Sox2 is essential for formation of trophectoderm in the preimplantation embryo

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Keramari, Maria ^a   Razavi, Janet ^a   Ingman, Karen A ^a   Patsch, Christoph ^b   Edenhofer, Frank ^b   Ward, Christopher M ^c   Kimber, Susan J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 4; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN EOMES; PROTEIN TEAD4; PROTEIN YAP; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; CDX2 PROTEIN, MOUSE; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; MUSCLE PROTEIN; PHOSPHOPROTEIN; POU5F1 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOX2 PROTEIN, MOUSE; TEAD4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYO (ANATOMY); EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FEMALE; GENE SILENCING; IN VITRO STUDY; INNER CELL MASS; MORULA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PREIMPLANTATION EMBRYO; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA INTERFERENCE; TROPHECTODERM; ANIMAL; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST;

MAMMALIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BLASTOCYST; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, CONFOCAL; MORULA; MUSCLE PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PHOSPHOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 78649751050     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013952     Document Type: Article

References (90)

1. Pevny LH, Lovell-Badge R (1997) Sox genes find their feet. Curr Opin Genet Dev 7: 338-344.
2. Scaffidi P, Bianchi ME (2001) Spatially precise DNA bending is an essential activity of the Sox-2 transcription factor. J Biol Chem 276: 47296-47301.
3. Wiebe MS, Wilder PJ, Kelly D, Rizzino A (2000) Isolation, characterization, and differential expression of the murine Sox-2 promoter. Gene 246: 383-393.
4. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, et al. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140.
5. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, et al. (1996) A comparison of the properties of Sox-3 with SRY and two related genes, Sox-1 and Sox-2. Development 122: 509-520.
6. Kamachi Y, Sockanathan S, Liu Q, Breitman M, Lovell-Badge R, et al. (1995) Involvement of SOX proteins in lens-specific activation of crystallin genes. EMBO J 14: 3510-3519.
7. Ragge NK, Lorenz B, Schneider A, Bushby K, de Sanctis L, et al. (2005) SOX2 anophthalmia syndrome. Am J Med Genet A 135: 1-7.
8. Kelberman D, Rizzoti K, Avilion A, Bitner-Glindzicz M, Cianfarani S, et al. (2006) Mutations within Sox2/SOX2 are associated with abnormalities in the hypothalamo-pituitary-gonadal axis in mice and humans. J Clin Invest 116: 2442-2455.
9. Kiernan AE, Pelling AL, Leung KKH, Tang ASP, Bell DM, et al. (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434: 1031-1035.
10. Okubo T, Pevny LH, Hogan BLM (2006) Sox2 is required for development of taste bud sensory cells. Genes Dev 20: 2654-2659.
11. Nishimoto M, Fukushima A, Okuda A, Muramatsu M (1999) The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol Cell Biol 19: 5453-5465.
12. Tokuzawa YE, Kaiho M, Maruyama K, Takahashi K, Mitsui M, et al. (2003) Fbx15 is a novel gene target of Oct3/4 but is dispensable for embryonic stem cell self-renewal and mouse development. Mol Cell Biol 23: 2699-2708.
13. Yuan H, Corbi N, Basilico C, Dailey L (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct3. Genes Dev 9: 2635-2645.
14. Shi W, Wang H, Pan G, Geng Y, Guo Y, et al. (2006) Regulation of the pluripotency marker Rex-1 by Nanog and Sox2. J Biol Chem 281: 23319-23325.
15. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, et al. (2007) Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9: 625-635.
16. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
17. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
18. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
19. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P (2010) Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocysts. Dev Cell 18: 675-685.
20. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, et al. (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391.
21. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, et al. (2005) Transcriptional regulation of Nanog by OCT4 and SOX2. J Biol Chem 280: 24731-24737.
22. Chickarmane V, Troein C, Nuber UA, Sauro HM, Peterson C (2006) Transcriptional dynamics of the embryonic stem cell switch. PLoS Comput Biol 2: 1080-1092.
23. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, et al. (2005) Octamer and Sox elements are required for transcription cis regulation of Nanog Gene Expression. Mol Cell Biol 25: 2475-2485.
24. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, et al. (2005) Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25: 6031-6046.
25. Chambers I, Colby D, Robertson M, Nichols J, Lee S, et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655.
26. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, et al. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642.
27. Okumura-Nakanishi S, Saito M, Niwa H, Ishikawa F (2005) Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 280: 5307-5317.
28. Sun Y, Li H, Yang H, Rao MS, Zhan M (2006) Mechanisms controlling embryonic stem cell self-renewal and differentiation. Crit Rev Eukaryot Gene Expr 16: 211-232.
29. Johnson MH, Ziomek CA (1981) The foundation of two distinct cell lineages within the mouse morula. Cell 24: 71-80.
30. Kimber SJ (1990) Glycoconjugates and cell surface interactions in pre- and peri-implantation mammalian embryonic development. Int Rev Cytol 120: 53-167.
31. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
32. Martin GR (1981) 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 78: 7634-7638.
33. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic Stem Cell Lines Derived from Human Blastocysts. Science 282: 1145-1147.
34. Brook FA, Gardner RL (1997) The origin and efficient derivation of embryonic stem cells in the mouse. Proc Natl Acad Sci U S A 94: 5709-5712.
35. Yamanaka Y, Ralston A, Stephenson RO, Rossant J (2006) Cell and molecular regulation of the mouse blastocyst. Dev Dyn 235: 2301-2314.
36. Ralston A, Rossant J (2005) Genetic regulation of stem cell origins in the mouse embryo. Clin Genet 68: 106-112.
37. Kunath T, Strumpf D, Rossant J (2004) Early trophoblast determination and stem cell maintenance in the mouse - a review. Placenta 25(Suppl. A): S32-S38.
38. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, et al. (2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132: 2093-2102.
39. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, et al. (2008) Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 125: 270-283.
40. Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P, Guo G, Robson P, Draper JS, Rossant J (2010) Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137: 395-403.
41. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F (1999) The transcription factor GATA6 is essential for early extraembryonic development. Development 126: 723-732.
42. 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.
43. Elling U, Klasen C, Eisenberger T, Anlag K, Treier M (2006) Murine inner cell mass-derived lineages depend on Sall4 function. Proc Natl Acad Sci U S A 103: 16319-16324.
44. Zhang J, Tam WL, Tong GQ, Wu Q, Chan HY, et al. (2006) Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol 8: 1114-1123.
45. Niswander L, Martin GR (1992) FGF-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114: 755-768.
46. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282: 2072-2075.
47. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P (1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci U S A 95: 5082-5087.
48. Haffner-Krausz R, Gorivodsky M, Chen Y, Lonai P (1999) Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mech Dev 85: 167-172.
49. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, et al. (2000) Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404: 95-99.
50. Griffin KJ, Amacher SL, Kimmel CB, Kimelman D (1998) Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125: 3379-3388.
51. Pownall ME, Isaacs HV, Slack JM (1998) Two phases of Hox gene regulation during early Xenopus development. Curr Biol 8: 673-676.
52. Bosnali M, Edenhofer F (2008) Generation of transducible versions of transcription factors Oct4 and Sox2. Biol Chem 389: 851-861.
53. Li X, Kato Y, Tsunoda Y (2005) Comparative analysis of development-related gene expression in mouse preimplantation embryos with different developmental potential. Mol Reprod Dev 72: 152-160.
54. Wianny F, Zernicka-Goetz M (2000) Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol 2: 70-75.
55. Kim MH, Yuan X, Okumura S, Ishikawa F (2002) Successful inactivation of endogenous Oct-3/4 and c-mos genes in mouse preimplantation embryos and oocytes using short interfering RNAs. Biochem Biophys Res Commun 296: 1372-1377.
56. Stein P, Zeng F, Pan H, Schultz RM (2005) Absence of non-specific effects of RNA interference triggered by long double-stranded RNA in mouse oocytes. Dev Biol 286: 464-471.
57. Sharova LV, Sharov AA, Piao Y, Shaik N, Sullivan T, et al. (2007) Global gene expression profiling reveals similarities and differences among mouse pluripotent stem cells of different origins and strains. Dev Biol 307: 446-459.
58. Kamjoo M, Brison DR, Kimber SJ (2002) Apoptosis in the preimplantation mouse embryo: effect of strain difference and in vitro culture. Mol Reprod Dev 61: 67-77.
59. Becker-Hapak M, McAllister SS, Dowdy SF (2001) TAT-mediated protein transduction into mammalian cells. Methods 24: 247-256.
60. Batchu RB, Moreno AM, Szmania SM, Bennett G, Spagnoli GC, Ponnazhagan S, Barlogie B, Tricot G, Van Rhee F (2005) Protein Transduction of Dendritic Cells for NY-ESO-1-Based Immunotherapy of Myeloma. Cancer Res 65: 10041-10049.
61. Dominguez-Bendala J, Klein D, Ribeiro M, Ricordi C, Inverardi L, Pastori R, Edlund H (2005) TAT-Mediated Neurogenin 3 Protein Transduction Stimulates Pancreatic Endocrine Differentiation In Vitro. Diabetes 54: 720-726.
62. Brooks H, Lebleu B, Vive's E (2005) Tat peptide-mediated cellular delivery: back to basics. Adv Drug Deliv Rev 57: 559-577.
63. Fleming TP, Butler L, Lei X, Collins J, Javed Q, et al. (1994) Molecular maturation of cell adhesion systems during mouse early development. Histochemistry 101: 1-7.
64. Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267: 246-249.
65. Senner CE, Hemberger M (2010) Regulation of early trophoblast differentiation - Lessons from the mouse. Placenta xxx [Epub ahead of print]. pp 1-7.
66. Rappolee DA, Basilico C, Patel Y, Werb Z (1994) Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development 120: 2259-2269.
67. Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, et al. (1998) FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol 198: 105-115.
68. Ambrosetti DC, Basilico C, Dailey L, (1997) Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on proteinprotein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol Cell Biol 17: 6321-6329.
69. Luster TA, Johnson LR, Nowling TK, Lamb KA, Philipsen S, et al. (2000) Effects of three Sp1 motifs on the transcription of the FGF-4 gene. Mol Reprod Dev 57: 4-15.
70. Luster TA, Rizzino A (2003) Regulation of the FGF-4 gene by a complex distal enhancer that functions in part as an enhanceosome. Gene 323: 163-172.
71. Keenan ID, Sharrard RM, Isaacs HV (2006) FGF signal transduction and the regulation of Cdx gene expression. Dev Biol 299: 478-488.
72. Tsukamoto T, Inada K, Tanaka H, Mizoshita T, Mihara M, et al. (2004) Down-regulation of a gastric transcription factor, Sox2, and ectopic expression of intestinal homeobox genes, Cdx1 and Cdx2: inverse correlation during progression from gastric/intestinal-mixed to complete intestinal metaplasia. J Cancer Res Clin Oncol 130: 135-145.
73. Tatematsu M, Tsukamoto T, Inada K (2003) Stem cells and gastric cancer: role of gastric and intestinal mixed intestinal metaplasia. Cancer Sci 94: 135-141.
74. 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.
75. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A (2009) Nanog is the gateway to the pluripotent ground state. Cell 138: 722-737.
76. Li J, Pan G, Cui K, Liu Y, Xu S, et al. (2007) A dominant negative form of mouse Sox2 induces trophectoderm differentiation and progressive polyploidy in mouse ES cells. J Biol Chem 282: 19481-19492.
77. Beddington RSP, Robertson EJ (1989) An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105: 733-737.
78. Johnson MH, Ziomek CA (1982) Cell subpopulations in the late morula and early blastocyst of the mouse. Dev Biol 91: 431-439.
79. Wilson M, Koopman P (2002) Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr Opin Genet Dev 12: 441-446.
80. Episkopou V (2005) SOX2 functions in adult neural stem cells. Trends Neurosci 28: 219-221.
81. Que J, Okubo T, Goldenring JR, Nam KT, Kurotani R, et al. (2007) Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development 134: 2521-2531.
82. Lim CY, Tam WL, Zhang J, Ang HS, Jia H, et al. (2008) Sall4 Regulates Distinct Transcription Circuitries in Different Blastocyst-Derived Stem Cell Lineages. Cell Stem Cell 3: 543-554.
83. Lian I, Kim J, Okazawa H, Zhao J, Zhao B, Yu J, Chinnaiyan A, Israel MA, Goldstein LS, Abujarour R, Ding S, Guan KL (2010) The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 24: 1106-1118.
84. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, et al. (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234.
85. Brison DR, Schultz RM (1997) Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol Reprod 56: 1088-1096.
86. Hardy K (1997) Cell death in the mammalian blastocyst. Mol Hum Reprod 3: 919-925.
87. Hardy K, Stark J, Winston RM (2003) Maintenance of the inner cell mass in human blastocysts from fragmented embryos. Biol Reprod 68: 1165-1169.
88. Ying QL, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21: 183-186.
89. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A (2004) Rational siRNA design for RNA interference. Nat Biotechnol 22: 326-330.
90. Grabarek JB, Plusa B, Glover DM, Zernicka-Goetz M (2002) Efficient delivery of dsRNA into zona-enclosed mouse oocytes and preimplantation embryos by electroporation. Genesis 32: 269-276.