Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation

Nature Cell Biology

Volumn 13, Issue 7, 2011, Pages 838-845

  Wray, Jason ^a,d   Kalkan, Tüzer ^a   Gomez Lopez, Sandra ^a,d,e   Eckardt, Dominik ^b,d,f   Cook, Andrew ^c   Kemler, Rolf ^b   Smith, Austin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c P zer Ltd   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^f MILTENYI BIOTEC GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; TRANSCRIPTION FACTOR 7 LIKE 1;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL METABOLISM; CELL RENEWAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME INHIBITION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GLYCOGEN SYNTHASE KINASE 3; MICE; PLURIPOTENT STEM CELLS; PROTEIN KINASE INHIBITORS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TRANSFECTION;

RODENTIA;

EID: 79959950773     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2267     Document Type: Article

References (41)

1. 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. 10, 55-63 (2004). (Pubitemid 38524699)
2. Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature 453, 519-523 (2008).
3. Cartwright, P. et al. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132, 885-896 (2005). (Pubitemid 40484924)
4. Doble, B. W. & Woodgett, J. R. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186 (2003). (Pubitemid 36410657)
5. Hsu, S. C., Galceran, J. & Grosschedl, R. Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with α-catenin. Mol. Cell Biol. 18, 4807-4818 (1998). (Pubitemid 28343065)
6. 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. 22, 746-755 (2008). (Pubitemid 351439106)
7. Clevers, H. Wnt/ α-catenin signaling in development and disease. Cell 127, 469-480 (2006). (Pubitemid 44647433)
8. Behrens, J. et al. Functional interaction of α-catenin with the transcription factor LEF-1. Nature 382, 638-642 (1996). (Pubitemid 26268958)
9. Molenaar, M. et al. XTcf-3 transcription factor mediates η-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399 (1996). (Pubitemid 26272079)
10. van de Wetering, M. et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799 (1997).
11. Aberle, H., Bauer, A., Stappert, J., Kispert, A. & Kemler, R. α-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804 (1997).
12. Rubinfeld, B. et al. Binding of GSK3+ to the APC- α-catenin complex and regulation of complex assembly. Science 272, 1023-1026 (1996). (Pubitemid 26259322)
13. Hanna, J. et al. Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 4, 513-524 (2009).
14. 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. 343, 159-166 (2006).
15. Matsuda, T. et al. STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J. 18, 4261-4269 (1999). (Pubitemid 29364128)
16. Niwa, H., Burdon, T., Chambers, I. & Smith, A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 12, 2048-2060 (1998). (Pubitemid 28323878)
17. Burdon, T., Stracey, C., Chambers, I., Nichols, J. & Smith, A. Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol. 210, 30-43 (1999). (Pubitemid 29275085)
18. Pereira, L., Yi, F. & Merrill, B. J. Repression of nanog gene transcription by tcf3 limits embryonic stem cell self-renewal. Mol. Cell Biol. 26, 7479-7491 (2006). (Pubitemid 44547699)
19. Guo, G., Huang, Y., Humphreys, P., Wang, X. & Smith, A. A PiggyBac-based recessive screening method to identify pluripotency regulators. PLoS One 18, e18189 (2011).
20. Haegel, H. et al. Lack of α-catenin affects mouse development at gastrulation. Development 121, 3529-3537 (1995). (Pubitemid 3000446)
21. Huelsken, J. et al. Requirement for α-catenin in anterior fiposterior axis formation in mice. J. Cell Biol. 148, 567-578 (2000).
22. 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 115, 281-292 (2003). (Pubitemid 37487702)
23. Bain, J. et al. The selectivity of protein kinase inhibitors; a further update. Biochem. J. 408, 297-315 (2007).
24. Doble, B. W., Patel, S., Wood, G. A., Kockeritz, L. K. & Woodgett, J. R. Functional redundancy of GSK-3+ and GSK-3+ in Wnt/ α-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12, 957-971 (2007). (Pubitemid 46805920)
25. Lyashenko, N. et al. Differential requirement for the dual functions of α-catenin in embryonic stem cell self-renewal and germ layer formation. Nat. Cell Biol. 13, 753-761 (2011).
26. Brons, I. G. et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195 (2007). (Pubitemid 47067373)
27. Tesar, P. J. et al. New cell lines from mouse epiblast share Defining features with human embryonic stem cells. Nature 448, 196-199 (2007). (Pubitemid 47067378)
28. Guo, G. et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069 (2009).
29. Soncin, F. et al. Abrogation of E-cadherin mediated cell of cell contact in mouse embryonic stem cells results in reversible LIF-independent self-renewal. Stem Cells 27, 2069-2080 (2009).
30. Anton, R., Kestler, H. A. & Kuhl, M. α-catenin signaling contributes to stemness and regulates early differentiation in murine embryonic stem cells. FEBS Lett. 581, 5247-5254 (2007). (Pubitemid 350018750)
31. Arnold, S. J. et al. Brachyury is a target gene of the Wnt/ α-catenin signaling pathway. Mech. Dev. 91, 249-258 (2000). (Pubitemid 30125923)
32. Wray, J., Kalkan, T. & Smith, A. G. The ground state of pluripotency. Biochem. Soc. Trans. 38, 1027-1032 (2010).
33. Li, X. et al. Generation of destabilized green fiuorescent protein as a transcription reporter. J. Biol. Chem. 273, 34970-34975 (1998). (Pubitemid 29028195)
34. Toyooka, Y., Shimosato, D., Murakami, K., Takahashi, K. & Niwa, H. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135, 909-918 (2008). (Pubitemid 351524145)
35. Robson, P., Stein, P., Zhou, B., Schultz, R. M. & Baldwin, H. S. Inner cell mass-specific expression of a cell adhesion molecule (PECAM-1/CD31) in the mouse blastocyst. Dev. Biol. 234, 317-329 (2001). (Pubitemid 32552661)
36. 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 26, 1951-1960 (2008).
37. Tam, W. L. et al. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 26, 2019-2031 (2008).
38. Kelly, K. F. et al. α-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 8, 214-227 (2011).
39. Moon, R. T. & Kimelman, D. From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. Bioessays 20, 536-545 (1998). (Pubitemid 28362299)
40. ten Berge, D. et al. Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3, 508-518 (2008).
41. Brault, V. et al. Inactivation of the α-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (2001). (Pubitemid 32409648)