β-catenin in pluripotency. Adhering to self-renewal or wnting to differentiate?

International Review of Cell and Molecular Biology

Volumn 312, Issue , 2014, Pages 53-78

  Sineva, Galina S ^a   Pospelov, Valery A ^a,b  

^a INSTITUTE OF CYTOLOGY   (Russian Federation)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Cadherin; Cell differentiation; Embryonic stem cells; Pluripotency; Tcf; Catenin

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; STAT3 PROTEIN; UVOMORULIN; CADHERIN; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL NUCLEUS; EMBRYONIC STEM CELL; ENZYME ACTIVITY; HUMAN; MEDIATOR; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN BINDING; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; WNT SIGNALING PATHWAY; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; BETA CATENIN; CADHERINS; CELL ADHESION; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LEUKEMIA INHIBITORY FACTOR; PLURIPOTENT STEM CELLS; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; WNT SIGNALING PATHWAY;

EID: 84913529067     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800178-3.00002-6     Document Type: Chapter

References (104)

1. Abramova M.V., Zatulovskiy E.A., Svetlikova S.B., Kukushkin A.N., Pospelov V.A. e2f1 gene is a new member of Wnt/β-catenin/Tcf-regulated genes. Biochem. Biophys. Res. Commun. 2010, 391:142-146.
2. Abu-Remaileh M., Gerson A., Farago M., Nathan G., Alkalay I., Zins Rousso S., Gur M., Fainsod A., Bergman Y. Oct-3/4 regulates stem cell identity and cell fate decisions by modulating Wnt/beta-catenin signalling. EMBO J. 2010, 29:3236-3248.
3. Anton R., Kestler H.A., Kuhl M. Beta-catenin signaling contributes to stemness and regulates early differentiation in murine embryonic stem cells. FEBS Lett. 2007, 581:5247-5254.
4. Atlasi Y., Noori R., Gaspar C., Franken P., Sacchetti A., Rafati H., Mahmoudi T., Decraene C., Calin G.A., Merrill B.J., Fodde R. Wnt signaling regulates the lineage differentiation potential of mouse embryonic stem cells through Tcf3 down-regulation. PLoS Genet. 2013, 9:e1003424.
5. Bedzhov I., Alotaibi H., Basilicata M.F., Ahlborn K., Liszewska E., Brabletz T., Stemmler M.P. Adhesion, but not a specific cadherin code, is indispensable for ES cell and induced pluripotency. Stem Cell Res. 2013, 11:1250-1263.
6. Blauwkamp T.A., Nigam S., Ardehali R., Weissman I.L., Nusse R. Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat. Commun. 2012, 3:1070.
7. Brautigam C., Raggioli A., Winter J. The Wnt/beta-catenin pathway regulates the expression of the miR-302 cluster in mouse ESCs and P19 cells. PLoS One 2013, 8:e75315.
8. Brembeck F.H., Schwarz-Romond T., Bakkers J., Wilhelm S., Hammerschmidt M., Birchmeier W. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev. 2004, 18:2225-2230.
9. Bryant D.M., Stow J.L. The ins and outs of E-cadherin trafficking. Trends Cell Biol. 2004, 14:427-434.
10. Cadigan K.M. TCFs and Wnt/beta-catenin signaling: more than one way to throw the switch. Curr. Top. Dev. Biol. 2012, 98:1-34.
11. Cadigan K.M., Waterman M.L. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb. Perspect. Biol. 2012, 4:a007906.
12. Chen Y., Blair K., Smith A. Robust self-renewal of rat embryonic stem cells requires fine-tuning of glycogen synthase kinase-3 inhibition. Stem Cell Rep. 2013, 1:209-217.
13. Cheng Y., Cheung A.K., Ko J.M., Phoon Y.P., Chiu P.M., Lo P.H., Waterman M.L., Lung M.L. Physiological beta-catenin signaling controls self-renewal networks and generation of stem-like cells from nasopharyngeal carcinoma. BMC Cell Biol. 2013, 14:44.
14. Choi S.H., Estaras C., Moresco J.J., Yates J.R., Jones K.A. Alpha-catenin interacts with APC to regulate beta-catenin proteolysis and transcriptional repression of Wnt target genes. Genes Dev. 2013, 27:2473-2488.
15. Chou Y.F., Chen H.H., Eijpe M., Yabuuchi A., Chenoweth J.G., Tesar P., Lu J., McKay R.D., Geijsen N. The growth factor environment defines distinct pluripotent ground states in novel blastocyst-derived stem cells. Cell 2008, 135:449-461.
16. Clevers H., Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012, 149:1192-1205.
17. Dalton S. Signaling networks in human pluripotent stem cells. Curr. Opin. Cell Biol. 2013, 25:241-246.
18. Daugherty R.L., Gottardi C.J. Phospho-regulation of beta-catenin adhesion and signaling functions. Physiology (Bethesda) 2007, 22:303-309.
19. Davidson K.C., Adams A.M., Goodson J.M., McDonald C.E., Potter J.C., Berndt J.D., Biechele T.L., Taylor R.J., Moon R.T. Wnt/beta-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc. Natl. Acad. Sci. U.S.A 2012, 109:4485-4490.
20. del Valle I., Rudloff S., Carles A., Li Y., Liszewska E., Vogt R., Kemler R. E-cadherin is required for the proper activation of the Lifr/Gp130 signaling pathway in mouse embryonic stem cells. Development 2013, 140:1684-1692.
21. Dravid G., Ye Z., Hammond H., Chen G., Pyle A., Donovan P., Yu X., Cheng L. Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 2005, 23:1489-1501.
22. Engert S., Burtscher I., Liao W.P., Dulev S., Schotta G., Lickert H. Wnt/beta-catenin signalling regulates Sox17 expression and is essential for organizer and endoderm formation in the mouse. Development 2013, 140:3128-3138.
23. Evans P.M., Chen X., Zhang W., Liu C. KLF4 interacts with beta-catenin/TCF4 and blocks p300/CBP recruitment by beta-catenin. Mol. Cell. Biol. 2010, 30:372-381.
24. Faunes F., Hayward P., Descalzo S.M., Chatterjee S.S., Balayo T., Trott J., Christoforou A., Ferrer-Vaquer A., Hadjantonakis A.K., Dasgupta R., Arias A.M. A membrane-associated beta-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells. Development 2013, 140:1171-1183.
25. Fernandez A., Huggins I.J., Perna L., Brafman D., Lu D., Yao S., Gaasterland T., Carson D.A., Willert K. The WNT receptor FZD7 is required for maintenance of the pluripotent state in human embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A 2014, 111:1409-1414.
26. Gardano L., Pucci F., Christian L., Le Bihan T., Harrington L. Telomeres, a busy platform for cell signaling. Front. Oncol. 2013, 3:146.
27. Gottardi C.J., Wong E., Gumbiner B.M. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J. Cell Biol. 2001, 153:1049-1060.
28. Groenendyk J., Michalak M. Disrupted WNT signaling in mouse embryonic stem cells in the absence of calreticulin. Stem Cell Rev. 2014, 10(2):191-206.
29. 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.
30. Hanna J.H., Saha K., Jaenisch R. Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 2010, 143:508-525.
31. 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.
32. Hawkins K., Mohamet L., Ritson S., Merry C.L., Ward C.M. E-cadherin and, in its absence, N-cadherin promotes Nanog expression in mouse embryonic stem cells via STAT3 phosphorylation. Stem Cells 2012, 30:1842-1851.
33. Hecht A., Kemler R. Curbing the nuclear activities of beta-catenin. Control over Wnt target gene expression. EMBO Rep. 2000, 1:24-28.
34. Heuberger J., Birchmeier W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb. Perspect. Biol. 2010, 2:a002915.
35. Hierholzer A., Kemler R. Beta-catenin-mediated signaling and cell adhesion in postgastrulation mouse embryos. Dev. Dyn. 2010, 239:191-199.
36. Hikasa H., Sokol S.Y. Phosphorylation of TCF proteins by homeodomain-interacting protein kinase 2. J. Biol. Chem. 2011, 286:12093-12100.
37. Hikasa H., Ezan J., Itoh K., Li X., Klymkowsky M.W., Sokol S.Y. Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev. Cell 2010, 19:521-532.
38. Hoffman J.A., Wu C.I., Merrill B.J. Tcf7l1 prepares epiblast cells in the gastrulating mouse embryo for lineage specification. Development 2013, 140:1665-1675.
39. Hoffmeyer K., Raggioli A., Rudloff S., Anton R., Hierholzer A., Del Valle I., Hein K., Vogt R., Kemler R. Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science 2012, 336:1549-1554.
40. Holland J.D., Klaus A., Garratt A.N., Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr. Opin. Cell Biol. 2013, 25:254-264.
41. 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.
42. Kan L., Israsena N., Zhang Z., Hu M., Zhao L.R., Jalali A., Sahni V., Kessler J.A. Sox1 acts through multiple independent pathways to promote neurogenesis. Dev. Biol. 2004, 269:580-594.
43. Kan N.G., Stemmler M.P., Junghans D., Kanzler B., de Vries W.N., Dominis M., Kemler R. Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm. Development 2007, 134:31-41.
44. 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.
45. Kim H., Wu J., Ye S., Tai C.I., Zhou X., Yan H., Li P., Pera M., Ying Q.L. Modulation of beta-catenin function maintains mouse epiblast stem cell and human embryonic stem cell self-renewal. Nat. Commun. 2013, 4:2403.
46. Kleber M., Sommer L. Wnt signaling and the regulation of stem cell function. Curr. Opin. Cell Biol. 2004, 16:681-687.
47. Kormish J.D., Sinner D., Zorn A.M. Interactions between SOX factors and Wnt/beta-catenin signaling in development and disease. Dev. Dyn. 2010, 239:56-68.
48. Krieghoff E., Behrens J., Mayr B. Nucleo-cytoplasmic distribution of beta-catenin is regulated by retention. J. Cell Sci. 2006, 119:1453-1463.
49. Kuhl S.J., Kuhl M. On the role of Wnt/beta-catenin signaling in stem cells. Biochim. Biophys. Acta 2013, 1830:2297-2306.
50. Labbe E., Letamendia A., Attisano L. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc. Natl. Acad. Sci. U.S.A 2000, 97:8358-8363.
51. Lako M., Lindsay S., Lincoln J., Cairns P.M., Armstrong L., Hole N. Characterisation of Wnt gene expression during the differentiation of murine embryonic stem cells in vitro: role of Wnt3 in enhancing haematopoietic differentiation. Mech. Dev. 2001, 103:49-59.
52. 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., 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.
53. Li Y., Yu W., Cooney A.J., Schwartz R.J., Liu Y. Brief report: Oct4 and canonical Wnt signaling regulate the cardiac lineage factor Mesp1 through a Tcf/Lef-Oct4 composite element. Stem Cells 2013, 31:1213-1217.
54. 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.
55. Lluis F., Pedone E., Pepe S., Cosma M.P. The Wnt/beta-catenin signaling pathway tips the balance between apoptosis and reprograming of cell fusion hybrids. Stem Cells 2010, 28:1940-1949.
56. Lluis F., Ombrato L., Pedone E., Pepe S., Merrill B.J., Cosma M.P. T-cell factor 3 (Tcf3) deletion increases somatic cell reprogramming by inducing epigenome modifications. Proc. Natl. Acad. Sci. U.S.A 2011, 108:11912-11917.
57. Luis T.C., Naber B.A., Roozen P.P., Brugman M.H., de Haas E.F., Ghazvini M., Fibbe W.E., van Dongen J.J., Fodde R., Staal F.J. Canonical wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem Cell 2011, 9:345-356.
58. Lyashenko N., Winter M., Migliorini D., Biechele T., Moon R.T., Hartmann C. Differential requirement for the dual functions of beta-catenin in embryonic stem cell self-renewal and germ layer formation. Nat. Cell Biol. 2011, 13:753-761.
59. Mahendram S., Kelly K.F., Paez-Parent S., Mahmood S., Polena E., Cooney A.J., Doble B.W. Ectopic gamma-catenin expression partially mimics the effects of stabilized beta-catenin on embryonic stem cell differentiation. PLoS One 2013, 8:e65320.
60. Martello G., Sugimoto T., Diamanti E., Joshi A., Hannah R., Ohtsuka S., Gottgens B., Niwa H., Smith A. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 2012, 11:491-504.
61. Meek S., Wei J., Sutherland L., Nilges B., Buehr M., Tomlinson S.R., Thomson A.J., Burdon T. Tuning of beta-catenin activity is required to stabilize self-renewal of rat embryonic stem cells. Stem Cells 2013, 31:2104-2115.
62. Miranda K.C., Khromykh T., Christy P., Le T.L., Gottardi C.J., Yap A.S., Stow J.L., Teasdale R.D. A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells. J. Biol. Chem. 2001, 276:22565-22572.
63. 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.
64. Nichols J., Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4:487-492.
65. Ohtsuka S., Nishikawa-Torikai S., Niwa H. E-cadherin promotes incorporation of mouse epiblast stem cells into normal development. PLoS One 2012, 7:e45220.
66. Okumura N., Akutsu H., Sugawara T., Miura T., Takezawa Y., Hosoda A., Yoshida K., Ichida J.K., Yamada M., Hamatani T., Kuji N., Miyado K., Yoshimura Y., Umezawa A. Beta-catenin functions pleiotropically in differentiation and tumorigenesis in mouse embryo-derived stem cells. PLoS One 2013, 8:e63265.
67. Osei-Sarfo K., Gudas L.J. Retinoic acid suppresses the canonical Wnt signaling pathway in embryonic stem cells and activates the noncanonical Wnt signaling pathway. Stem Cells 2014, 32(8):2061-2071.
68. 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.
69. Raggioli A., Junghans D., Rudloff S., Kemler R. Beta-catenin is vital for the integrity of mouse embryonic stem cells. PLoS ONE 2014, 9:e86691.
70. Redmer T., Diecke S., Grigoryan T., Quiroga-Negreira A., Birchmeier W., Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 2011, 12:720-726.
71. Saito-Diaz K., Chen T.W., Wang X., Thorne C.A., Wallace H.A., Page-McCaw A., Lee E. The way Wnt works: components and mechanism. Growth Factors 2013, 31:1-31.
72. Samavarchi-Tehrani P., Golipour A., David L., Sung H.K., Beyer T.A., Datti A., Woltjen K., Nagy A., Wrana J.L. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010, 7:64-77.
73. 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.
74. Sawa H. Control of cell polarity and asymmetric division in C. elegans. Curr. Top. Dev. Biol. 2012, 101:55-76.
75. Schmitz Y., Rateitschak K., Wolkenhauer O. Analysing the impact of nucleo-cytoplasmic shuttling of beta-catenin and its antagonists APC, Axin and GSK3 on Wnt/beta-catenin signalling. Cell. Signal. 2013, 25:2210-2221.
76. Seidensticker M.J., Behrens J. Biochemical interactions in the wnt pathway. Biochim. Biophys. Acta 2000, 1495:168-182.
77. Seo E., Basu-Roy U., Zavadil J., Basilico C., Mansukhani A. Distinct functions of Sox2 control self-renewal and differentiation in the osteoblast lineage. Mol. Cell. Biol. 2011, 31:4593-4608.
78. Shy B.R., Wu C.I., Khramtsova G.F., Zhang J.Y., Olopade O.I., Goss K.H., Merrill B.J. Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt/beta-catenin signaling. Cell Rep. 2013, 4:1-9.
79. Sineva G.S., Pospelov V.A. Inhibition of GSK3beta enhances both adhesive and signalling activities of beta-catenin in mouse embryonic stem cells. Biol. Cell. 2010, 102:549-560.
80. Sineva G.S., Cherepkova M.Y., Pospelov V.A. Wnt, MEK/ERK and mTOR signaling pathways interaction in mouse embryonic stem cells. 38th FEBS Congress. FEBS J. 2013, 280(Issue supplement S1):452-453.
81. Singh A.M., Bechard M., Smith K., Dalton S. Reconciling the different roles of Gsk3beta in "naive" and "primed" pluripotent stem cells. Cell Cycle 2012, 11:2991-2996.
82. Soncin F., Mohamet L., Eckardt D., Ritson S., Eastham A.M., Bobola N., Russell A., Davies S., Kemler R., Merry C.L., Ward C.M. Abrogation of E-cadherin-mediated cell-cell contact in mouse embryonic stem cells results in reversible LIF-independent self-renewal. Stem Cells 2009, 27:2069-2080.
83. Soncin F., Mohamet L., Ritson S., Hawkins K., Bobola N., Zeef L., Merry C.L., Ward C.M. E-cadherin acts as a regulator of transcripts associated with a wide range of cellular processes in mouse embryonic stem cells. PLoS One 2011, 6:e21463.
84. Stamos J.L., Weis W.I. The beta-catenin destruction complex. Cold Spring Harb. Perspect. Biol. 2013, 5:a007898.
85. Stepniak E., Radice G.L., Vasioukhin V. Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb. Perspect. Biol. 2009, 1:a002949.
86. Sumi T., Tsuneyoshi N., Nakatsuji N., Suemori H. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 2008, 135:2969-2979.
87. Sumi T., Oki S., Kitajima K., Meno C. Epiblast ground state is controlled by canonical Wnt/beta-catenin signaling in the postimplantation mouse embryo and epiblast stem cells. PLoS ONE 2013, 8:e63378.
88. Suvorova I.I., Katolikova N.V., Pospelov V.A. New insights into cell cycle regulation and DNA damage response in embryonic stem cells. Int. Rev. Cell Mol. Biol. 2012, 299:161-198.
89. 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.
90. 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.
91. Tarafdar A., Dobbin E., Corrigan P., Freeburn R., Wheadon H. Canonical Wnt signaling promotes early hematopoietic progenitor formation and erythroid specification during embryonic stem cell differentiation. PLoS One 2013, 8:e81030.
92. Trott J., Martinez Arias A. Single cell lineage analysis of mouse embryonic stem cells at the exit from pluripotency. Biol. Open 2013, 2:1049-1056.
93. Ueno S., Weidinger G., Osugi T., Kohn A.D., Golob J.L., Pabon L., Reinecke H., Moon R.T., Murry C.E. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A 2007, 104:9685-9690.
94. Ullmann U., Gilles C., De Rycke M., Van de Velde H., Sermon K., Liebaers I. GSK-3-specific inhibitor-supplemented hESC medium prevents the epithelial-mesenchymal transition process and the up-regulation of matrix metalloproteinases in hESCs cultured in feeder-free conditions. Mol. Hum. Reprod. 2008, 14:169-179.
95. Wang J., Sinha T., Wynshaw-Boris A. Wnt signaling in mammalian development: lessons from mouse genetics. Cold Spring Harb. Perspect. Biol. 2012, 4:a007963.
96. Widelitz R. Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 2005, 23:111-116.
97. Willert K., Jones K.A. Wnt signaling: is the party in the nucleus?. Genes Dev. 2006, 20:1394-1404.
98. Wray J., Kalkan T., Gomez-Lopez S., Eckardt D., Cook A., Kemler R., Smith A. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat. Cell Biol. 2011, 13:838-845.
99. Wu C.I., Hoffman J.A., Shy B.R., Ford E.M., Fuchs E., Nguyen H., Merrill B.J. Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 2012, 139:2118-2129.
100. 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.
101. Yi F., Pereira L., Hoffman J.A., Shy B.R., Yuen C.M., Liu D.R., Merrill B.J. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 2011, 13:762-770.
102. Ying Q.L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
103. Zhang W., Chen X., Kato Y., Evans P.M., Yuan S., Yang J., Rychahou P.G., Yang V.W., He X., Evers B.M., Liu C. Novel cross talk of Kruppel-like factor 4 and beta-catenin regulates normal intestinal homeostasis and tumor repression. Mol. Cell. Biol. 2006, 26:2055-2064.
104. Zhang X., Peterson K.A., Liu X.S., McMahon A.P., Ohba S. Gene regulatory networks mediating canonical Wnt signal directed control of pluripotency and differentiation in embryo stem cells. Stem Cells 2013, 31(12):2667-2679.