The molecular underpinnings of totipotency

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1657, 2014, Pages

  Morgani, Sophie M ^a   Brickman, Joshua M ^a  

^a University of Copenhagen   (Denmark)

Author keywords

Embryonic stem cells; Endoderm; Pluripotency; Totipotency; Trophoblast

Indexed keywords

EMPIRICAL ANALYSIS; GENE EXPRESSION; MOLECULAR ANALYSIS; SIGNALING;

CHROMATIN;

ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; CELL PROLIFERATION; CHROMATIN; CYTOLOGY; EMBRYONIC STEM CELL; GENE REGULATORY NETWORK; GENETICS; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TOTIPOTENT STEM CELL;

ANIMALS; CELL LINEAGE; CELL PROLIFERATION; CHROMATIN; EMBRYONIC STEM CELLS; GENE REGULATORY NETWORKS; MICE; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; TOTIPOTENT STEM CELLS;

EID: 84908245609     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0549     Document Type: Review

References (78)

1. Tarkowski AK, Suwinska A, Czolowska R, Ozdzenski W. 2010 Individual blastomeres of 16-and 32-cell mouse embryos are able to develop into foetuses and mice. Dev. Biol. 348, 190-198. (doi:10.1016/j. ydbio.2010.09.022)
2. Rossant J, Lis WT. 1979 Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev. Biol. 70, 255-261. (doi:10.1016/0012-1606(79)90022-8)
3. Handyside AH. 1978 Time of commitment of inside cells isolated from preimplantation mouse embryos. J.Embryol. Exp. Morphol. 45, 37-53.
4. Hogan B, Tilly R. 1978 In vitro development of inner cell masses isolated immunosurgically from mouse blastocysts. I. Inner cell masses from 3.5-day p.c. blastocysts incubated for 24h before immunosurgery. J. Embryol. Exp. Morphol. 45, 93-105.
5. Spindle AI. 1978 Trophoblast regeneration by inner cell masses isolated from cultured mouse embryos. J. Exp. Zool. 203, 483-489. (doi:10.1002/jez. 1402030315)
6. Rossant J, Vijh KM. 1980 Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Dev. Biol. 76, 475-482. (doi:10.1016/0012-1606(80)90395-4)
7. Suwinska A, Czolowska R, Ozdzenski W, Tarkowski AK. 2008 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. Dev. Biol. 322, 133-144. (doi:10. 1016/j.ydbio.2008.07.019)
8. Grabarek JB, Zyzynska K, Saiz N, Piliszek A, Frankenberg S, Nichols J, Hadjantonakis A-K, Plusa B. 2012 Differential plasticity of epiblast and primitive endoderm precursors within the ICM of the early mouse embryo. Development 139, 129-139. (doi:10.1242/dev.067702)
9. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. 1985 The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87, 27-45.
10. Nichols J, Evans EP, Smith AG. 1990 Establishment of germ-line-competent embryonic stem (ES) cells using differentiation inhibiting activity. Development 110, 1341-1348.
11. Ying QL, Nichols J, Chambers I, Smith A. 2003 BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292. (doi:10.1016/S0092-8674(03)00847-X)
12. Huang Y, Osorno R, Tsakiridis A, Wilson V. 2012 In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep. 2, 1571-1578. (doi:10.1016/j.celrep.2012. 10.022)
13. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RDG. 2007 New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199. (doi:10.1038/nature05972)
14. Kojima Y et al. 2014 The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak. Cell Stem Cell 14, 107-120. (doi:10.1016/j.stem.2013.09.014)
15. Chan YS et al. 2013 Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell 13, 663-675. (doi:10.1016/j.stem.2013.11.015)
16. Gafni O et al. 2013 Derivation of novel human ground state naive pluripotent stem cells. Nature 504, 282-286. (doi:10.1038/nature12745)
17. Ware CB et al. 2014 Derivation of naive human embryonic stem cells. Proc. Natl Acad. Sci. USA 111, 4484-4489. (doi:10.1073/pnas.1319738111)
18. Diwan SB, Stevens LC. 1976 Development of teratomas from the ectoderm of mouse egg cylinders. J. Natl Cancer Inst. 57, 937-942.
19. Condic ML. 2014 Totipotency: what it is and what it is not. Stem Cells Dev. 23, 796-812. (doi:10.1089/ scd.2013.0364)
20. Nagy A et al. 1990 Embryonic stem cells alone are able to support fetal development in the mouse. Development 110, 815-821.
21. Wang Z, Jaenisch R. 2004 At most three ES cells contribute to the somatic lineages of chimeric mice and of mice produced by ES-tetraploid complementation. Dev. Biol. 275, 192-201. (doi:10.1016/j.ydbio.2004.06.026)
22. Eakin GS, Hadjantonakis AK, Papaioannou VE, Behringer RR. 2005 Developmental potential and behavior of tetraploid cells in the mouse embryo. Dev. Biol. 288, 150-159. (doi:10.1016/j.ydbio.2005.09.028)
23. Lallemand Y, Brulet P. 1990 An in situ assessment of the routes and extents of colonisation of the mouse embryo by embryonic stem cells and their descendants. Development 110, 1241-1248.
24. DeChiara TM, Poueymirou WT, Auerbach W, Frendewey D, Yancopoulos GD, Valenzuela DM. 2010 Producing fully ES cell-derived mice from eight-cell stage embryo injections. Methods Enzymol. 476, 285-294. (doi:10.1016/S0076-6879(10)76016-X)
25. Saburi S, Azuma S, Sato E, Toyoda Y, Tachi C. 1997 Developmental fate of single embryonic stem cells microinjected into 8-cell-stage mouse embryos. Differentiation 62, 1-11. (doi:10.1046/j.1432-0436. 1997.6210001.x)
26. Canham MA, Sharov AA, Ko MS, Brickman JM. 2010 Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379. (doi:10.1371/journal.pbio.1000379)
27. Chambers I et al. 2007 Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234. (doi:10.1038/ nature06403)
28. Singh AM, Hamazaki T, Hankowski KE, Terada N. 2007 A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25, 2534-2542. (doi:10.1634/stemcells.2007-0126)
29. Falco G, Lee SL, Stanghellini I, Bassey UC, Hamatani T, Ko MS. 2007 Zscan4: a novel gene expressed exclusively in late 2-cell embryos and embryonic stem cells. Dev. Biol. 307, 539-550. (doi:10.1016/j. ydbio.2007.05.003)
30. Zalzman M et al. 2010 Zscan4 regulates telomere elongation and genomic stability in ES cells. Nature 464, 858-863. (doi:10.1038/nature08882)
31. Macfarlan TS et al. 2012 Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487, 57-63. (doi:10.1038/ nature11244)
32. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008 The ground state of embryonic stem cell self-renewal. Nature 453, 519-523. (doi:10.1038/nature06968)
33. Nichols J, Jones K, Phillips JM, Newland SA, Roode M, Mansfield W, Smith A, Cooke A. 2009 Validated germline-competent embryonic stem cell lines from nonobese diabetic mice. Nat. Med. 15, 814-818. (doi:10.1038/nm.1996)
34. Buehr M et al. 2008 Capture of authentic embryonic stem cells from rat blastocysts. Cell 135, 1287-1298. (doi:10.1016/j.cell.2008.12.007)
35. Morgani SM, Canham MA, Nichols J, Sharov AA, Migueles RP, Ko MS, Brickman JM. 2013 Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep. 3, 1945-1957. (doi:10.1016/j. celrep.2013.04.034)
36. Takahashi K, Yamanaka S. 2006 Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. (doi:10.1016/j.cell.2006.07.024)
37. Abad M et al. 2013 Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502, 340-345. (doi:10.1038/ nature12586)
38. Dietrich JE, Hiiragi T. 2007 Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219-4231. (doi:10.1242/dev.003798)
39. Ralston A, Rossant J. 2008 Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 313, 614-629. (doi:10.1016/j.ydbio. 2007.10.054)
40. Chazaud C, Yamanaka Y, Pawson T, Rossant J. 2006 Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624. (doi:10.1016/j.devcel.2006.02.020)
41. Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK. 2008 Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091. (doi:10.1242/dev.021519)
42. Tang F et al. 2011 Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS ONE 6, e21208. (doi:10.1371/ journal.pone.0021208)
43. Peaston AE et al. 2004 Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7, 597-606. (doi:10.1016/j. devcel.2004.09.004)
44. Dan J et al. 2013 Roles for Tbx3 in regulation of two-cell state and telomere elongation in mouse ES cells. Sci. Rep. 3, 3492. (doi:10.1038/ srep03492)
45. Guallar D, Perez-Palacios R, Climent M, Martinez-Abadia I, Larraga A, Fernandez-Juan M, Vallejo C, Muniesa P, Schoorlemmer J. 2012 Expression of endogenous retroviruses is negatively regulated by the pluripotency marker Rex1/Zfp42. Nucl. Acids Res. 40, 8993-9007. (doi:10.1093/nar/gks686)
46. Climent M et al. 2013 Functional analysis of Rex1 during preimplantation development. Stem Cells Dev. 22, 459-472. (doi:10.1089/scd.2012.0211)
47. Obokata H et al. 2014 Bidirectional developmental potential in reprogrammed cells with acquired pluripotency. Nature 505, 676-680. (doi:10.1038/ nature12969)
48. Hung SS, Wong RC, Sharov AA, Nakatake Y, Yu H, Ko MS. 2013 Repression of global protein synthesis by Eif1a-like genes that are expressed specifically in the two-cell embryos and the transient Zscan4-positive state of embryonic stem cells. DNA Res. 20, 391-402. (doi:10.1093/dnares/dst018)
49. Frum T, Halbisen MA, Wang C, Amiri H, Robson P, Ralston A. 2013 Oct4 cell-autonomously promotes primitive endoderm development in the mouse blastocyst. Dev. Cell 25, 610-622. (doi:10.1016/j. devcel.2013.05.004)
50. Le Bin GC et al. 2014 Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst. Development 141, 1001-1010. (doi:10.1242/dev.096875)
51. Messerschmidt DM, Kemler R. 2010 Nanog is required for primitive endoderm formation through a non-cell autonomous mechanism. Dev. Biol. 344, 129-137. (doi:10.1016/j.ydbio.2010.04.020)
52. Mitsui K et al. 2003 The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642. (doi:10. 1016/S0092-8674(03)00393-3)
53. Cai KQ, Capo-Chichi CD, Rula ME, Yang DH, Xu XX. 2008 Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Dev. Dyn. 237, 2820-2829. (doi:10.1002/dvdy.21703)
54. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, Meissner A. 2012 A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344. (doi:10.1038/ nature10960)
55. Gama-Sosa MA, Slagel VA, Trewyn RW, Oxenhandler R, Kuo KC, Gehrke CW, Ehrlich M. 1983 The 5-methylcytosine content of DNA from human tumors. Nucl. Acids Res. 11, 6883-6894. (doi:10. 1093/nar/11.19.6883)
56. Grabole N, Tischler J, Hackett JA, Kim S, Tang F, Leitch HG, Surani MA. 2013 Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep. 14, 629-637. (doi:10.1038/embor.2013.67)
57. Ficz G et al. 2013 FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 13, 351-359. (doi:10.1016/j.stem.2013.06.004)
58. Leitch HG et al. 2013 Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20, 311-316. (doi:10.1038/nsmb.2510)
59. Marks H et al. 2012 The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604. (doi:10.1016/j. cell.2012.03.026)
60. Burton A, Muller J, Tu S, Padilla-Longoria P, Guccione E, Torres-Padilla M-E. 2013 Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Rep. 5, 687-701. (doi:10.1016/j. celrep.2013.09.044)
61. Boyer LA et al. 2006 Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349-353. (doi:10.1038/ nature04733)
62. Reddington JP et al. 2013 Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb target genes. Genome Biol. 14, R25. (doi:10.1186/gb-2013-14-3-r25)
63. Benetti R, Garcia-Cao M, Blasco MA. 2007 Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39, 243-250. (doi:10.1038/ng1952)
64. Gonzalo S, Jaco I, Fraga MF, Chen T, Li E, Esteller M, Blasco MA. 2006 DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8, 416-424. (doi:10.1038/ncb1386)
65. Gonzalo S et al. 2005 Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin. Nat. Cell Biol. 7, 420-428. (doi:10.1038/ncb1235)
66. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA. 2004 Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36, 94-99. (doi:10.1038/ng1278)
67. Huang J et al. 2011 Association of telomere length with authentic pluripotency of ES/iPS cells. Cell Res. 21, 779-792. (doi:10.1038/cr.2011.16)
68. Wong CW et al. 2010 Kruppel-like transcription factor 4 contributes to maintenance of telomerase activity in stem cells. Stem Cells 28, 1510-1517. (doi:10.1002/stem.477)
69. Nakanishi MO, Hayakawa K, Nakabayashi K, Hata K, Shiota K, Tanaka S. 2012 Trophoblast-specific DNA methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse periimplantation embryo. Epigenetics 7, 173-182. (doi:10.4161/epi.7.2.18962)
70. Artus J, Cohen-Tannoudji M. 2008 Cell cycle regulation during early mouse embryogenesis. Mol. Cell. Endocrinol. 282, 78-86. (doi:10.1016/j.mce. 2007.11.008)
71. Goldin SN, Papaioannou VE. 2003 Paracrine action of FGF4 during periimplantation development maintains trophectoderm and primitive endoderm. Genesis 36, 40-47. (doi:10.1002/gene.10192)
72. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. 1998 Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075. (doi:10.1126/science.282.5396.2072)
73. Nichols J, Silva J, Roode M, Smith A. 2009 Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136, 3215-3222. (doi:10.1242/dev.038893)
74. Kang M, Piliszek A, Artus J, Hadjantonakis AK. 2013 FGF4 is required for lineage restriction and salt-andpepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140, 267-279. (doi:10.1242/dev.084996)
75. Krawchuk D, Honma-Yamanaka N, Anani S, Yamanaka Y. 2013 FGF4 is a limiting factor controlling the proportions of primitive endoderm and epiblast in the ICM of the mouse blastocyst. Dev. Biol. 384, 65-71. (doi:10.1016/j.ydbio.2013.09.023)
76. Frankenberg S et al. 2011 Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev. Cell 21, 1005-1013. (doi:10.1016/j.devcel.2011.10.019)
77. Chen Y, Blair K, Smith A. 2013 Robust self-renewal of rat embryonic stem cells requires fine-tuning of glycogen synthase kinase-3 inhibition. Stem Cell Rep. 1, 209-217. (doi:10.1016/j.stemcr.2013.07.003)
78. Cerulo L et al. 2014 Identification of a novel gene signature of ES cells self-renewal fluctuation through system-wide analysis. PLoS ONE 9, e83235. (doi:10.1371/journal.pone.0083235)