Dynamic changes in Wnt signaling are required for neuronal differentiation of mouse embryonic stem cells

Molecular and Cellular Neuroscience

Volumn 48, Issue 3, 2011, Pages 205-216

  Slawny, N A ^a   O'Shea, K S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

catenin; Ectoderm; Gastrulation; Mesendoderm; ShRNA; Tcf Lef

Indexed keywords

BETA CATENIN; BETA TUBULIN; BETA3 TUBULIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX3; TRANSCRIPTION FACTOR TCF4; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDODERM; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GASTRULATION; IMMUNOHISTOCHEMISTRY; MESODERM; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEURAL TUBE; NEURULATION; NIDATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; WESTERN BLOTTING;

ANIMALS; CELL LINE; CELL LINEAGE; CELLS, CULTURED; EMBRYONIC STEM CELLS; MICE; NEUROGENESIS; NEURONS; WNT SIGNALING PATHWAY;

MUS;

EID: 80053384049     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.07.010     Document Type: Article

References (89)

1. Arce L., Yokoyama N.N., Waterman M.L. Diversity of LEF/TCF action in development and disease. Oncogene 2006, 25:7492-7504.
2. Aubert J., Dunstan H., Chambers I., Smith A.G. Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat. Biotechnol. 2002, 20:1240-1245.
3. Ben-Haim N., Lu C., Guzman-Ayala M., Pescatore L., Mesnard D., Bischofberger M., Naef F., Robertson E.J., Constam D.B. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell 2006, 11:313-323.
4. Blauwkamp T.A., Chang M.V., Cadigan K.M. Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 2008, 27:1436-1446.
5. Bone H.K., Damiano T., Bartlett S., Perry A., Letchford J., Ripoll Y.S., Nelson A.S., Welham M.J. Involvement of GSK-3 in regulation of murine embryonic stem cell self-renewal revealed by a series of bisindolylmaleimides. Chem. Biol. 2009, 16:15-27.
6. Brantjes H., Roose J., van De Wetering M., Clevers H. All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 2001, 29:1410-1419.
7. Cajanek L., Ribeiro D., Liste I., Parish C.L., Bryja V., Arenas E. Wnt/beta-catenin signaling blockade promotes neuronal induction and dopaminergic differentiation in embryonic stem cells. Stem Cells 2009, 27:2917-2927.
8. Chesnutt C., Burrus L.W., Brown A.M., Niswander L. Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev. Biol. 2004, 274:334-347.
9. Chien A.J., Conrad W.H., Moon R.T. A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 2009, 129:1614-1627.
10. Ciani L., Salinas P.C. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 2005, 6:351-362.
11. Cole M.F., Johnstone S.E., Newman J.J., Kagey M.H., Young R.A. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev. 2008, 22:746-755.
12. Daniels D.L., Weis W.I. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 2005, 12:364-371.
13. Desbaillets I., Ziegler U., Groscurth P., Gassmann M. Embryoid bodies: an in vitro model of mouse embryogenesis. Exp. Physiol. 2000, 85:645-651.
14. Doble B.W., Woodgett J.R. Role of glycogen synthase kinase-3 in cell fate and epithelial-mesenchymal transitions. Cells Tissues Organs 2007, 185:73-84.
15. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
16. Finlay D., Patel S., Dickson L.M., Shpiro N., Marquez R., Rhodes C.J., Sutherland C. Glycogen synthase kinase-3 regulates IGFBP-1 gene transcription through the thymine-rich insulin response element. BMC Mol. Biol. 2004, 5:15.
17. Gadue P., Huber T.L., Paddison P.J., Keller G.M. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16806-16811.
18. Galceran J., Farinas I., Depew M.J., Clevers H., Grosschedl R. Wnt3a-/--like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 1999, 13:709-717.
19. Gao Z., Ure K., Ables J.L., Lagace D.C., Nave K.A., Goebbels S., Eisch A.J., Hsieh J. Neurod1 is essential for the survival and maturation of adult-born neurons. Nat. Neurosci. 2009, 12:1090-1092.
20. Gaulden J., Reiter J.F. Neur-ons and neur-offs: regulators of neural induction in vertebrate embryos and embryonic stem cells. Hum. Mol. Genet. 2008, 17:R60-R66.
21. Gratsch T.E., DeBoer L.S., O'Shea K.S. RNA inhibition of BMP-4 gene expression in postimplantation mouse embryos. Genesis 2003, 37:12-17.
22. Haegel H., Larue L., Ohsugi M., Fedorov L., Herrenknecht K., Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development 1995, 121:3529-3537.
23. Haegele L., Ingold B., Naumann H., Tabatabal G., Ledermann B., Brandner S. Wnt signaling inhibits neural differentiation of embryonic stem cells by controlling bone morphogenetic protein expression. Mol. Cell. Neurosci. 2003, 24:696-708.
24. Hao J., Li T.G., Qi X., Zhao D.F., Zhao G.Q. WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev. Biol. 2006, 290:81-91.
25. Hirabayashi Y., Itoh Y., Tabata H., Nakajima K., Akiyama T., Masuyama N., Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004, 131:2791-2801.
26. Horn Z., Papachristou P., Shariatmadari M., Peyronnet J., Eriksson B., Ringstedt T. Wnt7a overexpression delays beta-tubulin III expression in transgenic mouse embryos. Brain Res. 2007, 1130:67-72.
27. Houart C., Caneparo L., Heisenberg C., Barth K., Take-Uchi M., Wilson S. Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling. Neuron 2002, 35:255-265.
28. Huelsken J., Vogel R., Brinkmann V., Erdmann B., Birchmeier C., Birchmeier W. Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 2000, 148:567-578.
29. Hughes T.A., Brady H.J. Regulation of axin2 expression at the levels of transcription, translation and protein stability in lung and colon cancer. Cancer Lett. 2006, 233:338-347.
30. Ishikawa T.O., Tamai Y., Li Q., Oshima M., Taketo M.M. Requirement for tumor suppressor Apc in the morphogenesis of anterior and ventral mouse embryo. Dev. Biol. 2003, 253:230-246.
31. Israsena N., Hu M., Fu W., Kan L., Kessler J.A. The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 2004, 268:220-231.
32. Jho E.H., Zhang T., Domon C., Joo C.K., Freund J.N., Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 2002, 22:1172-1183.
33. Kalani M.Y., Cheshier S.H., Cord B.J., Bababeygy S.R., Vogel H., Weissman I.L., Palmer T.D., Nusse R. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16970-16975.
34. Kelly O.G., Pinson K.I., Skarnes W.C. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004, 131:2803-2815.
35. Kelly K.F., Ng D.Y., Jayakumaran G., Wood G.A., Koide H., Doble B.W. Beta-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 2011, 8:214-227.
36. Kemler R., Hierholzer A., Kanzler B., Kuppig S., Hansen K., Taketo M.M., de Vries W.N., Knowles B.B., Solter D. Stabilization of beta-catenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 2004, 131:5817-5824.
37. Kolligs F.T., Hu G., Dang C.V., Fearon E.R. Neoplastic transformation of RK3E by mutant beta-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol. Cell. Biol. 1999, 19:5696-5706.
38. Kong X.B., Zhang C. Dickkopf (Dkk) 1 promotes the differentiation of mouse embryonic stem cells toward neuroectoderm. In Vitro Cell. Dev. Biol. Anim. 2009, 45:185-193.
39. Kuwabara T., Hsieh J., Muotri A., Yeo G., Warashina M., Lie D.C., Moore L., Nakashima K., Asashima M., Gage F.H. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat. Neurosci. 2009, 12:1097-1105.
40. Lagutin O.V., Zhu C.C., Kobayashi D., Topczewski J., Shimamura K., Puelles L., Russell H.R., McKinnon P.J., Solnica-Krezel L., Oliver G. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 2003, 17:368-379.
41. Lee M.Y., Lim H.W., Lee S.H., Han H.J. Smad, PI3K/Akt, and Wnt-dependent signaling pathways are involved in BMP-4-induced ESC self-renewal. Stem Cells 2009, 27:1858-1868.
42. Leung J.Y., Kolligs F.T., Wu R., Zhai Y., Kuick R., Hanash S., Cho K.R., Fearon E.R. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J. Biol. Chem. 2002, 277:21657-21665.
43. Li R., Liang J., Ni S., Zhou T., Qing X., Li H., He W., Chen J., Li F., Zhuang Q., Qin B., Xu J., Li W., Yang J., Gan Y., Qin D., Feng S., Song H., Yang D., Zhang B., Zeng L., Lai L., Miguel Esteban M.A., Pei D. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010, 7:51-63.
44. Lie D.C., Colamarino S.A., Song H.J., Desire L., Mira H., Consiglio A., Lein E.S., Jessberger S., Lansford H., Dearie A.R., Gage F.H. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005, 437:1370-1375.
45. Lindsley R.C., Gill J.G., Kyba M., Murphy T.L., Murphy K.M. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 2006, 133:3787-3796.
46. Linker C., Stern C.D. Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 2004, 131:5671-5681.
47. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 1999, 22:361-365.
48. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3299-3304.
49. 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, 78:7634-7638.
50. Masui S., Shimosato D., Toyooka Y., Yagi R., Takahashi K., Niwa H. An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic Acids Res. 2005, 33:e43.
51. Merrill B.J., Pasolli H.A., Polak L., Rendl M., Garcia-Garcia M.J., Anderson K.V., Fuchs E. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 2004, 131:263-274.
52. Miyabayashi T., Teo J.L., Yamamoto M., McMillan M., Nguyen C., Kahn M. Wnt/beta-catenin/CBP signaling maintains long-term murine embryonic stem cell pluripotency. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5668-5673.
53. Mohamed O.A., Clarke H.J., Dufort D. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev. Dyn. 2004, 231:416-424.
54. Muroyama Y., Fujihara M., Ikeya M., Kondoh H., Takada S. Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 2002, 16:548-553.
55. Nakanishi M., Kurisaki A., Hayashi Y., Warashina M., Ishiura S., Kusuda-Furue M., Asashima M. Directed induction of anterior and posterior primitive streak by Wnt from embryonic stem cells cultured in a chemically defined serum-free medium. FASEB J. 2009, 23:114-122.
56. Nordin N., Li M., Mason J.O. Expression profiles of Wnt genes during neural differentiation of mouse embryonic stem cells. Cloning Stem Cells 2008, 10:37-48.
57. Nordstrom U., Jessell T.M., Edlund T. Progressive induction of caudal neural character by graded Wnt signaling. Nat. Neurosci. 2002, 5:525-532.
58. Ogawa K., Nishinakamura R., Iwamatsu Y., Shimosato D., Niwa H. Synergistic action of Wnt and LIF in maintaining pluripotency of mouse ES cells. Biochem. Biophys. Res. Commun. 2006, 343:159-166.
59. Otero J.J., Fu W., Kan L., Cuadra A.E., Kessler J.A. Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development 2004, 131:3545-3557.
60. Paling N.R., Wheadon H., Bone H.K., Welham M.J. Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling. J. Biol. Chem. 2004, 279:48063-48070.
61. Pereira L., Yi F., Merrill B.J. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol. Cell. Biol. 2006, 26:7479-7491.
62. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
63. Popperl H., Schmidt C., Wilson V., Hume C.R., Dodd J., Krumlauf R., Beddington R.S. Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development 1997, 124:2997-3005.
64. Qi X., Li T.G., Hao J., Hu J., Wang J., Simmons H., Miura S., Mishina Y., Zhao G.Q. BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6027-6032.
65. Sato N., Meijer L., Skaltsounis L., Greengard P., Brivanlou A.H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 2004, 10:55-63.
66. Shimizu T., Kagawa T., Inoue T., Nonaka A., Takada S., Aburatani H., Taga T. Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol. Cell. Biol. 2008, 28:7427-7441.
67. Singla D.K., Schneider D.J., LeWinter M.M., Sobel B.E. wnt3a but not wnt11 supports self-renewal of embryonic stem cells. Biochem. Biophys. Res. Commun. 2006, 345:789-795.
68. Sinner D., Rankin S., Lee M., Zorn A.M. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 2004, 131:3069-3080.
69. Smith S.K., Charnock-Jones D.S., Sharkey A.M. The role of leukemia inhibitory factor and interleukin-6 in human reproduction. Hum. Reprod. 1998, 13(Suppl 3):237-243. discussion 244-6.
70. Takao Y., Yokota T., Koide H. Beta-catenin up-regulates Nanog expression through interaction with Oct-3/4 in embryonic stem cells. Biochem. Biophys. Res. Commun. 2007, 353:699-705.
71. Tam W.L., Lim C.Y., Han J., Zhang J., Ang Y.S., Ng H.H., Yang H., Lim B. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008, 26:2019-2031.
72. ten Berge D., Koole W., Fuerer C., Fish M., Eroglu E., Nusse R. Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 2008, 3:508-518.
73. Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker J.A., Warman M.L. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 2000, 29(52):54.
74. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 136:3205-3214.
75. Vanderhaeghen P. Wnts blow on NeuroD1 to promote adult neuron production and diversity. Nat. Neurosci. 2009, 12:1079-1081.
76. Verani R., Cappuccio I., Spinsanti P., Gradini R., Caruso A., Magnotti M.C., Motolese M., Nicoletti F., Melchiorri D. Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid. J. Neurochem. 2007, 100:242-250.
77. Watanabe S., Umehara H., Murayama K., Okabe M., Kimura T., Nakano T. Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene 2006, 25:2697-2707.
78. Wexler E.M., Paucer A., Kornblum H.I., Palmer T.D., Geschwind D.H. Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells 2009, 27:1130-1141.
79. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336:684-687.
80. Yamaguchi T.P., Takada S., Yoshikawa Y., Wu N., McMahon A.P. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 1999, 13:3185-3190.
81. Yan D., Wiesmann M., Rohan M., Chan V., Jefferson A.B., Guo L., Sakamoto D., Caothien R.H., Fuller J.H., Reinhard C., Garcia P.D., Randazzo F.M., Escobedo J., Fantl W.J., Williams L.T. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:14973-14978.
82. Yi F., Pereira L., Merrill B.J. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008, 26:1951-1960.
83. Ying Q.L., Stavridis M., Griffiths D., Li M., Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 2003, 21:183-186.
84. Yoshikawa Y., Fujimori T., McMahon A.P., Takada S. Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev. Biol. 1997, 183:234-242.
85. Yu H.M., Liu B., Costantini F., Hsu W. Impaired neural development caused by inducible expression of Axin in transgenic mice. Mech. Dev. 2007, 124:146-156.
86. Zechner D., Fujita Y., Hulsken J., Muller T., Walther I., Taketo M.M., Crenshaw E.B., Birchmeier W., Birchmeier C. Beta-catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 2003, 258:406-418.
87. Zechner D., Muller T., Wende H., Walther I., Taketo M.M., Crenshaw E.B., Treier M., Birchmeier W., Birchmeier C. Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev. Biol. 2007, 303:181-190.
88. Zeng L., Fagotto F., Zhang T., Hsu W., Vasicek T.J., Perry W.L., Lee J.J., Tilghman S.M., Gumbiner B.M., Costantini F. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 1997, 90:181-192.
89. Zhang K., Li L., Huang C., Shen C., Tan F., Xia C., Liu P., Rossant J., Jing N. Distinct functions of BMP4 during different stages of mouse ES cell neural commitment. Development 2010, 137:2095-2105.