Wnt some lose some: Transcriptional governance of stem cells by Wnt/β-catenin signaling

Genes and Development

Volumn 28, Issue 14, 2014, Pages 1517-1532

  Lien, Wen Hui ^a   Fuchs, Elaine ^b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

LEF TCF; Stem cells; Wnt signaling; catenin

Indexed keywords

LEF/TCF; STEM CELLS; WNT SIGNALING; Β-CATENIN;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

EID: 84904314069     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.244772.114     Document Type: Review

References (177)

1. Ahumada A, Slusarski DC, Liu X, Moon RT, Malbon CC, Wang HY. 2002. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298: 2006-2010.
2. Allen TD, Potten CS. 1974. Fine-structural identification and organization of the epidermal proliferative unit. J Cell Sci 15: 291-319.
3. Andl T, Reddy ST, Gaddapara T, Millar SE. 2002. WNT signals are required for the initiation of hair follicle development. Dev Cell 2: 643-653.
4. Andreu P, Colnot S, Godard C, Gad S, Chafey P, Niwa-Kawakita M, Laurent-Puig P, Kahn A, Robine S, Perret C, et al. 2005. Cryptrestricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development 132: 1443-1451.
5. Andreu P, Peignon G, Slomianny C, Taketo MM, Colnot S, Robine S, Lamarque D, Laurent-Puig P, Perret C, Romagnolo B. 2008. A genetic study of the role of the Wnt/β-catenin signalling in Paneth cell differentiation. Dev Biol 324: 288-296.
6. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, Dupont S, Piccolo S. 2013. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell sore N. *Dupont S.*Piccolo S
7. Arce L, Pate KT, Waterman ML. 2009. Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer 9: 159.
8. Atlasi Y, Looijenga L, Fodde R. 2014. Cancer Stem cells, pluripotency, and cellular heterogeneity: a WNTer perspective. Curr Top Dev Biol 107: 373-404.
9. Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N. 1998. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev 12: 2610-2622.
10. Azzolin L, Zanconato F, Bresolin S, Forcato M, Basso G, Bicciato S, Cordenonsi M, Piccolo S. 2012. Role of TAZ as mediator of Wnt signaling. Cell 151: 1443-1456.
11. Azzolin L, Panciera T, Soligo S, Enzo E, Bicciato S, Dupont S, Bresolin S, FrassonC, Basso G, GuzzardoV, et al. 2014. YAP/TAZ incorporation in the β-catenin destruction complex orchestrates theWnt response. Cell doi: 10.1016/j.cell.2014.06.013.
12. Bakre MM, Hoi A, Mong JC, Koh YY, Wong KY, Stanton LW. 2007. Generation of multipotential mesendodermal progenitors from mouse embryonic stem cells via sustained Wnt pathway activation. J Biol Chem 282: 31703-31712.
13. Barker N, Hurlstone A, Musisi H, Miles A, Bienz M, Clevers H. 2001. The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J 20: 4935-4943.
14. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
15. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382: 638-642.
16. Beronja S, Janki P, Heller E, Lien WH, Keyes BE, Oshimori N, Fuchs E. 2013. RNAi screens in mice identify physiological regulators of oncogenic growth. Nature 501: 185-190.
17. Bickenbach JR, Holbrook KA. 1987. Label-retaining cells in human embryonic and fetal epidermis. J Invest Dermatol 88: 42-46.
18. Blanpain C, Fuchs E. 2009. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 10: 207-217.
19. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E. 2004. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648.
20. Blauwkamp TA, Nigam S, Ardehali R, Weissman IL, Nusse R. 2012. Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 3: 1070.
21. Boj SF, van Es JH, Huch M, Li VS, Jose A, Hatzis P, Mokry M, Haegebarth A, van den Born M, Chambon P, et al. 2012. Diabetes risk gene and Wnt effector Tcf7l2/TCF4 controls hepatic response to perinatal and adult metabolic demand. Cell 151: 1595-1607.
22. Bottomly D, Kyler SL, McWeeney SK, Yochum GS. 2010. Identification of β-catenin binding regions in colon cancer cells using ChIP-Seq. Nucleic Acids Res 38: 5735-5745.
23. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
24. Brantjes H, Roose J, van De Wetering M, Clevers H. 2001. All Tcf HMG box transcription factors interact with Grouchorelated co-repressors. Nucleic Acids Res 29: 1410-1419.
25. Brunner E, Peter O, Schweizer L, Basler K. 1997. pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385: 829-833.
26. Buczacki SJ, Zecchini HI, Nicholson AM, Russell R, Vermeulen L, Kemp R, Winton DJ. 2013. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495: 65-69.
27. Cadigan KM, Waterman ML. 2012. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol 4: a007906.
28. Cavallo RA, Cox RT, MolineMM, Roose J, Polevoy GA, Clevers H, Peifer M, Bejsovec A. 1998. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395: 604-608.
29. Chan EF, Gat U, McNiff JM, Fuchs E. 1999. A common human skin tumour is caused by activating mutations in β-catenin. Nat Genet 21: 410-413.
30. Chen G, Fernandez J, Mische S, Courey AJ. 1999. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev 13: 2218-2230.
31. Chodaparambil JV, Pate KT, Hepler MR, Tsai BP, Muthurajan UM, Luger K, Waterman ML, Weis WI. 2014. Molecular functions of the TLE tetramerization domain in Wnt target gene repression. EMBO J 33: 719-731.
32. Choi YS, Zhang Y, Xu M, Yang Y, Ito M, Peng T, Cui Z, Nagy A, Hadjantonakis AK, Lang RA, et al. 2013. Distinct functions for Wnt/β-catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell 13: 720-733.
33. Ciarapica R, Methot L, Tang Y, Lo R, Dali R, Buscarlet M, Locatelli F, del Sal G, Rota R, Stifani S. 2014. Prolyl isomerase Pin1 and protein kinase HIPK2 cooperate to promote cortical neurogenesis by suppressing Groucho/TLE:Hes1-mediated inhibition of neuronal differentiation. Cell Death Differ 21: 321-332.
34. Clayton E, Doupe DP, Klein AM, Winton DJ, Simons BD, Jones PH. 2007. A single type of progenitor cell maintains normal epidermis. Nature 446: 185-189.
35. Clevers H. 2011. The cancer stem cell: premises, promises and challenges. Nat Med 17: 313-319.
36. Clevers H, Nusse R. 2012. Wnt/β-catenin signaling and disease. Cell 149: 1192-1205.
37. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. 2008. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 22: 746-755.
38. Cuilliere-Dartigues P, El-Bchiri J, Krimi A, Buhard O, Fontanges P, Flejou JF, Hamelin R, Duval A. 2006. TCF-4 isoforms absent in TCF-4 mutated MSI-H colorectal cancer cells colocalize with nuclear CtBP and repress TCF-4-mediated transcription. Oncogene 25: 4441-4448.
39. Daniels DL, WeisWI. 2005. β-Catenin directly displaces Groucho/ TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 12: 364-371.
40. DasGupta R, Fuchs E. 1999. Multiple roles for activated LEF/ TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
41. Davidson KC, Adams AM, Goodson JM, McDonald CE, Potter JC, Berndt JD, Biechele TL, Taylor RJ, Moon RT. 2012. Wnt/ β-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc Natl Acad Sci 109: 4485-4490.
42. de la Roche M, Bienz M. 2007. Wingless-independent association of Pygopus with dTCF target genes. Curr Biol 17: 556-561.
43. Deschene ER, Myung P, Rompolas P, Zito G, Sun TY, Taketo MM, Saotome I, Greco V. 2014. β-Catenin activation regulates tissue growth non-cell autonomously in the hair stem cell niche. Science 343: 1353-1356.
44. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. 2012. Defining the mode of tumour growth by clonal analysis. Nature 488: 527-530.
45. Florian MC, Nattamai KJ, Dorr K, Marka G, Uberle B, Vas V, Eckl C, Andra I, Schiemann M, Oostendorp RA, et al. 2013. A canonical to non-canonical Wnt signalling switch in haematopoietic stem-cell ageing. Nature 503: 392-396.
46. Gat U, DasGupta R, Degenstein L, Fuchs E. 1998. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell 95: 605-614.
47. Giese K, Amsterdam A, Grosschedl R. 1991. DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev 5: 2567-2578.
48. Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C, Niehrs C. 1998. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391: 357-362.
49. Grbavec D, Lo R, Liu Y, Stifani S. 1998. Transducin-like Enhancer of split 2, a mammalian homologue of Drosophila Groucho, acts as a transcriptional repressor, interacts with Hairy/Enhancer of split proteins, and is expressed during neuronal development. Eur J Biochem 258: 339-349.
50. Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Stokes N, Dela Cruz-Racelis J, Fuchs E. 2009. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4: 155-169.
51. Green H. 1991. Cultured cells for the treatment of disease. Sci Am 265: 96-102.
52. Gregorieff A, Pinto D, Begthel H, Destree O, Kielman M, Clevers H. 2005. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 129: 626-638.
53. Gu B, Watanabe K, Sun P, Fallahi M, Dai X. 2013. Chromatin effector Pygo2 mediates Wnt-notch crosstalk to suppress luminal/alveolar potential of mammary stem and basal cells. Cell Stem Cell 13: 48-61.
54. Habib SJ, Chen BC, Tsai FC, Anastassiadis K, Meyer T, Betzig E, Nusse R. 2013. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339: 1445-1448.
55. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R et al. 1999. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol 9: 207-210.
56. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, et al. 2004. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-β-catenin signaling. Nat Genet 36: 1117-1121.
57. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF. 2011. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332: 458-461.
58. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R. 2000. The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO J 19: 1839-1850.
59. Hikasa H, Sokol SY. 2011. Phosphorylation of TCF proteins by homeodomain-interacting protein kinase 2. J Biol Chem 286: 12093-12100.
60. Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY. 2010. Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 19: 521-532.
61. Ho R, Papp B, Hoffman JA, Merrill BJ, Plath K. 2013. Stagespecific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and T cell factor proteins. Cell Reports 3: 2113-2126.
62. Hoffmans R, Basler K. 2004. Identification and in vivo role of the Armadillo-Legless interaction. Development 131: 4393-4400.
63. Holland JD, Klaus A, Garratt AN, Birchmeier W. 2013. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol 25: 254-264.
64. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E. 2008. NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132: 299-310.
65. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB, Nathans J. 1999. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 398: 431-436.
66. Hsu SC, Galceran J, Grosschedl R. 1998. Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with β-catenin. Mol Cell Biol 18: 4807-4818.
67. Hsu YC, Pasolli HA, Fuchs E. 2011. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144: 92-105.
68. Hsu YC, Li L, Fuchs E. 2014. Transit-amplifying cells orchestrate stem cell activity and tissue regeneration. Cell 157: 935-949.
69. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. 1996. Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech Dev 59: 3-10.
70. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W. 2001. β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105: 533-545.
71. Hulsken J, Birchmeier W, Behrens J. 1994. E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J Cell Biol 127: 2061-2069.
72. Hurlstone A, Clevers H. 2002. T-cell factors: turn-ons and turnoffs. EMBO J 21: 2303-2311.
73. Imajo M, Miyatake K, Iimura A, Miyamoto A, Nishida E. 2012. A molecular mechanism that links Hippo signalling to the inhibition of Wnt/β-catenin signalling. EMBO J 31: 1109-1122.
74. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ, Winton DJ. 2004. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of β-catenin. Gastroenterology 126: 1236-1246.
75. 2+ pathway to antagonize Wnt/β-catenin signaling. Mol Cell Biol 23: 131-139.
76. Jones PH, Harper S, Watt FM. 1995. Stem cell patterning and fate in human epidermis. Cell 80: 83-93.
77. Keyes BE, Segal JP, Heller E, Lien WH, Chang CY, Guo X, Oristian DS, Zheng D, Fuchs E. 2013. Nfatc1 orchestrates aging in hair follicle stem cells. Proc Natl Acad Sci 110:E4950-E4959.
78. Klingensmith J, Nusse R, Perrimon N. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev 8: 118-130.
79. Kohn AD, Moon RT. 2005. Wnt and calcium signaling: β-cateninindependent pathways. Cell Calcium 38: 439-446.
80. _/_ colon carcinoma. Science 275: 1784-1787.
81. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. 1998. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383.
82. Kramps T, Peter O, Brunner E, Nellen D, Froesch B, Chatterjee S, Murone M, Zullig S, Basler K. 2002. Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex. Cell 109: 47-60.
83. 2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 16: 279-283.
84. 2+ signaling. Mech Dev 106: 61-76.
85. Lavker RM, Sun TT. 1982. Heterogeneity in epidermal basal keratinocytes: morphological and functional correlations. Science 215: 1239-1241.
86. Lechler T, Fuchs E. 2005. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437: 275-280.
87. Lee E, Salic A, Kruger R, Heinrich R, Kirschner MW. 2003. The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 1: E10.
88. Lee E, Madar A, David G, Garabedian MJ, Dasgupta R, Logan SK. 2013. Inhibition of androgen receptor and β-catenin activity in prostate cancer. Proc Natl Acad Sci 110: 15710-15715.
89. Le Grand F, Jones AE, Seale V, Scime A, Rudnicki MA. 2009. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4: 535-547.
90. Li B, Rheaume C, Teng A, Bilanchone V, Munguia JE, Hu M, Jessen S, Piccolo S, Waterman ML, Dai X. 2007. Developmental phenotypes and reduced Wnt signaling in mice deficient for pygopus 2. Genesis 45: 318-325.
91. Lien WH, Polak L, Lin M, Lay K, Zheng D, Fuchs E. 2014. In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators. Nat Cell Biol 16: 179-190.
92. Lim X, Tan SH, Koh WL, Chau RM, Yan KS, Kuo CJ, van Amerongen R, Klein AM, Nusse R. 2013. Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling. Science 342: 1226-1230.
93. Lindsley RC, Gill JG, Kyba M, Murphy TL, Murphy KM. 2006. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133: 3787-3796.
94. Liu C, Kato Y, Zhang Z, Do VM, Yankner BA, He X. 1999a. β-Trcp couples β-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc Natl Acad Sci 96: 6273-6278.
95. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999b. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365.
96. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837-847.
97. Liu Y, Rubin B, Bodine PV, Billiard J. 2008. Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J Cell Biochem 105: 497-502.
98. Liu XH, Wu Y, Yao S, Levine AC, Kirschenbaum A, Collier L, Bauman WA, Cardozo CP. 2013. Androgens up-regulate transcription of the Notch inhibitor Numb in C2C12 myoblasts via Wnt/β-catenin signaling to T cell factor elements in the Numb promoter. J Biol Chem 288: 17990-17998.
99. Lluis F, Pedone E, Pepe S, Cosma MP. 2008. Periodic activation of Wnt/β-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 3: 493-507.
100. Lluis F, Ombrato L, Pedone E, Pepe S, Merrill BJ, Cosma MP. 2011. T-cell factor 3 (Tcf3) deletion increases somatic cell reprogramming by inducing epigenome modifications. Proc Natl Acad Sci 108: 11912-11917.
101. Lyashenko N, Winter M, Migliorini D, Biechele T, Moon RT, Hartmann C. 2011. Differential requirement for the dual functions of β-catenin in embryonic stem cell self-renewal and germ layer formation. Nat Cell Biol 13: 753-761.
102. 2+ non-canonical pathway. J Biol Chem 282: 28980-28990.
103. Mahmoudi T, Boj SF, Hatzis P, Li VS, Taouatas N, Vries RG, Teunissen H, Begthel H, Korving J, Mohammed S, et al. 2010. The leukemia-associated Mllt10/Af10-Dot1l are Tcf4/βcatenin coactivators essential for intestinal homeostasis. PLoS Biol 8: e1000539.
104. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, et al. 2008. Cutaneous cancer stem cell maintenance is dependent on β-catenin signalling. Nature 452: 650-653.
105. Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA, Jaenisch R. 2008. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 3: 132-135.
106. Mascre G, Dekoninck S, Drogat B, Youssef KK, Brohee S, Sotiropoulou PA, Simons BD, Blanpain C. 2012. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489: 257-262.
107. Merrill BJ. 2012. Wnt pathway regulation of embryonic stem cell self-renewal. Cold Spring Harb Perspect Biol 4: a007971.
108. Merrill BJ, Gat U, DasGupta R, Fuchs E. 2001. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 15: 1688-1705.
109. Merrill BJ, Pasolli HA, Polak L, Rendl M, Garcia-Garcia MJ, Anderson KV, Fuchs E. 2004. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131: 263-274.
110. Mieszczanek J, de la Roche M, Bienz M. 2008. A role of Pygopus as an anti-repressor in facilitating Wnt-dependent transcription. Proc Natl Acad Sci 105: 19324-19329.
111. Mikels AJ, Nusse R. 2006. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
112. Mizumoto K, Sawa H. 2007. Cortical β-catenin and APC regulate asymmetric nuclear β-catenin localization during asymmetric cell division in C. elegans. Dev Cell 12: 287-299.
113. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O, Clevers H. 1996. XTcf-3 transcription factor mediates β-catenininduced axis formation in Xenopus embryos. Cell 86: 391-399.
114. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. 1997. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 275: 1787-1790.
115. Mosimann C, Hausmann G, Basler K. 2009. β-Catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 10: 276-286.
116. Murphy LL, Hughes CC. 2002. Endothelial cells stimulate T cell NFAT nuclear translocation in the presence of cyclosporin A: involvement of the wnt/glycogen synthase kinase-3β pathway. J Immunol 169: 3717-3725.
117. Nateri AS, Spencer-Dene B, Behrens A. 2005. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285.
118. Nelson WJ, Nusse R. 2004. Convergence of Wnt, β-catenin, and cadherin pathways. Science 303: 1483-1487.
119. Neumuller RA, Knoblich JA. 2009. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23: 2675-2699.
120. Nguyen H, Rendl M, Fuchs E. 2006. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 127: 171-183.
121. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, Pasolli HA, Fuchs E. 2009. Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 41: 1068-1075.
122. Nichols J, Smith A. 2009. Naive and primed pluripotent states. Cell Stem Cell 4: 487-492.
123. Niemann C, Owens DM, Hulsken J, Birchmeier W, Watt FM. 2002. Expression of DNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours. Development 129: 95-109.
124. Noordermeer J, Klingensmith J, Perrimon N, Nusse R. 1994. dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature 367: 80-83.
125. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, et al. 2003. The receptor tyrosine kinase Ror2 is involved in noncanonical Wnt5a/JNK signalling pathway. Genes Cells 8: 645-654.
126. Owraghi M, Broitman-Maduro G, Luu T, Roberson H, Maduro MF. 2010. Roles of the Wnt effector POP-1/TCF in the C. elegans endomesoderm specification gene network. Dev Biol 340: 209-221.
127. Palmer HG, Anjos-Afonso F, Carmeliet G, Takeda H, Watt FM. 2008. The vitamin D receptor is a Wnt effector that controls hair follicle differentiation and specifies tumor type in adult epidermis. PLoS ONE 3: e1483.
128. Pardo M, Lang B, Yu L, Prosser H, Bradley A, Babu MM, Choudhary J. 2010. An expanded Oct4 interaction network: implications for stem cell biology, development, and disease. Cell Stem Cell 6: 382-395.
129. Pereira L, Yi F, Merrill BJ. 2006. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 26: 7479-7491.
130. Petersson M, Brylka H, Kraus A, John S, Rappl G, Schettina P, Niemann C. 2011. TCF/Lef1 activity controls establishment of diverse stem and progenitor cell compartments in mouse epidermis. EMBO J 30: 3004-3018.
131. Pinto D, Gregorieff A, Begthel H, Clevers H. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev 17: 1709-1713.
132. Poulson ND, Lechler T. 2010. Robust control of mitotic spindle orientation in the developing epidermis. J Cell Biol 191: 915-922. Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG,
133. Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG, Jenkins NA, Nathans J. 1997. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci 94: 2859-2863.
134. Ren H, Zhang H. 2010. Wnt signaling controls temporal identities of seam cells in Caenorhabditis elegans. Dev Biol 345: 144-155.
135. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL. 2003. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414.
136. Ring A, Kim YM, Kahn M. 2014. Wnt/catenin signaling in adult stem cell physiology and disease. Stem Cell Rev doi: 10.1007/s12015-014-9515-2.
137. Ritsma L, Ellenbroek SI, Zomer A, Snippert HJ, de Sauvage FJ, Simons BD, Clevers H, van Rheenen J. 2014. Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging. Nature 507: 362-365.
138. Roose J, Molenaar M, Peterson J, Hurenkamp J, Brantjes H, Moerer P, van de Wetering M, Destree O, Clevers H. 1998. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395: 608-612.
139. Sangiorgi E, Capecchi MR. 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920.
140. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. 2004. 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.
141. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
142. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418.
143. Schambony A, Wedlich D. 2007. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev Cell 12: 779-792.
144. Shah S, Islam MN, Dakshanamurthy S, Rizvi I, Rao M, Herrell R, Zinser G, Valrance M, Aranda A, Moras D, et al. 2006. The molecular basis of vitamin D receptor and β-catenin crossregulation. Mol Cell 21: 799-809.
145. 2+ flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 161: 769-777.
146. Shy BR, Wu CI, Khramtsova GF, Zhang JY, Olopade OI, Goss KH, Merrill BJ. 2013. Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt/β-catenin signaling. Cell Reports 4: 1-9.
147. Sokol SY. 2011. Maintaining embryonic stem cell pluripotency with Wnt signaling. Development 138: 4341-4350.
148. Song LN, Herrell R, Byers S, Shah S, Wilson EM, Gelmann EP. 2003. β-Catenin binds to the activation function 2 region of the androgen receptor and modulates the effects of the Nterminal domain and TIF2 on ligand-dependent transcription. Mol Cell Biol 23: 1674-1687.
149. Sugimura R, He XC, Venkatraman A, Arai F, Box A, Semerad C, Haug JS, Peng L, Zhong XB, Suda T, et al. 2012. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 150: 351-365.
150. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
151. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
152. Takemaru KI, Moon RT. 2000. The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J Cell Biol 149: 249-254.
153. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH, Yang H, Lim B. 2008. 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.
154. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X. 2000. LDL-receptorrelated proteins in Wnt signal transduction. Nature 407: 530-535.
155. ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, Eroglu E, Siu RK, Nusse R. 2011. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 13: 1070-1075.
156. Thompson B, Townsley F, Rosin-Arbesfeld R, Musisi H, Bienz M. 2002. A new nuclear component of the Wnt signalling pathway. Nat Cell Biol 4: 367-373.
157. Tian H, Biehs B, Warming S, Leong KG, Rangell L, Klein OD, de Sauvage FJ. 2011. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478: 255-259.
158. Townsley FM, Cliffe A, Bienz M. 2004. Pygopus and Legless target Armadillo/β-catenin to the nucleus to enable its transcriptional co-activator function. Nat Cell Biol 6: 626-633.
159. Trompouki E, Bowman TV, Lawton LN, Fan ZP, Wu DC, DiBiase A, Martin CS, Cech JN, Sessa AK, Leblanc JL, et al. 2011. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 147: 577-589.
160. Valenta T, Lukas J, Korinek V. 2003. HMG box transcription factor TCF-4's interaction with CtBP1 controls the expression of the Wnt target Axin2/Conductin in human embryonic kidney cells. Nucleic Acids Res 31: 2369-2380.
161. Van Camp JK, Beckers S, Zegers D, Van Hul W. 2014. Wnt signaling and the control of human stem cell fate. Stem Cell Rev 10: 207-229.
162. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, Demmers J, Chambers I, Poot RA. 2010. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6: 369-381.
163. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, et al. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88: 789-799.
164. van Es JH, Haegebarth A, Kujala P, Itzkovitz S, Koo BK, Boj SF, Korving J, van den Born M, van Oudenaarden A, Robine S, et al. 2012. A critical role for the Wnt effector Tcf4 in adult intestinal homeostatic self-renewal. Mol Cell Biol 32: 1918-1927.
165. Varelas X, Miller BW, Sopko R, Song S, Gregorieff A, Fellouse FA, Sakuma R, Pawson T, Hunziker W, McNeill H, et al. 2010. The Hippo pathway regulates Wnt/β-catenin signaling. Dev Cell 18: 579-591.
166. Vasioukhin V, Degenstein L, Wise B, Fuchs E. 1999. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci 96: 8551-8556.
167. Verzi MP, Hatzis P, Sulahian R, Philips J, Schuijers J, Shin H, Freed E, Lynch JP, Dang DT, Brown M, et al. 2010. TCF4 and CDX2, major transcription factors for intestinal function, converge on the same cis-regulatory regions. Proc Natl Acad Sci 107: 15157-15162.
168. Vinson CR, Conover S, Adler PN. 1989. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338: 263-264.
169. Wehrli M, Dougan ST, Caldwell K, O'Keefe L, Schwartz S, Vaizel-Ohayon D, Schejter E, Tomlinson A, DiNardo S. 2000. arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407: 527-530.
170. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, Smith A. 2011. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat Cell Biol 13: 838-845.
171. Wu CI, Hoffman JA, Shy BR, Ford EM, Fuchs E, Nguyen H, Merrill BJ. 2012. Function of Wnt/β-catenin in counteracting Tcf3 repression through the Tcf3-β-catenin interaction. Development 139: 2118-2129.
172. Yamashita YM, Yuan H, Cheng J, Hunt AJ. 2010. Polarity in stem cell division: asymmetric stem cell division in tissue homeostasis. Cold Spring Harb Perspect Biol 2: a001313.
173. Yan KS, Chia LA, Li X, Ootani A, Su J, Lee JY, Su N, Luo Y, Heilshorn SC, Amieva MR, et al. 2012. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci 109: 466-471.
174. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ. 2011. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 13: 762-770.
175. + stem cell. Nat Med 18: 618-623.
176. Zhang P, Chang WH, Fong B, Gao F, Liu C, Al Alam D, Bellusci S, Lu W. 2014. Regulation of iPS cell induction by Wnt/ β-catenin signaling. J Biol Chem 289: 9221-9232.
177. Zhou P, Byrne C, Jacobs J, Fuchs E. 1995. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9: 700-713.