β-catenin signaling is required for neural diffrerentiation of embryonic stem cells

Development

Volumn 131, Issue 15, 2004, Pages 3545-3557

  Otero, José Javier ^a   Fu, Weimin ^a   Kan, Lixin ^a   Cuadra, Adolfo E ^a   Kessler, John A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

catenin; Cell density; Embryonic stem cells; Neurogenesis; Retinoic acid; Tyrosine hydroxylase

Indexed keywords

BETA CATENIN; CELL MARKER; HOX PROTEIN; RETINOIC ACID; UVOMORULIN; WNT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COUNT; CELL CULTURE; CELL DENSITY; CELL LINEAGE; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INHIBITION KINETICS; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; BETA CATENIN; BIOLOGICAL MARKERS; CADHERINS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CYTOSKELETAL PROTEINS; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRETINOIN; WNT PROTEINS;

ARMADILLO;

EID: 4444361024     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01218     Document Type: Article

References (66)

1. Aberle, H., Schwartz, H. and Kemler, R. (1996). Cadherin-catenin complex, protein interactions and their implications for cadherin function. J. Cell Biochem. 61, 514-523.
2. Aubert, J., Dunstan, H., Chambers, I. and Smith, A. (2002). Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat. Biotech. 20, 1240-1245.
3. Bain, G., Kitchens, D., Yao, M., Huettner, J. E. and Gottlieb, D. I. (1995). Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
4. Baker, J. C., Beddington, R. S. and Harland, R. M. (1999). Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development. Genes Dev. 13, 3149-3159.
5. Bartlett, P. F., Brooker, G. J., Faux, C. H., Dutton, R., Murphy, M., Turnley, A. and Kilpatrick, T. J. (1998). Regulation of neural stem cell differentiation in the forebrain. Immunol. Cell Biol. 76, 414-418.
6. Brantjes, H., van Barker, N. E. J. and Clevers, H. (2002). TCF, Lady Justice casting the final Verdict on the outcome of Wnt signalling. Biol. Chem. 383, 255-261.
7. Brewer, G. J., Torricelli, J. R., Evege, E. K. and Price, P. J. (1993). Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
8. Brustle, O., Jones, K. N., Learish, R. D., Karram, K., Choudhary, K., Wiestler, O. D., Duncan, I. D. and McKay, R. D. (1999). Embryonic stem cell-derived glial precursors, a source of myelinating transplants. Science 285, 754-756.
9. Byers, S., Pishvaian, M., Crockett, C., Peer, C., Tozeren, A., Sporn, M., Anzano, M. and Lechleider, R. (1996). Retinoids increase cell-cell adhesion strength, beta-catenin protein stability, and localization to the cell membrane in a breast cancer cell line, a role for serine kinase activity. Endocrinology 137, 3265-3273.
10. Chazaud, C., Chambon, P. and Dolle, P. (1999). Retinoic acid is required in the mouse embryo for left-right asymmetry determination and heart morphogenesis. Development 126, 2589-2596.
11. Chen, U. and Mok, H. (1995). Development of mouse embryonic stem (ES) cells, IV. Differentiation to mature T and B lymphocytes after implantation of embryoid bodies into nude mice. Dev. Immunol. 4, 79-84.
12. Chenn, A. and Walsh, C. A. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
13. Cho, E. A. and Dressler, G. R. (1998). TCF-4 binds beta-catenin and is expressed in distinct regions of the embryonic brain and limbs. Mech. Dev. 77, 9-18.
14. Chung, S., Sonntag, K. C., Andersson, T., Bjorklund, L. M., Park, J. J., Kim, D. W., Kang, U. J., Isacson, O. and Kim, K. S. (2002). Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur. J. Neurosci. 16, 1829-1838.
15. Collins, M. D. and Mao, G. E. (1999). Teratology of retinoids. Annu. Rev. Pharmacol. Toxicol. 39, 399-430.
16. Dietrich, C., Scherwat, J., Faust, D. and Oesch, F. (2002). Subcellular localization of beta-catenin is regulated by cell density. Biochem. Biophys. Res. Commun. 292, 195-199.
17. Ding, S., Wu, T. Y., Brinker, A., Peters, E. C., Hur, W., Gray, N. S. and Schultz, P. G. (2003). Synthetic small molecules that control stem cell fate. Proc. Natl. Acad. Sci. USA 100, 7632-7637.
18. Dinsmore, J., Ratliff, J., Deacon, T., Pakzaban, P., Jacoby, D., Galpern, W. and Isacson, O. (1996). Embryonic stem cells differentiated in vitro as a novel source of cells for transplantation. Cell Transplant. 5, 131-143.
19. Dorsky, R. I., Moon, R. T. and Raible, D. W. (1998). Control of neural crest cell fate by the Wnt signalling pathway. Nature 396, 370-373.
20. Easwaran, V., Pishvaian, M., Salimuddin, X. and Byers, S. (1999). Cross-regulation of beta-catenin-LEF/TCF and retinoid signaling pathways. Curr. Biol. 9, 1415-1418.
21. Gratsch, T. E. and O'Shea, K. S. (2002). Noggin and chordin have distinct activities in promoting lineage commitment of mouse embryonic stem (ES) cells. Dev. Biol. 245, 83-94.
22. Gumbiner, B. M. and McCrea, P. D. (1993). Catenins as mediators of the cytoplasmic functions of cadherins. J. Cell Sci. Suppl. 17, 155-158.
23. Haegele, L., Ingold, B., Neumann, H., Tabatabai, G., Ledermann, B. and Brandner, S. (2003). Wnt signalling inhibits neural differentiation of embryonic stem cells by controlling bone morphogenetic protein expression. Mol. Cell. Neurosci. 24, 696-708.
24. Hsu, S. C., Galceran, J. and Grosschedl, R. (1998). Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with beta-catenin. Mol. Cell. Biol. 18, 4807-4818.
25. Ioffe, E., Liu, Y., Bhaumik, M., Poirier, F., Factor, S. M. and Stanley, P. (1995). WW6, an embryonic stem cell line with an inert genetic marker that can be traced in chimeras. Proc. Natl. Acad. Sci. USA 92, 7357-7361.
26. Israsena, N., Hu, M., Fu, W., Kan, L. and Kessler, J. A. (2004). The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220-231.
27. Jamora, C., DasGupta, R., Kocieniewski, P. and Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322.
28. Jin, E. J., Erickson, C. A., Takada, S. and Burrus, L. W. (2001). Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev. Biol. 233, 22-37.
29. Kang, D. E., Soriano, S., Xia, X., Eberhart, C. G., De Strooper, B., Zheng, H. and Koo, E. H. (2002). Presenilin couples the paired phosphorylation of beta-catenin independent of axin, implications for beta-catenin activation in tumorigenesis. Cell 110, 751-762.
30. Katoh, M. (2002). Regulation of WNT signaling molecules by retinoic acid during neuronal differentiation in NT2 cells, threshold model of WNT action. Int. J. Mol. Med. 10, 683-687.
31. Kawasaki, H., Mizuseki, K., Nishikawa, S., Kaneko, S., Kuwana, Y., Nakanishi, S., Nishikawa, S. I. and Sasai, Y. (2000). Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40.
32. Kielman, M. F., Rindapaa, M., Gaspar, C., van Poppel, N., Breukel, C., van Leeuwen, S., Taketo, M. M., Roberts, S., Smits, R. and Fodde, R. (2002). Apc modulates embryonic stem-cell differentiation by controlling the dosage of beta-catenin signaling. Nat. Genet. 32, 594-605.
33. Kikuchi, A. (1999). Roles of Axin in the Wnt signalling pathway. Cell Signal 11, 777-788.
34. Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J. et al. (2002). Identification of a Wnt/Dvl/beta-catenin→Pitx2 pathway mediating celltype-specific proliferation during development. Cell 111, 673-685.
35. Korswagen, H. C. (2002). Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans, variations on a common signaling theme. BioEssays 24, 801-810.
36. Kudoh, T., Wilson, S. W. and Dawid, I. B. (2002). Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development, 129, 4335-4346.
37. Kuhl, M. (2002). Non-canonical Wnt signaling in Xenopus, regulation of axis formation and gastrulation. Semin. Cell Dev. Biol. 13, 243-249.
38. Lickert, H. and Kemler, R. (2002). Functional analysis of cis-regulatory elements controlling initiation and maintenance of early Cdx1 gene expression in the mouse. Dev. Dyn. 225, 216-220.
39. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847.
40. Liu, S., Qu, Y., Stewart, T. J., Howard, M. J., Chakrabortty, S., Holekamp, T. F. and McDonald, J. W. (2000). Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl. Acad. Sci. USA 97, 6126-6131.
41. Lucas, J. J., Hernandez, F., Gomez-Ramos, P., Moran, M. A., Hen, R. and Avila, J. (2001). Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20, 27-39.
42. Lui, T., Lee, Y. N., Malbon, C. C. and Wang, H. Y. (2002). Activation of the beta-catenin/LEF-TCF pathway is obligate for formation of primitive endoderm by mouse F9 totipotent teratocarcinoma cells in response to retinoic acid. J. Biol. Chem. 277, 30887-30891.
43. Lyu, J., Costantini, F., Jho, E. H. and Joo, C. K. (2003). Ectopic expression of axin blocks neuronal differentiation of embryonic carcinoma p19 cells. J. Biol. Chem. 278, 13487-13495.
44. Martin, D. M., Skidmore, J. M., Fox, S. E., Gage, P. J. and Camper, S. A. (2002). Pitx2 distinguishes subtypes of terminally differentiated neurons in the developing mouse neuroepithelium. Dev. Biol. 252, 84-99.
45. McGrew, L. L., Takemaru, K., Bates, R. and Moon, R. T. (1999). Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway and a molecular screen for Wnt-responsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus. Mech. Dev. 87, 21-32.
46. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
47. Novak, A. and Dedhar, S. (1999). Signaling through beta-catenin and Lef/Tcf. Cell. Mol. Life Sci. 56, 523-537.
48. Pandur, P., Lasche, M., Eisenberg, L. M. and Kuhl, M. (2002a). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641.
49. Pandur, P., Maurus, D. and Kuhl, M. (2002b). Increasingly complex, New players enter the Wnt signaling network. BioEssays 24, 881-884.
50. Patapoutian, A. and Reichardt, L. F. (2000). Roles of Wnt proteins in neural development and maintenance. Curr. Opin. Neurobiol. 10, 392-399.
51. Peifer, M., Rauskolb, C., Williams, M., Riggleman, B. and Wieschaus, E. (1991). The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation. Development 111, 1029-1043.
52. Salic, A., Lee, E., Mayer, L. and Kirschner, M. W. (2000a). Control of beta-catenin stability, reconstitution of the cytoplasmic steps of the wnt pathway in Xenopus egg extracts. Mol. Cell 5, 523-532.
53. Salic, A., Lee, E., Mayer, L. and Kirschner, M. W. (2000b). Control of beta-catenin stability, reconstitution of the cytoplasmic steps of the wnt pathway in Xenopus egg extracts. Mol. Cell 5, 523-532.
54. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. and Brivanlou, A. H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nature Med. 10, 55-63.
55. Tada, M., Concha, M. L. and Heisenberg, C. P. (2002). Non-canonical Wnt signalling and regulation of gastrulation movements. Semin. Cell Dev. Biol. 13, 251-260.
56. Tropepe, V., Hitoshi, S., Sirard, C., Mak, T. W., Rossant, J. and van der Kooy, D. (2001). Direct neural fate specification from embryonic stem cells, a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30, 65-78.
57. Vaccarino, F. M., Schwartz, M. L., Raballo, R., Nilsen, J., Rhee, J., Zhou, M., Doetschman, T., Coffin, J. D., Wyland, J. J. and Hung, Y. T. (1999). Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 2, 246-253.
58. van de Wetering, M., Cavallo, R., Dooijes, D., van Beest, M., van Es, J., Loureiro, J., Ypma, A., Hursh, D., Jones, T. and Bejsovec, A. (1997). Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799.
59. Vizirianakis, I. S., Chen, Y. Q., Kantak, S. S., Tsiftsoglou, A. S. and Kramer, R. H. (2002). Dominant-negative E-cadherin alters adhesion and reverses contact inhibition of growth in breast carcinoma cells. Int. J. Oncol. 21, 135-144.
60. Vleminckx, K., Kemler, R. and Hecht, A. (1999). The C-terminal transactivation domain of beta-catenin is necessary and sufficient for signaling by the LEF-1/beta-catenin complex in Xenopus laevis. Mech. Dev. 81, 65-74.
61. Westmoreland, J. J., McEwen, J., Moore, B. A., Jin, Y. and Condie, B. G. (2001). Conserved function of Caenorhabditis elegans UNC-30 and mouse Pitx2 in controlling GABAergic neuron differentiation. J. Neurosci. 21, 6810-6819.
62. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S. and Nishida, E. (2002). JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3, 69-75.
63. Ying, Q. L., Stavridis, M., Griffiths, D., Li, M. and Smith, A. (2003). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186.
64. Zechner, D., Fujita, V., Hulsken, J., Muller, T., Walther, I., Taketo, M. M., Crenshaw, E. B., 3rd, Birchmeier, W. and Birchmeier, C. (2003). beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258, 406-418.
65. Zhu, A. J. and Watt, F. M. (1996). Expression of a dominant negative cadherin mutant inhibits proliferation and stimulates terminal differentiation of human epidermal keratinocytes. J. Cell Sci. 109, 3013-3023.
66. Zhu, G., Mehler, M. F., Zhao, J., Yu Yung, S. and Kessler, J. A. (1999). Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells. Dev. Biol. 215, 118-129.