Mechanisms of Pluripotency In Vivo and In Vitro

Current Topics in Developmental Biology

Volumn 107, Issue , 2014, Pages 1-37

  Posfai, Eszter ^a   Tam, Oliver H ^a   Rossant, Janet ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Embryonic stem cell; Epiblast stem cell; Lineage maintenance; Lineage specification; Mouse embryo; Pluripotency; Signaling pathway; Transcription factor

Indexed keywords

SIGNAL PEPTIDE; TRANSCRIPTION FACTOR;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; EMBRYONIC STEM CELL; EPIBLAST STEM CELL; GERM LAYER; LINEAGE MAINTENANCE; LINEAGE SPECIFICATION; METABOLISM; MOUSE; MOUSE EMBRYO; PHYSIOLOGY; PLURIPOTENCY; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; SIGNALING PATHWAY;

EMBRYONIC STEM CELL; EPIBLAST STEM CELL; LINEAGE MAINTENANCE; LINEAGE SPECIFICATION; MOUSE EMBRYO; PLURIPOTENCY; SIGNALING PATHWAY; TRANSCRIPTION FACTOR;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC STEM CELLS; GERM LAYERS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MODELS, BIOLOGICAL; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84892467332     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-416022-4.00001-9     Document Type: Chapter

References (177)

1. Aksoy I., Jauch R., Chen J., Dyla M., Divakar U., Bogu G.K., et al. Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm. The EMBO Journal 2013, 32(7):938-953.
2. Alarcon V.B. Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo. Biology of Reproduction 2010, 83(3):347-358.
3. Arman E.E., Haffner-Krausz R.R., Chen Y.Y., Heath J.K.J., Lonai P.P. 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 1998, 95(9):5082-5087.
4. Arnold S.J., Robertson E.J. Making a commitment: Cell lineage allocation and axis patterning in the early mouse embryo. Nature Reviews. Molecular Cell Biology 2009, 10(2):91-103.
5. Atlasi Y., Looijenga L., Fodde R. Cancer stem cells, pluripotency, and cellular heterogeneity: A WNTer perspective. Current Topics in Developmental Biology 2013, 107:373-404.
6. Barrow J.R., Howell W.D., Rule M., Hayashi S., Thomas K.R., Capecchi M.R., et al. Wnt3 signaling in the epiblast is required for proper orientation of the anteroposterior axis. Developmental Biology 2007, 312(1):312-320.
7. Batlle-Morera L., Smith A., Nichols J. Parameters influencing derivation of embryonic stem cells from murine embryos. Genesis 2008, 46(12):758-767.
8. Beddington R.S.R., Robertson E.J.E. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 1989, 105(4):733-737.
9. Bernardo A.S., Faial T., Gardner L., Niakan K.K., Ortmann D., Senner C.E., et al. BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 2011, 9(2):144-155.
10. Bernemann C., Greber B., Ko K., Sterneckert J., Han D.W., Araúzo-Bravo M.J., et al. Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features. Stem Cells 2011, 29(10):1496-1503.
11. Biechele S., Cockburn K., Lanner F., Cox B.J., Rossant J. Porcn-dependent Wnt signaling is not required prior to mouse gastrulation. Development 2013, 140(14):2961-2971.
12. Biechele S., Cox B.J., Rossant J. Porcupine homolog is required for canonical Wnt signaling and gastrulation in mouse embryos. Developmental Biology 2011, 355(2):275-285.
13. Bradley A., Evans M., Kaufman M.H., Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 1984, 309(5965):255-256.
14. Brons I.G.M., Smithers L.E., Trotter M.W.B., Rugg-Gunn P., Sun B., de Sousa Chuva, et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007, 448(7150):191-195.
15. Brook F.A., Gardner R.L. 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 1997, 94(11):5709-5712.
16. Brown K.A., Pietenpol J.A., Moses H.L. A tale of two proteins: Differential roles and regulation of Smad2 and Smad3 in TGF-β signaling. Journal of Cellular Biochemistry 2007, 101(1):9-33.
17. Buehr M., Smith A. Genesis of embryonic stem cells. Philosophical Transactions of the Royal Society B: Biological Sciences 2003, 358(1436):1397-1402.
18. Cai K.Q.K., Capo-Chichi C.D.C., Rula M.E.M., Yang D.-H.D., Xu X.-X.X. Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Developmental Dynamics 2008, 237(10):2820-2829.
19. Canham M.A., Sharov A.A., Ko M.S.H., Brickman J.M. Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biology 2010, 8(5). 10.1371/journal.pbio.1000379.
20. Chambers I., Silva J., Colby D., Nichols J., Nijmeijer B., Robertson M., et al. Nanog safeguards pluripotency and mediates germline development. Nature 2007, 450(7173):1230-1234.
21. Chazaud C., Yamanaka Y., Pawson T., Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Developmental Cell 2006, 10(5):615-624.
22. Cheng A.M., Saxton T.M., Sakai R., Kulkarni S., Mbamalu G., Vogel W., et al. Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 1998, 95(6):11.
23. Cockburn K., Biechele S., Garner J., Rossant J. The Hippo pathway member Nf2 is required for inner cell mass specification. Current Biology 2013, 23(13):1195-1201.
24. Cockburn K., Rossant J. Making the blastocyst: Lessons from the mouse. The Journal of Clinical Investigation 2010, 120(4):995-1003.
25. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., et al. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 1994, 120(7):1919-1928.
26. Coucouvanis E., Martin G.R. Signals for death and survival: A two-step mechanism for cavitation in the vertebrate embryo. Cell 1995, 83(2):279-287.
27. Coucouvanis E., Martin G.R. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 1999, 126(3):535-546.
28. Cross J.C. How to make a placenta: Mechanisms of trophoblast cell differentiation in mice-A review. Placenta 2005, 26:S3-S9.
29. Currier N., Chea K., Hlavacova M., Sussman D.J., Seldin D.C., Dominguez I. Dynamic expression of a LEF-EGFP Wnt reporter in mouse development and cancer. Genesis 2010, 48:183-194.
30. Dailey L., Ambrosetti D., Mansukhani A., Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine & Growth Factor Reviews 2005, 16(2):233-247.
31. Davies O.R., Lin C.-Y., Radzisheuskaya A., Zhou X., Taube J., Blin G., et al. Tcf15 primes pluripotent cells for differentiation. Cell Reports 2013, 3(2):472-484.
32. De Los Angeles A., Loh Y.-H., Tesar P.J., Daley G.Q. Accessing naïve human pluripotency. Current Opinion in Genetics & Development 2012, 22(3):272-282.
33. Dietrich J.-E.J., Hiiragi T.T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007, 134(23):4219-4231.
34. Di-Gregorio A., Sancho M., Stuckey D.W., Crompton L.A., Godwin J., Mishina Y., et al. BMP signalling inhibits premature neural differentiation in the mouse embryo. Development 2007, 134(18):3359-3369.
35. Dillon N. Factor mediated gene priming in pluripotent stem cells sets the stage for lineage specification. BioEssays 2012, 34(3):194-204.
36. Do D.V., Ueda J., Messerschmidt D.M., Lorthongpanich C., Zhou Y., Feng B., et al. A genetic and developmental pathway from STAT3 to the OCT4-NANOG circuit is essential for maintenance of ICM lineages in vivo. Genes and Development 2013, 27(12):1378-1390.
37. Ducibella T., Ukena T., Karnovsky M., Anderson E. Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo. The Journal of Cell Biology 1977, 74(1):153-167.
38. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292(5819):154-156.
39. Faddah D.A., Wang H., Cheng A.W., Katz Y., Buganim Y., Jaenisch R. Cell Stem Cell 2013, 13(1):23-29.
40. Fei T., Xia K., Li Z., Zhou B., Zhu S., Chen H., et al. Genome-wide mapping of SMAD target genes reveals the role of BMP signaling in embryonic stem cell fate determination. Genome Research 2010, 20(1):36-44.
41. Fei T., Zhu S., Xia K., Zhang J., Li Z., Han J.-D.J., et al. Smad2 mediates Activin/Nodal signaling in mesendoderm differentiation of mouse embryonic stem cells. Cell Research 2010, 20(12):1306-1318.
42. Feldman B., Poueymirou W., Papaioannou V.E., DeChiara T.M., Goldfarb M. Requirement of FGF-4 for postimplantation mouse development. Science 1995, 267(5195):246-249.
43. Festuccia N., Osorno R., Halbritter F., Karwacki-Neisius V., Navarro P., Colby D., et al. Esrrb is a direct nanog target gene that can substitute for nanog function in pluripotent cells. Cell Stem Cell 2012, 11(4):477-490.
44. Ficz G., Hore T.A., Santos F., Lee H.J., Dean W., Arand J., et al. Cell Stem Cell 2013, 13(1):1-9.
45. Filipczyk A., Gkatzis K., Fu J., Hoppe P.S., Lickert H., Anastassiadis K., et al. Biallelic expression of Nanog protein in mouse embryonic stem cells. Cell Stem Cell 2013, 13(1):12-13.
46. Frankenberg S., Gerbe F., Bessonnard S., Belville C., Pouchin P., Bardot O., et al. Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Developmental Cell 2011, 21(6):1005-1013.
47. Frum T., Halbisen M.A., Wang C., Amiri H., Robson P., Ralston A. Oct4 cell-autonomously promotes PE development. Developmental Cell 2013, 25:1-13.
48. Fujikura J.J., Yamato E.E., Yonemura S.S., Hosoda K.K., Masui S.S., Nakao K.K., et al. Differentiation of embryonic stem cells is induced by GATA factors. Genes and Development 2002, 16(7):784-789.
49. Gerbe F., Cox B., Rossant J., Chazaud C. Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst. Developmental Biology 2008, 313(2):594-602.
50. Goldin S.N., Papaioannou V.E. Paracrine action of FGF4 during periimplantation development maintains trophectoderm and primitive endoderm. Genesis 2003, 36(1):40-47.
51. Greber B., Wu G., Bernemann C., Joo J.Y., Han D.W., Ko K., et al. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 2010, 6(3):215-226.
52. Guo Guoji, Huss M., Tong G.Q., Wang C., Sun L.L., Clarke N.D., et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Developmental Cell 2010, 18(4):675-685.
53. Guo Ge, Yang J., Nichols J., Hall J.S., Eyres I., Mansfield W., et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009, 136(7):1063-1069.
54. Hamazaki T., Kehoe S.M., Nakano T., Terada N. The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Molecular and Cellular Biology 2006, 26(20):7539-7549.
55. Han D.W., Tapia N., Joo J.Y., Greber B., Araúzo-Bravo M.J., Bernemann C., et al. Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell 2010, 143(4):617-627.
56. Handyside A.H.A. Distribution of antibody- and lectin-binding sites on dissociated blastomeres from mouse morulae: Evidence for polarization at compaction. Journal of Embryology and Experimental Morphology 1980, 60:99-116.
57. Hanna J., Markoulaki S., Mitalipova M., Cheng A.W., Cassady J.P., Staerk J., et al. Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 2009, 4(6):513-524.
58. Hartshorn C., Eckert J.J., Hartung O., Wangh L.J. Single-cell duplex RT-LATE-PCR reveals Oct4 and Xist RNA gradients in 8-cell embryos. BMC Biotechnology 2007, 7(1):87.
59. Hay D.C.D., Sutherland L.L., Clark J.J., Burdon T.T. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 2004, 22(2):225-235.
60. Hayashi K., De Sousa Lopes S.M.C., Tang F., Surani M.A. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 2008, 3(4):11.
61. Hirate Y., Hirahara S., Inoue K.-I., Suzuki A., Alarcon V.B., Akimoto K., et al. Polarity-dependent distribution of angiomotin localizes hippo signaling in preimplantation embryos. Current Biology 2013, 23(13):1181-1194.
62. Hsieh J.-C., Lee L., Zhang L., Wefer S., Brown K., DeRossi C., et al. Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell 2003, 112(3):13.
63. Huang Y., Osorno R., Tsakiridis A., Wilson V. In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Reports 2012, 2(6):1571-1578.
64. Jauch R., Aksoy I., Hutchins A.P., Ng C.K.L., Tian X.F., Chen J., et al. Conversion of Sox17 into a pluripotency reprogramming factor by reengineering its association with Oct4 on DNA. Stem Cells 2011, 29(6):940-951.
65. Johnson C.E., Crawford B.E., Stavridis M., Ten Dam G., Wat A.L., Rushton G., et al. Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 2007, 25(8):1913-1923.
66. Johnson M.H., Ziomek C.A. Induction of polarity in mouse 8-cell blastomeres: Specificity, geometry, and stability. The Journal of Cell Biology 1981, 91(1):303-308.
67. Johnson M.H., Ziomek C.A. Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16- to the 32-cell stage. Developmental Biology 1983, 95(1):211-218.
68. Johnston R.J., Desplan C. Stochastic mechanisms of cell fate specification that yield random or robust outcomes. Annual Review of Cell and Developmental Biology 2010, 26:689-719.
69. Kalmar T., Lim C., Hayward P., Muñoz-Descalzo S., Nichols J., Garcia-Ojalvo J., et al. Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biology 2009, 7(7).
70. Kang M.M., Piliszek A.A., Artus J.J., Hadjantonakis A.-K.A. FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 2013, 140(2):267-279.
71. Karwacki-Neisius V., Göke J., Osorno R., Halbritter F., Ng J.H., Weiße A.Y., et al. Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog. Cell Stem Cell 2013, 12(5):531-545.
72. Kelly S.J. Studies of the developmental potential of 4- and 8-cell stage mouse blastomeres. Journal of Experimental Zoology 1977, 200(3):365-376.
73. Kelly O.G., Pinson K.I., Skarnes W.C. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004, 131(12):2803-2815.
74. Koutsourakis M., Langeveld A., Patient R., Beddington R., Grosveld F. The transcription factor GATA6 is essential for early extraembryonic development. Development 1999, 126(9):723-732.
75. Kraushaar D.C., Rai S., Condac E., Nairn A., Zhang S., Yamaguchi Y., et al. Heparan sulfate facilitates FGF and BMP signaling to drive mesoderm differentiation of mouse embryonic stem cells. The Journal of Biological Chemistry 2012, 287(27):22691-22700.
76. Kraushaar D.C., Yamaguchi Y., Wang L. Heparan sulfate is required for embryonic stem cells to exit from self-renewal. The Journal of Biological Chemistry 2010, 285(8):5907-5916.
77. Kunath T., Arnaud D., Uy G.D., Okamoto I., Chureau C., Yamanaka Y., et al. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 2005, 132(7):1649-1661.
78. Kunath T., Saba-El-Leil M.K., Almousailleakh M., Wray J., Meloche S., Smith A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007, 134(16):2895-2902.
79. Kurimoto K., Yabuta Y., Ohinata Y., Ono Y., Uno K.D., Yamada R.G., et al. An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Research 2006, 34(5):e42.
80. Lanner F., Lee K.L., Sohl M., Holmborn K., Yang H., Wilbertz J., et al. Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 2010, 28(2):191-200.
81. Lanner F., Rossant J. The role of FGF/Erk signaling in pluripotent cells. Development 2010, 137(20):3351-3360.
82. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes and Development 1999, 13(4):424-436.
83. Lawson K.A., Meneses J.J., Pedersen R.A. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 1991, 113(3):891-911.
84. Lee K.L., Lim S.K., Orlov Y.L., Yit L.Y., Yang H., Ang L.T., et al. Graded nodal/activin signaling titrates conversion of quantitative phospho-Smad2 levels into qualitative embryonic stem cell fate decisions. PLoS Genetics 2011, 7(6). 10.1371/journal.pbio.1000149.
85. Li Z., Chen Y.-G. Fine-tune of intrinsic ERK activity by extrinsic BMP signaling in mouse embryonic stem cells. Protein & Cell 2012, 3(6):401-404.
86. Li M.M., Sendtner M.M., Smith A.A. Essential function of LIF receptor in motor neurons. Nature 1995, 378(6558):724-727.
87. Lian I., Kim J., Okazawa H., Zhao J., Zhao B., Yu J., et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes and Development 2010, 24(11):1106-1118.
88. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nature Genetics 1999, 22(4):361-365.
89. Lorthongpanich C., Doris T.P.Y., Limviphuvadh V., Knowles B.B., Solter D. Developmental fate and lineage commitment of singled mouse blastomeres. Development 2012, 139(20):3722-3731.
90. Lorthongpanich C., Messerschmidt D.M., Chan S.W., Hong W., Knowles B.B., Solter D. Temporal reduction of LATS kinases in the early preimplantation embryo prevents ICM lineage differentiation. Genes and Development 2013, 27(13):1441-1446.
91. Magnúsdóttir E., Gillich A., Grabole N., Surani M.A. Combinatorial control of cell fate and reprogramming in the mammalian germline. Current Opinion in Genetics & Development 2012, 22(5):466-474.
92. Maretto S.S., Cordenonsi M.M., Dupont S.S., Braghetta P.P., Broccoli V.V., Hassan A.B.A., et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(6):3299-3304.
93. Maro B., Johnson M.H., Pickering S.J., Louvard D. Changes in the distribution of membranous organelles during mouse early development. Journal of Embryology and Experimental Morphology 1985, 90:287-309.
94. Martello G., Sugimoto T., Diamanti E., Joshi A., Hannah R., Ohtsuka S., et al. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 2012, 11(4):491-504.
95. Martin G.R. 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 1981, 78(12):7634-7638.
96. Meilhac S.M., Adams R.J., Morris S.A., Danckaert A., Le Garrec J.-F., Zernicka-Goetz M. Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst. Developmental Biology 2009, 331(2):210-221.
97. Mesnard D.D., Guzman-Ayala M.M., Constam D.B.D. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 2006, 133(13):2497-2505.
98. Messerschmidt D.M., Kemler R. Nanog is required for primitive endoderm formation through a non-cell autonomous mechanism. Developmental Biology 2010, 344(1):129-137.
99. Mishina Y., Suzuki A., Ueno N., Behringer R.R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes and Development 1995, 9(24):3027-3037.
100. Mitsui K.K., Tokuzawa Y.Y., Itoh H.H., Segawa K.K., Murakami M.M., Takahashi K.K., et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113(5):12.
101. Miyanari Y., Torres-Padilla M.-E. Control of ground-state pluripotency by allelic regulation of Nanog. Nature 2012, 483(7390):470-473.
102. Mohamed O.A., Clarke H.J., Dufort D. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Developmental Dynamics 2004, 231(2):416-424.
103. Morgani S.M., Canham M.A., Nichols J., Sharov A.A., Migueles R.P., Ko M.S.H., et al. Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Reports 2013, 3(6):1945-1957.
104. Morris S.A., Teo R.T.Y., Li H., Robson P., Glover D.M., Zernicka-Goetz M. 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 2010, 107(14):6364-6369.
105. Morrisey E.E., Tang Z., Sigrist K., Lu M.M., Jiang F., Ip H.S., et al. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes and Development 1998, 12(22):3579-3590.
106. Najm F.J., Chenoweth J.G., Anderson P.D., Nadeau J.H., Redline R.W., McKay R.D.G., et al. Isolation of epiblast stem cells from preimplantation mouse embryos. Cell Stem Cell 2011, 8(3):318-325.
107. Nakai-Futatsugi Y.Y., Niwa H.H. Transcription factor network in embryonic stem cells: Heterogeneity under the stringency. Biological & Pharmaceutical Bulletin 2013, 36(2):166-170.
108. Nakashima K.K., Wiese S.S., Yanagisawa M.M., Arakawa H.H., Kimura N.N., Hisatsune T.T., et al. Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. The Journal of Neuroscience 1999, 19(13):5429-5434.
109. Niakan K.K., Ji H., Maehr R., Vokes S.A., Rodolfa K.T., Sherwood R.I., et al. Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes and Development 2010, 24(3):312-326.
110. Nichols J., Chambers I., Taga T., Smith A. Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines. Development 2001, 128(12):2333-2339.
111. Nichols J., Davidson D., Taga T., Yoshida K., Chambers I., Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mechanisms of Development 1996, 57(2):123-131.
112. Nichols J., Silva J., Roode M., Smith A. Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 2009, 136(19):3215-3222.
113. Nichols J., Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4(6):487-492.
114. Nishioka N., Inoue K.-I., Adachi K., Kiyonari H., Ota M., Ralston A., et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Developmental Cell 2009, 16(3):398-410.
115. Niswander L., Martin G.R. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 1992, 114(3):755-768.
116. Niwa H., Toyooka Y., Shimosato D., Strumpf D., Takahashi K., Yagi R., et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123(5):917-929.
117. Nostro M.C., Cheng X., Keller G.M., Gadue P. Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2008, 2(1):60-71.
118. Nowotschin S., Costello I., Piliszek A., Kwon G.S., Mao C.-A., Klein W.H., et al. The T-box transcription factor Eomesodermin is essential for AVE induction in the mouse embryo. Genes and Development 2013, 27(9):997-1002.
119. Nowotschin S., Hadjantonakis A.-K. Cellular dynamics in the early mouse embryo: From axis formation to gastrulation. Current Opinion in Genetics & Development 2010, 20(4):420-427.
120. Ogawa K., Saito A., Matsui H., Suzuki H., Ohtsuka S., Shimosato D., et al. Activin-Nodal signaling is involved in propagation of mouse embryonic stem cells. Journal of Cell Science 2007, 120(1):55-65.
121. Palmieri S.L.S., Peter W.W., Hess H.H., Schöler H.R.H. Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Developmental Biology 1994, 166(1):259-267.
122. Pfendler K.C., Catuar C.S., Meneses J.J., Pedersen R.A. Overexpression of Nodal promotes differentiation of mouse embryonic stem cells into mesoderm and endoderm at the expense of neuroectoderm formation. Stem Cells and Development 2005, 14(2):162-172.
123. Pietersen A.M., van Lohuizen M. Stem cell regulation by polycomb repressors: Postponing commitment. Current Opinion in Cell Biology 2008, 20(2):201-207.
124. Plusa B., Frankenberg S., Chalmers A., Hadjantonakis A.-K., Moore C.A., Papalopulu N., et al. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. Journal of Cell Science 2005, 118(3):505-515.
125. Plusa B., Piliszek A., Frankenberg S., Artus J., Hadjantonakis A.-K. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 2008, 135(18):3081-3091.
126. Pratt H.P., Ziomek C.A., Reeve W.J., Johnson M.H. Compaction of the mouse embryo: An analysis of its components. Journal of Embryology and Experimental Morphology 1982, 70:113-132.
127. Qi X., Li T.-G., Hao J., Hu J., Wang J., Simmons H., et al. BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(16):6027-6032.
128. Radzisheuskaya A., Le Bin Chia G., dos Santos R.L., Theunissen T.W., Castro L.F.C., Nichols J., et al. A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages. Nature Cell Biology 2013, 15(6):579-590.
129. Ralston A., Rossant J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Developmental Biology 2008, 313(2):614-629.
130. Rappolee D.A., Basilico C., Patel Y., Werb Z. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development 1994, 120(8):2259-2269.
131. Reeve W.J.W., Ziomek C.A.C. Distribution of microvilli on dissociated blastomeres from mouse embryos: Evidence for surface polarization at compaction. Journal of Embryology and Experimental Morphology 1981, 62:339-350.
132. Rossant J., Cross J.C. Placental development: Lessons from mouse mutants. Nature Reviews. Genetics 2001, 2(7):538-548.
133. Rossant J., Tam P.P.L. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 2009, 136(5):701-713.
134. Santostefano K.E., Hamazaki T., Pardo C.E., Kladde M.P., Terada N. Fibroblast growth factor receptor 2 homodimerization rapidly reduces transcription of the pluripotency gene Nanog without dissociation of activating transcription factors. The Journal of Biological Chemistry 2012, 287(36):30507-30517.
135. Schrode N., Xenopoulos P., Piliszek A., Frankenberg S., Plusa B., Hadjantonakis A.-K. Anatomy of a blastocyst: Cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis 2013, 51(4):219-233.
136. Shen M.M.M. Nodal signaling: Developmental roles and regulation. Development 2007, 134(6):1023-1034.
137. Silva J., Nichols J., Theunissen T.W., Guo G., van Oosten A.L., Barrandon O., et al. Nanog is the gateway to the pluripotent ground state. Cell 2009, 138(4):722-737.
138. Singh A.M., Hamazaki T., Hankowski K.E., Terada N. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 2007, 25(10):2534-2542.
139. Sirard C., Kim S., Mirtsos C., Tadich P., Hoodless P.A., Itie A., et al. Targeted disruption in murine cells reveals variable requirement for Smad4 in transforming growth factor β-related signaling. Journal of Biological Chemistry 2000, 275(3):2063-2070.
140. Skamagki M., Wicher K.B., Jedrusik A., Ganguly S., Zernicka-Goetz M. Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Cell Reports 2013, 3:1-16.
141. Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., et al. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988, 336(6200):688-690.
142. Stavridis M.P., Collins B.J., Storey K.G. Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation. Development 2010, 137(6):881-890.
143. Stavridis M.P., Lunn J.S., Collins B.J., Storey K.G. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 2007, 134(16):2889-2894.
144. Stephenson R.O., Rossant J., Tam P.P.L. Intercellular interactions, position, and polarity in establishing blastocyst cell lineages and embryonic axes. Cold Spring Harbor Perspectives in Biology 2012, 4(11). 10.1101/cshperspect.a008235.
145. Stephenson R.O.R., Yamanaka Y.Y., Rossant J.J. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development 2010, 137(20):3383-3391.
146. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Köntgen F., et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359(6390):76-79.
147. Strumpf D., Mao C.-A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132(9):2093-2102.
148. Sumi T., Oki S., Kitajima K., Meno C. Epiblast ground state is controlled by canonical Wnt/β-catenin signaling in the postimplantation mouse embryo and epiblast stem cells. PLoS One 2013, 8(5).
149. Suzuki A., Raya Á., Kawakami Y., Morita M., Matsui T., Nakashima K., et al. Nanog binds to Smad1 and blocks bone morphogenetic protein-induced differentiation of embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(27):10294-10299.
150. Tabansky I., Lenarcic A., Draft R.W., Loulier K., Keskin D.B., Rosains J., et al. Developmental bias in cleavage-stage mouse blastomeres. Current Biology 2013, 23(1):21-31.
151. Tamm C., Böwer N., Annerén C. Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. Journal of Cell Science 2011, 124(7):1136-1144.
152. Tanaka S. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282(5396):2072-2075.
153. Tarkowski A.K. Experiments on the development of isolated blastomeres of mouse eggs. Nature 1959, 184:1286-1287.
154. Tarkowski A.K., Wróblewska J. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. Journal of Embryology and Experimental Morphology 1967, 18(1):155-180.
155. ten Berge D., Kurek D., Blauwkamp T., Koole W., Maas A., Eroglu E., et al. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nature Cell Biology 2011, 13(9):1070-1075.
156. Tesar P.J., Chenoweth J.G., Brook F.A., Davies T.J., Evans E.P., Mack D.L., et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448(7150):196-199.
157. Torres-Padilla M.-E., Parfitt D.-E., Kouzarides T., Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007, 445(7124):214-218.
158. Toyooka Y., Shimosato D., Murakami K., Takahashi K., Niwa H. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 2008, 135(5):909-918.
159. Tremblay K.D., Hoodless P.A., Bikoff E.K., Robertson E.J. Formation of the definitive endoderm in mouse is a Smad2-dependent process. Development 2000, 127(14):3079-3090.
160. Tropepe V., Hitoshi S., Sirard C., Mak T.W., Rossant J., van der Kooy D. Direct neural fate specification from embryonic stem cells-A primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 2001, 30(1):14.
161. Vallier L., Mendjan S., Brown S., Chng Z., Teo A., Smithers L.E., et al. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 2009, 136(8):1339-1349.
162. Wang Y.Y., Smedberg J.L.J., Cai K.Q.K., Capo-Chichi D.C.D., Xu X.-X.X. Ectopic expression of GATA6 bypasses requirement for Grb2 in primitive endoderm formation. Developmental Dynamics 2011, 240(3):566-576.
163. Wang C.C., Song B.B. Cell-type-specific expression of the platelet-derived growth factor alpha receptor: A role for GATA-binding protein. Molecular and Cellular Biology 1996, 16(2):712-723.
164. Ware C.B., Horowitz M.C., Renshaw B.R., Hunt J.S., Liggitt D., Koblar S.A., et al. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 1995, 121(5):1283-1299.
165. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., et al. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336(6200):684-687.
166. Winnier G., Blessing M., Labosky P.A., Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes and Development 1995, 9(17):2105-2116.
167. Wu G., Gentile L., Fuchikami T., Sutter J., Psathaki K., Esteves T.C., et al. Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development 2010, 137(24):4159-4169.
168. Yagi R., Kohn M.J., Karavanova I., Kaneko K.J., Vullhorst D., DePamphilis M.L., et al. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 2007, 134(21):3827-3836.
169. Yamanaka Y., Lanner F., Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 2010, 137(5):715-724.
170. Yamanaka Y.Y., Ralston A.A., Stephenson R.O.R., Rossant J.J. Cell and molecular regulation of the mouse blastocyst. Developmental Dynamics 2006, 235(9):2301-2314.
171. Ying Q.-L., Nichols J., Chambers I., Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003, 115(3):281-292.
172. Ying Q.-L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., et al. The ground state of embryonic stem cell self-renewal. Nature 2008, 453(7194):519-523.
173. Yoshida K.K., Taga T.T., Saito M.M., Suematsu S.S., Kumanogoh A.A., Tanaka T.T., 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 1996, 93(1):407-411.
174. Yoshida-Koide U., Matsuda T., Saikawa K., Nakanuma Y., Yokota T., Asashima M., et al. Involvement of Ras in extraembryonic endoderm differentiation of embryonic stem cells. Biochemical and Biophysical Research Communications 2004, 313(3):475-481.
175. Zernicka-Goetz M., Morris S.A., Bruce A.W. Making a firm decision: Multifaceted regulation of cell fate in the early mouse embryo. Nature Publishing Group 2009, 10(7):467-477.
176. Zhang J., Fei T., Li Z., Zhu G., Wang L., Chen Y.G. BMP induces cochlin expression to facilitate self-renewal and suppress neural differentiation of mouse embryonic stem cells. Journal of Biological Chemistry 2013, 288(12):8053-8060.
177. Zhang K., Li L., Huang C., Shen C., Tan F., Xia C., et al. Distinct functions of BMP4 during different stages of mouse ES cell neural commitment. Development 2010, 137(13):2095-2105.