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Pluripotency Dynamics during Embryogenesis and in Cell Culture

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Abstract

The early embryonic development of mice and humans is characterized by the presence of pluripotent cells, which give rise to all tissues of the developing embryo. About 40 years ago, these cells were isolated and maintained in culture in a stable pluripotent state. Since then, a plethora of data regarding the mechanisms underlying the functioning of these cells, key genes necessary for their work, as well as their differentiation into various cell types. Nowadays, depending on the stage of embryogenesis, multiple types of pluripotent stem cells can be distinguished, and these types fundamentally differ from each other in signaling, culture condition dependendence, and differentiation abilities. This review summarizes currently available information on the dynamics of pluripotency during embryogenesis as well as in cultured pluripotent cells.

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REFERENCES

  1. Azami, T., Matsumoto, K., Jeon, H., et al., Klf5 suppresses ERK signaling in mouse pluripotent stem cells, PLoS One, 2018, vol. 13, no. 11, art. e0207321.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Barral, A., Rollan, I., Sanchez-Iranzo, H., et al., Nanog regulates Pou3f1 expression at the exit from pluripotency during gastrulation, Biol. Open, 2019, vol. 8, no. 11, art. bio046367.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bayerl, J., Ayyash, M., Shani, T., et al., Principles of signaling pathway modulation for enhancing human naive pluripotency induction, Cell Stem Cell, 2021, vol. 28, pp. 1–17.

    Article  Google Scholar 

  4. Bedzhov, I., Bialecka, M., Zielinska, A., et al., Development of the anterior-posterior axis is a self-organizing process in the absence of maternal cues in the mouse embryo, Cell Res., 2015, vol. 25, no. 12, pp. 1368–1371.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ben-Haim, N., Lu, C., Guzman-Ayala, M., et al., The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4, Dev. Cell, 2006, vol. 11, no. 3, pp. 313–323.

    Article  CAS  PubMed  Google Scholar 

  6. Bessonnard, S., De Mot, L., Gonze, D., et al., Gata6, Nanog and Erk signaling control cell fate in the inner cell mass through a tristable regulatory network, Development, 2014, vol. 141, no. 19, pp. 3637–3648.

    Article  CAS  PubMed  Google Scholar 

  7. Blanco, E., González-Ramírez, M., Alcaine-Colet, A., et al., The bivalent genome: characterization, structure, and regulation, Trends Genet., 2020, vol. 36, no. 2, pp. 118–131.

    Article  CAS  PubMed  Google Scholar 

  8. Boroviak, T., Loos, R., Bertone, P., et al., The ability of inner-cell-mass cells to self-renew as embryonic stem cells is acquired following epiblast specification, Nat. Cell Biol., 2014, vol. 16, no. 6, pp. 513–525.

    Article  Google Scholar 

  9. Brons, I.G.M., Smithers, L.E., Trotter, M.W.B., et al., Derivation of pluripotent epiblast stem cells from mammalian embryos, Nature, 2007, vol. 448, no. 7150, pp. 191–195.

    Article  CAS  PubMed  Google Scholar 

  10. Buecker, C., Srinivasan, R., Wu, Z., et al., Reorganization of enhancer patterns in transition from naive to primed pluripotency, Cell Stem Cell, 2014, vol. 14, no. 6, pp. 838–853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cajal, M., Lawson, K.A., Hill, B., et al., Clonal and molecular analysis of the prospective anterior neural boundary in the mouse embryo, Development, 2012, vol. 139, no. 2, pp. 423–436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chambers, I., Colby, D., Robertson, M., et al., Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells, Cell, 2003, vol. 113, no. 5, pp. 643–655.

    Article  CAS  PubMed  Google Scholar 

  13. Chambers, I., Silva, J., Colby, D., et al., Nanog safeguards pluripotency and mediates germline development, Nature, 2007, vol. 450, no. 7173, pp. 1230–1234.

    Article  CAS  PubMed  Google Scholar 

  14. Chan, Y.S., Göke, J., Ng, J.H., et al., Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast, Cell Stem Cell, 2013, vol. 13, no. 6, pp. 663–675.

    Article  CAS  PubMed  Google Scholar 

  15. Chhabra, S., Liu, L., Goh, R., et al., Dissecting the dynamics of signaling events in the BMP, WNT, and NODAL cascade during self-organized fate patterning in human gastruloids, PLoS Biol., 2019, vol. 17, no. 10, art. e3000498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Choi, H. W., Joo, J.Y., Hong, Y.J., et al., Distinct enhancer activity of Oct4 in naive and primed mouse pluripotency, Stem Cell Rep., 2016, vol. 7, no. 5, pp. 911–926.

    Article  CAS  Google Scholar 

  17. Costello, I., Pimeisl, I.M., Dräger, S., et al., The T-box transcription factor eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation, Nat. Cell Biol., 2011, vol. 13, no. 9, pp. 1084–1091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cruz-Molina, S., Respuela, P., Tebartz, C., et al., Prc2 facilitates the regulatory topology required for poised enhancer function during pluripotent stem cell differentiation, Cell Stem Cell, 2017, vol. 20, no. 5, pp. 689–705.

    Article  CAS  PubMed  Google Scholar 

  19. DeVeale, B., Brokhman, I., Mohseni, P., et al., Oct4 is required ~E7.5 for proliferation in the primitive streak, PLoS Genet., 2013, vol. 9, no. 11.

  20. Evans, M.J. and Kaufman, M.H., Establishment in culture of pluripotential cells from mouse embryos, Nature, 1981, vol. 292, no. 5819, pp. 154–156.

    Article  CAS  PubMed  Google Scholar 

  21. Factor, D.C., Corradin, O., Zentner, G.E., et al., Epigenomic comparison reveals activation of “seed” enhancers during transition from naive to primed pluripotency, Cell Stem Cell, 2014, vol. 14, no. 6, pp. 854–863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ferretti, E. and Hadjantonakis, A.K., Mesoderm specification and diversification: from single cells to emergent tissues, Curr. Opin. Cell Biol., 2019, vol. 61, pp. 110–116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Francou, A. and Anderson, K.V., The epithelial-to-mesenchymal transition in development and cancer, Annu. Rev. Cancer Biol., 2020, vol. 4, pp. 197–220.

    Article  PubMed  Google Scholar 

  24. Grosswendt, S., Kretzmer, H., Smith, Z.D., et al., Epigenetic regulator function through mouse gastrulation, Nature, 2020, vol. 584, no. 7819, pp. 102–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Guo, Q. and Li, J.Y.H., Distinct functions of the major Fgf8 spliceform, before and during mouse gastrulation, Development, 2007, vol. 134, no. 12, pp. 2251–2260.

    Article  CAS  PubMed  Google Scholar 

  26. Guo, G., Pinello, L., Han, X., et al., Serum-based culture conditions provoke gene expression variability in mouse embryonic stem cells as revealed by single-cell analysis, Cell Rep., 2016, vol. 14, no. 4, pp. 956–965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Habibi, E., Brinkman, A.B., Arand, J., et al., Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells, Cell Stem Cell, 2013, vol. 13, no. 3, pp. 360–369.

    Article  CAS  PubMed  Google Scholar 

  28. Hayashi, K., Lopes, S.M.C., Tang, F., et al., Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states, Cell Stem Cell, 2008, vol. 3, no. 4, pp. 391–401.

    Article  CAS  PubMed  Google Scholar 

  29. Hayashi, K., Ohta, H., Kurimoto, K., et al., Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells, Cell, 2011, vol. 146, no. 4, pp. 519–532.

    Article  CAS  PubMed  Google Scholar 

  30. Huang, Y., Osorno, R., Tsakiridis, A., et al., In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation, Cell Rep., 2012, vol. 2, no. 6, pp. 1571–1578.

    Article  CAS  PubMed  Google Scholar 

  31. Ivanova, N., Dobrin, R., Lu, R., et al., Dissecting self-renewal in stem cells with rna interference, Nature, 2006, vol. 442, no. 7102, pp. 533–538.

    Article  CAS  PubMed  Google Scholar 

  32. Kimura-Yoshida, C., Nakano, H., Okamura, D., et al., Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm, Dev. Cell, 2005, vol. 9, no. 5, pp. 639–650.

    Article  CAS  PubMed  Google Scholar 

  33. Kinoshita, M., Barber, M., Mansfield, W., et al., Capture of mouse and human stem cells with features of formative pluripotency, Cell Stem Cell, 2021, vol. 28, no. 3, pp. 453–471.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Koch, F., Scholze, M., Wittler, L., et al., Antagonistic activities of Sox2 and Brachyury control the fate choice of neuro-mesodermal progenitors, Dev. Cell, 2017, vol. 42, no. 5, pp. 514–526.

    Article  CAS  PubMed  Google Scholar 

  35. Kojima, Y., Kaufman-Francis, K., Studdert, J.B., et al., The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak, Cell Stem Cell, 2014, vol. 14, no. 1, pp. 107–120.

    Article  CAS  PubMed  Google Scholar 

  36. Kopp, J.L., Ormsbee, B.D., Desler, M., et al., Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells, Stem Cells, 2008, vol. 26, no. 4, pp. 903–911.

    Article  CAS  PubMed  Google Scholar 

  37. Kwon, G.S., Viotti, M., and Hadjantonakis, A.K., The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages, Dev. Cell, 2008, vol. 15, no. 4, pp. 509–520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu, C., Wang, R., He, Z., et al., Suppressing nodal signaling activity predisposes ectodermal differentiation of epiblast stem cells, Stem Cell Rep., 2018, vol. 11, no. 1, pp. 43–57.

    Article  CAS  Google Scholar 

  39. Malleshaiah, M., Padi, M., Rue, P., et al., Nac1 coordinates a sub-network of pluripotency factors to regulate embryonic stem cell differentiation, Cell Rep., 2016, vol. 14, no. 5, pp. 1181–1194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Martin, G.R., 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., 1981, vol. 78, no. 12, part II, pp. 7634–7638.

  41. Martin Gonzalez, J., Morgani, S.M., Bone, R.A., et al., Embryonic stem cell culture conditions support distinct states associated with different developmental stages and potency, Stem Cell Rep., 2016, vol. 7, no. 2, pp. 177–191.

    Article  CAS  Google Scholar 

  42. Martyn, I., Siggia, E.D., and Brivanlou, A.H., Mapping cell migrations and fates in a gastruloid model to the human primitive streak, Curr. Opin. Cell Biol., 2019, vol. 66, pp. 89–96.

    Google Scholar 

  43. Mas, G., Blanco, E., Ballaré, C., et al., Promoter bivalency favors an open chromatin architecture in embryonic stem cells, Nat. Genet., 2018, vol. 50, no. 10, pp. 1452–1462.

    Article  CAS  PubMed  Google Scholar 

  44. Masui, S., Nakatake, Y., Toyooka, Y., et al., Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells, Nat. Cell Biol., 2007, vol. 9, no. 6, pp. 625–635.

    Article  CAS  PubMed  Google Scholar 

  45. Meyenn, F. von, Iurlaro, M., Habibi, E., et al., Impairment of DNA methylation maintenance is the main cause of global demethylation in naive embryonic stem cells, Mol. Cell, 2016, vol. 62, no. 6, pp. 848–861.

    Article  Google Scholar 

  46. Mittnenzweig, M., Mayshar, Y., Cheng, S., et al., Article a single-embryo, single-cell time-resolved model for mouse gastrulation a single-embryo, single-cell time-resolved model for mouse gastrulation, Cell, 2021, vol. 184, no. 11, pp. 2825–2842. e22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mohammed, H., Hernando-Herraez, I., Savino, A., et al., Single-cell landscape of transcriptional heterogeneity and cell fate decisions during mouse early gastrulation, Cell Rep., 2017, vol. 20, no. 5, pp. 1215–1228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Morgani, S., Nichols, J., and Hadjantonakis, A.K., The many faces of pluripotency: in vitro adaptations of a continuum of in vivo states, BMC Dev. Biol., 2017, vol. 17, no. 1, pp. 1–20.

    Article  Google Scholar 

  49. Morgani, S.M., Metzger, J.J., Nichols, J., et al., Micropattern differentiation of mouse pluripotent stem cells recapitulates embryo regionalized cell fate patterning, Elife, 2018, vol. 7, no. 7, art. e32839.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Mulas, C., Chia, G., Jones, K.A., et al., Oct4 regulates the embryonic axis and coordinates exit from pluripotency and germ layer specification in the mouse embryo, Development, 2018, vol. 145, no. 12, pp. 1–13.

    Article  Google Scholar 

  51. Neagu, A., van Genderen, E., Escudero, I., et al., In vitro capture and characterization of embryonic rosette-stage pluripotency between naive and primed states, Nat. Cell Biol., 2020, vol. 22, no. 5, pp. 534–545.

    Article  CAS  PubMed  Google Scholar 

  52. Niwa, H., Miyazaki, J., and Smith, A.G., Quantitative expression of oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells, Nat. Genet., 2000, vol. 24, no. 4, pp. 372–376.

    Article  CAS  PubMed  Google Scholar 

  53. Niwa, H., Ogawa, K., Shimosato, D., et al., A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells, Nature, 2009, vol. 460, no. 7251, pp. 118–122.

    Article  CAS  PubMed  Google Scholar 

  54. Nowotschin, S., Setty, M., Kuo, Y.Y., et al., The emergent landscape of the mouse gut endoderm at single-cell resolution, Nature, 2019, vol. 569, no. 7756, pp. 361–367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ohinata, Y., Ohta, H., Shigeta, M., et al., A signaling principle for the specification of the germ cell lineage in mice, Cell, 2009, vol. 137, no. 3, pp. 571–584.

    Article  CAS  PubMed  Google Scholar 

  56. Perea-Gomez, A., Vella, F.D.J., Shawlot, W., et al., Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks, Dev. Cell, 2002, vol. 3, no. 5, pp. 745–756.

    Article  CAS  PubMed  Google Scholar 

  57. Pijuan-Sala, B., Griffiths, J.A., Guibentif, C., et al., A single-cell molecular map of mouse gastrulation and early organogenesis, Nature, 2019, vol. 566, no. 7745, pp. 490–495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Radzisheuskaya, A., Chia Gle.B., dos Santos, R.L., et al., A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages, Nat. Cell Biol., 2013, vol. 15, no. 6, pp. 579–590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Rodriguez, T.A., Srinivas, S., Clements, M.P., et al., Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm, Development, 2005, vol. 132, no. 11, pp. 2513–2520.

    Article  CAS  PubMed  Google Scholar 

  60. Saykali, B., Mathiah, N., Nahaboo, W., et al., Distinct mesoderm migration phenotypes in extra-embryonic and embryonic regions of the early mouse embryo, Elife, 2019, vol. 8, art. e42434.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Shahbazi, M.N., Scialdone, A., Skorupska, N., et al., Pluripotent state transitions coordinate morphogenesis in mouse and human embryos, Nature, 2017, vol. 552, pp. 239–243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Smith, A., Formative pluripotency: the executive phase in a developmental continuum, Development, 2017, vol. 144, no. 3, pp. 365–373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sozen, B., Cox, A.L., De Jonghe, J., et al., Self-organization of mouse stem cells into an extended potential blastoid, Dev. Cell, 2019, vol. 51, no. 6, pp. 698–712.

    Article  CAS  PubMed  Google Scholar 

  64. Srinivas, S., Rodriguez, T., Clements, M., et al., Active cell migration drives the unilateral movements of the anterior visceral endoderm, Development, 2004, vol. 131, no. 5, pp. 1157–1164.

    Article  CAS  PubMed  Google Scholar 

  65. Takaoka, K., Yamamoto, M., Shiratori, H., et al., The mouse embryo autonomously acquires anterior-posterior polarity at implantation, Dev. Cell, 2006, vol. 10, no. 4, pp. 451–459.

    Article  CAS  PubMed  Google Scholar 

  66. Tee, W.W., Shen, S.S., Oksuz, O., et al., Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs, Cell, 2014, vol. 156, no. 4, pp. 678–690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Teo, A.K.K., Arnold, S.J., Trotter, M.W.B., et al., Pluripotency factors regulate definitive endoderm specification through eomesodermin, Genes Dev., 2011, vol. 25, no. 3, pp. 238–250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Tesar, P.J., Chenoweth, J.G., Brook, F.A., et al., New cell lines from mouse epiblast share defining features with human embryonic stem cells, Nature, 2007, vol. 448, no. 7150, pp. 196–199.

    Article  CAS  PubMed  Google Scholar 

  69. Theunissen, T.W., Friedli, M., He, Y., et al., Molecular criteria for defining the naive human pluripotent state, Cell Stem Cell, 2016, vol. 19, no. 4, pp. 502–515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., et al., Embryonic stem cell lines derived from human blastocysts, Science, 1998, vol. 282, no. 5391, pp. 1145–1147.

    Article  CAS  PubMed  Google Scholar 

  71. Thomson, M., Liu, S.J., Zou, L.N., et al., Pluripotency factors in embryonic stem cells regulate differentiation into germ layers, Cell, 2011, vol. 14, no. 6, pp. 875–889.

    Article  Google Scholar 

  72. Tortelote, G.G., Hernández-Hernández, J.M., Quaresma, A.J.C., et al., Wnt3 function in the epiblast is required for the maintenance but not the initiation of gastrulation in mice, Dev. Biol., 2013, vol. 374, no. 1, pp. 164–173.

    Article  CAS  PubMed  Google Scholar 

  73. Viotti, M., Nowotschin, S., and Hadjantonakis, A.K., SOX17 links gut endoderm morphogenesis and germ layer segregation, Nat. Cell Biol., 2014, vol. 16, no. 12, pp. 1146–1156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Wang, Z., Oron, E., Nelson, B., et al., Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells, Cell Stem Cell, 2012, vol. 10, no. 4, pp. 440–454.

    Article  CAS  PubMed  Google Scholar 

  75. Wang, R.N., Green, J., Wang, Z., et al., Bone morphogenetic protein (BMP) signaling in development and human diseases, Genes Dis., 2014, vol. 1, no. 1, pp. 87–105.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Wu, J., Okamura, D., Li, M., et al., An alternative pluripotent state confers interspecies chimaeric competency, Nature, 2015, vol. 521, no. 7552, pp. 316–321.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yang, S.H., Kalkan, T., Morissroe, C., et al., Otx2 and Oct4 drive early enhancer activation during embryonic stem cell transition from naive pluripotency, Cell Rep., 2014, vol. 7, no. 6, pp. 1968–1981.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Yang, J., Ryan, D.J., Wang, W., et al., Establishment of mouse expanded potential stem cells, Nature, 2017, vol. 550, no. 7676, pp. 393–397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Yeom, Y.Il., Fuhrmann, G., Ovitt, C.E., et al., Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells, Development, 1996, vol. 122, no. 3, pp. 881–894.

    Article  CAS  PubMed  Google Scholar 

  80. Yi, F., Pereira, L., Hoffman, J.A., et al., Opposing effects of Tcf3 and Tcf1 control wnt stimulation of embryonic stem cell self-renewal, Nat. Cell Biol., 2011, vol. 13, no. 7, pp. 762–770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Ying, Q.L., Wray, J., Nichols, J., et al., The ground state of embryonic stem cell self-renewal, Nature, 2008, vol. 453, no. 7194, pp. 519–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Yu, Y., Wang, X., Zhang, X., et al., ERK inhibition promotes neuroectodermal precursor commitment by blocking self-renewal and primitive streak formation of the epiblast, Stem Cell Res. Ther., 2018, vol. 9, no. 1, p. 2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Yu, L., Wei, Y., Sun, H.X., et al., Derivation of intermediate pluripotent stem cells amenable to primordial germ cell specification, Cell Stem Cell, 2021, vol. 28, no. 3, pp. 550–567. e12.

    Article  CAS  PubMed  Google Scholar 

  84. Zalc, A., Sinha, R., Gulati, G.S., et al., Reactivation of the pluripotency program precedes formation of the cranial neural crest, Science, 2021, vol. 371, no. 6529.

  85. Zhang, M., Leitch, H.G., Tang, W.W.C., et al., Esrrb complementation rescues development of Nanog-null germ cells, Cell Rep., 2018, vol. 22, no. 2, pp. 332–339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Zhang, S., Bell, E., Zhi, H., et al., OCT4 and PAX6 determine the dual function of SOX2 in human ESCs as a key pluripotent or neural factor, Stem Cell Res. Ther., 2019, vol. 10, no. 1, pp. 1–14.

    Article  Google Scholar 

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Funding

The work was performed with the financial support of the grant of the Russian Science Foundation, no. 20-74-00072.

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  1. Institute of Cytology, Russian Academy of Sciences, 194064, St. Petersburg, Russia

    M. N. Gordeev, E. I. Bakhmet & A. N. Tomilin

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Gordeev M.N. wrote the main part of the text, analyzed literature, and prepared illustrations. Bakhmet E.I. analyzed the literature, wrote an introduction and conclusion, and edited the text. Tomilin A. N. edited the text and made final edits.

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Correspondence to A. N. Tomilin.

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The authors declare that they have no conflict of interests. This article does not contain any studies involving human participants or laboratory animals as experimental models performed by the authors.

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Translated by A. Ermakov

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Gordeev, M.N., Bakhmet, E.I. & Tomilin, A.N. Pluripotency Dynamics during Embryogenesis and in Cell Culture. Russ J Dev Biol 52, 379–389 (2021). https://doi.org/10.1134/S1062360421060059

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