publisher · View at Google Scholar · View at Scopus
  188. H. Marks, T. Kalkan, R. Menafra et al., “The transcriptional and epigenomic foundations of ground state pluripotency,” Cell, vol. 149, no. 3, pp. 590–604, 2012. View at Publisher · View at Google Scholar · View at Scopus
  189. W. B. Hamilton, K. Kaji, and T. Kunath, “ERK2 suppresses self-renewal capacity of embryonic stem cells, but is not required for multi-lineage commitment,” PLoS ONE, vol. 8, no. 4, Article ID e60907, 2013. View at Google Scholar
  190. Y. Miyanari and M. Torres-Padilla, “Control of ground-state pluripotency by allelic regulation of Nanog,” Nature, vol. 483, no. 7390, pp. 470–473, 2012. View at Publisher · View at Google Scholar · View at Scopus
  191. E. Habibi, A. B. Brinkman, J. Arand et al., “Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells,” Cell Stem Cell, vol. 13, no. 3, pp. 360–369, 2013. View at Publisher · View at Google Scholar
  192. J. N. Hughes, J. M. Washington, Z. Zheng et al., “Manipulation of cell: cell contacts and mesoderm suppressing activity direct lineage choice from pluripotent primitive ectoderm-like cells in culture,” PLoS ONE, vol. 4, no. 5, Article ID e5579, 2009. View at Publisher · View at Google Scholar · View at Scopus
  193. A. G. Smith, “Mouse embryo stem cells: their identification, propagation and manipulation,” Seminars in Cell and Developmental Biology, vol. 3, no. 6, pp. 385–399, 1992. View at Google Scholar · View at Scopus
  194. M. M. Shen and P. Leder, “Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 17, pp. 8240–8244, 1992. View at Google Scholar · View at Scopus
  195. Z. Zheng, R. U. de Iongh, P. D. Rathjen, and J. Rathjen, “A requirement for FGF signalling in the formation of primitive streak-like intermediates from primitive ectoderm in culture,” PloS ONE, vol. 5, no. 9, Article ID e12555, 2010. View at Google Scholar · View at Scopus
  196. B. E. Reubinoff, M. F. Pera, C. Fong, A. Trounson, and A. Bongso, “Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro,” Nature Biotechnology, vol. 18, no. 4, pp. 399–404, 2000. View at Publisher · View at Google Scholar · View at Scopus
  197. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar · View at Scopus
  198. K. Watanabe, M. Ueno, D. Kamiya et al., “A ROCK inhibitor permits survival of dissociated human embryonic stem cells,” Nature Biotechnology, vol. 25, no. 6, pp. 681–686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  199. G. Chen, D. R. Gulbranson, Z. Hou et al., “Chemically defined conditions for human iPSC derivation and culture,” Nature Methods, vol. 8, no. 5, pp. 424–429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  200. R. C. B. Wong, M. F. Pera, and A. Pébay, “Maintenance of human embryonic stem cells by sphingosine-1-phosphate and platelet-derived growth factor,” Methods in Molecular Biology, vol. 874, pp. 167–175, 2012. View at Publisher · View at Google Scholar · View at Scopus
  201. K. Hasegawa, S. Y. Yasuda, J.-L. Teo et al., “Wnt signaling orchestration with a small molecule DYRK inhibitor provides long-term xeno-free human pluripotent cell expansion,” Stem Cells Translational Medicine, vol. 1, no. 1, pp. 18–28, 2012. View at Publisher · View at Google Scholar
  202. R. Xu, X. Chen, D. S. Li et al., “BMP4 initiates human embryonic stem cell differentiation to trophoblast,” Nature Biotechnology, vol. 20, no. 12, pp. 1261–1264, 2002. View at Publisher · View at Google Scholar · View at Scopus
  203. A. S. Bernardo, T. Faial, L. Gardner et al., “BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages,” Cell Stem Cell, vol. 9, no. 2, pp. 144–155, 2011. View at Publisher · View at Google Scholar · View at Scopus
  204. C. Buecker, H. Chen, J. M. Polo et al., “A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells,” Cell Stem Cell, vol. 6, no. 6, pp. 535–546, 2010. View at Publisher · View at Google Scholar · View at Scopus
  205. J. Hanna, A. W. Cheng, K. Saha et al., “Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 20, pp. 9222–9227, 2010. View at Publisher · View at Google Scholar · View at Scopus
  206. C. J. Lengner, A. A. Gimelbrant, J. A. Erwin et al., “Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations,” Cell, vol. 141, no. 5, pp. 872–883, 2010. View at Publisher · View at Google Scholar · View at Scopus
  207. Q. Gu, J. Hao, X.-Y. Zhao et al., “Rapid conversion of human ESCs into mouse ESC-like pluripotent state by optimizing culture conditions,” Protein & Cell, vol. 3, no. 1, pp. 71–79, 2012. View at Publisher · View at Google Scholar
  208. O. Gafni, L. Weinberger, A. A. Mansour et al., “Derivation of novel human ground state naive pluripotent stem cells,” Nature, vol. 504, no. 7479, pp. 282–286, 2013. View at Google Scholar
  209. T. O'Leary, B. Heindryckx, S. Lierman et al., “Tracking the progression of the human inner cell mass during embryonic stem cell derivation,” Nature Biotechnology, vol. 30, no. 3, pp. 278–282, 2012. View at Publisher · View at Google Scholar · View at Scopus
  210. T. Ezashi, B. P. Telugu, and R. M. Roberts, “Model systems for studying trophoblast differentiation from human pluripotent stem cells,” Cell and Tissue Research, vol. 349, no. 3, pp. 809–824, 2012. View at Publisher · View at Google Scholar
  211. M. B. Renfree and G. Shaw, “Diapause,” Annual Review of Physiology, vol. 62, pp. 353–375, 2000. View at Publisher · View at Google Scholar · View at Scopus
  212. S. R. Hough, A. L. Laslett, S. B. Grimmond, G. Kolle, and M. F. Pera, “A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells,” PLoS ONE, vol. 4, no. 11, Article ID e7708, 2009. View at Publisher · View at Google Scholar · View at Scopus
  213. M. F. Pera, “Defining pluripotency,” Nature Methods, vol. 7, no. 11, pp. 885–886, 2010. View at Publisher · View at Google Scholar · View at Scopus
  214. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus